From 9bd680132c7f8889de6375718aa8a32e4fa026d9 Mon Sep 17 00:00:00 2001 From: mugdhapolimera <35502000+mugdhapolimera@users.noreply.github.com> Date: Mon, 30 Sep 2024 13:34:21 -0400 Subject: [PATCH] Modified read-in of pubdate in JATS parser (#133) * correctly input pubdate for jats * formatting fixes: * modified electronic vs print date condition * added detagging to license field in jats * updated list of accepted date types * updating rebase * adding missing tests in jats --------- Co-authored-by: Mugdha Polimera Co-authored-by: Mugdha Polimera --- adsingestp/parsers/base.py | 1 + adsingestp/parsers/jats.py | 13 +- ...ts_nature_41467_2023_Article_40261_nlm.xml | 415 +- .../jats_nature_article_pubdatetype_1.xml | 2552 ++++++++++ .../input/jats_nature_natsd_12_7375.xml | 3101 +++++++++++- .../jats_springer_article_pubdatetype_2.xml | 4415 +++++++++++++++++ tests/stubdata/output/jats_a+a_subtitle.json | 8 +- tests/stubdata/output/jats_apj_967_1_35.json | 2 +- .../output/jats_iop_blank_affil_removed.json | 2 +- .../output/jats_iop_blank_affil_removed2.json | 2 +- .../output/jats_iop_jinst_17_05_P05009.json | 2 +- .../output/jats_iop_no_orcid_tag.json | 2 +- .../output/jats_iop_preprint_in_record.json | 2 +- .../stubdata/output/jats_iucr_d-60-02355.json | 2 +- .../stubdata/output/jats_iucr_d-75-00616.json | 2 +- ...s_nature_41467_2023_Article_40261_nlm.json | 8 +- .../jats_nature_article_pubdatetype_1.json | 310 ++ .../output/jats_nature_natsd_12_7375.json | 110 +- .../output/jats_no_issue_pagecount.json | 8 +- .../jats_springer_Article_collab_nlm.json | 10 +- ...jats_springer_EPJC_s10052-023-11699-1.json | 10 +- ...jats_springer_EPJC_s10052-023-11733-2.json | 10 +- .../jats_springer_JHEP_JHEP07_2023_200.json | 10 +- ...ats_springer_NatCo_s41467-023-40272-3.json | 10 +- ...ats_springer_Natur_s41598-023-38673-x.json | 10 +- ...inger_SoPh_s11207-023-02231-5_mathtex.json | 2 +- .../jats_springer_article_pubdatetype_2.json | 313 ++ .../output/jats_springer_cldy_84_1543.json | 8 +- .../output/jats_springer_jhep_2022_05_05.json | 10 +- tests/test_jats.py | 2 + 30 files changed, 11267 insertions(+), 85 deletions(-) create mode 100644 tests/stubdata/input/jats_nature_article_pubdatetype_1.xml create mode 100644 tests/stubdata/input/jats_springer_article_pubdatetype_2.xml create mode 100644 tests/stubdata/output/jats_nature_article_pubdatetype_1.json create mode 100644 tests/stubdata/output/jats_springer_article_pubdatetype_2.json diff --git a/adsingestp/parsers/base.py b/adsingestp/parsers/base.py index c531559..ad6f210 100644 --- a/adsingestp/parsers/base.py +++ b/adsingestp/parsers/base.py @@ -508,6 +508,7 @@ class BaseBeautifulSoupParser(IngestBase): "comments": HTML_TAGS_MATH + HTML_TAGS_HTML + ["a", "pre", "br", "p"], "affiliations": ["email", "orcid"], "keywords": HTML_TAGS_HTML, + "license": HTML_TAGS_MATH + HTML_TAGS_HTML + ["a", "pre", "br"], } HTML_TAGS_DANGER = ["php", "script", "css"] diff --git a/adsingestp/parsers/jats.py b/adsingestp/parsers/jats.py index 7b91f67..d8ee058 100644 --- a/adsingestp/parsers/jats.py +++ b/adsingestp/parsers/jats.py @@ -938,21 +938,27 @@ def _parse_pubdate(self): for d in pub_dates: pub_format = d.get("publication-format", "") pub_type = d.get("pub-type", "") + date_type = d.get("date-type", "") + accepted_date_types = ["pub", "", "first_release"] pubdate = self._get_date(d) if ( pub_format == "print" or pub_type == "ppub" or pub_type == "cover" or (pub_type == "" and pub_format == "") - ): + ) and (date_type == "pub" or date_type == ""): self.base_metadata["pubdate_print"] = pubdate + if ( pub_format == "electronic" or pub_type == "epub" or (pub_type == "" and pub_format == "") - ): + ) and (date_type in accepted_date_types): self.base_metadata["pubdate_electronic"] = pubdate + elif (date_type != "pub") and (date_type != ""): + self.base_metadata["pubdate_other"] = [{"type": date_type, "date": pubdate}] + if pub_type == "open-access": self.base_metadata.setdefault("openAccess", {}).setdefault("open", True) @@ -969,7 +975,8 @@ def _parse_permissions(self): license_text = p.find("license-p") if license_text: self.base_metadata.setdefault("openAccess", {}).setdefault( - "license", license_text.get_text() + "license", + self._detag(license_text.get_text(), self.HTML_TAGSET["license"]).strip(), ) license_uri = license_text.find("ext-link") if license_uri: diff --git a/tests/stubdata/input/jats_nature_41467_2023_Article_40261_nlm.xml b/tests/stubdata/input/jats_nature_41467_2023_Article_40261_nlm.xml index 56f2c04..f85c792 100644 --- a/tests/stubdata/input/jats_nature_41467_2023_Article_40261_nlm.xml +++ b/tests/stubdata/input/jats_nature_41467_2023_Article_40261_nlm.xml @@ -1 +1,414 @@ -
4146710.1038/41467.2041-1723Nature CommunicationsNat Commun2041-1723Nature Publishing Group UKLondons41467-023-40261-64026110.1038/s41467-023-40261-6Author Correction/631/114/1564/631/114/2404/631/1647/328/2238author-correctionAuthor Correction: Super-resolved trajectory-derived nanoclustering analysis using spatiotemporal indexinghttp://orcid.org/0000-0002-6515-9157WallisTristan P.1aJiangAnmin1YoungKyle2HouHuiyi1http://orcid.org/0000-0003-3094-438XKudoKye1McCannAlex J.1DurisicNela3http://orcid.org/0000-0002-4533-0455JoensuuMerja15http://orcid.org/0000-0001-6981-4350OelzDietmar2NguyenHien2http://orcid.org/0000-0003-1604-0253GormalRachel S.1mhttp://orcid.org/0000-0001-6400-1107MeunierFrédéric A.14ngrid.1003.20000 0000 9320 7537Clem Jones Centre for Ageing Dementia Research, Queensland Brain InstituteThe University of Queensland4072BrisbaneQLDAustraliagrid.1003.20000 0000 9320 7537School of Mathematics and PhysicsThe University of Queensland4072BrisbaneQLDAustraliagrid.1003.20000 0000 9320 7537Queensland Brain InstituteThe University of Queensland4072BrisbaneQLDAustraliagrid.1003.20000 0000 9320 7537School of Biomedical SciencesThe University of Queensland4072BrisbaneQLDAustraliagrid.1003.20000 0000 9320 7537Australian Institute for Bioengineering and NanotechnologyThe University of Queensland4072BrisbaneQLDAustraliat.wallis@uq.edu.aur.gormal@uq.edu.auf.meunier@uq.edu.au2572023122023141446820720232572023© The Author(s) 20232023Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.publisher-imprint-nameNature Portfoliovolume-issue-count1issue-article-count4468issue-toc-levels0issue-pricelist-year2023issue-copyright-holderSpringer Nature Limitedissue-copyright-year2023article-contains-esmNoarticle-numbering-styleUnnumberedarticle-registration-date-year2023article-registration-date-month7article-registration-date-day20article-toc-levels0toc-levels0volume-typeRegularjournal-productNonStandardArchiveJournalnumbering-styleUnnumberedarticle-grants-typeOpenChoicemetadata-grantOpenAccessabstract-grantOpenAccessbodypdf-grantOpenAccessbodyhtml-grantOpenAccessbibliography-grantOpenAccessesm-grantOpenAccessonline-firstfalsepdf-file-referenceBodyRef/PDF/41467_2023_Article_40261.pdfpdf-typeTypesettarget-typeOnlinePDFissue-typeRegulararticle-typeErratumjournal-subject-primaryScience, Humanities and Social Sciences, multidisciplinaryjournal-subject-secondaryScience, Humanities and Social Sciences, multidisciplinaryjournal-subject-secondaryScience, multidisciplinaryjournal-subject-collectionScience (multidisciplinary)open-accesstrue

The original article can be found online at https://doi.org/10.1038/s41467-023-38866-y.

Correction to: Nature Communicationshttps://doi.org/10.1038/s41467-023-38866-y, published online 08 June 2023

In this article the grant number R21AG080435 relating to the National Institute on Aging of the National Institutes of Health for Frédéric A. Meunier was omitted. The original article has been corrected.

+ + +
+ + + + 41467 + 10.1038/41467.2041-1723 + + Nature Communications + Nat Commun + + 2041-1723 + + Nature Publishing Group UK + London + + + + s41467-023-40261-6 + 40261 + 10.1038/s41467-023-40261-6 + + + Author Correction + + + /631/114/1564 + + + /631/114/2404 + + + /631/1647/328/2238 + + + author-correction + + + + Author Correction: Super-resolved trajectory-derived nanoclustering analysis using spatiotemporal indexing + + + + http://orcid.org/0000-0002-6515-9157 + + Wallis + Tristan P. + + 1 + a + + + + Jiang + Anmin + + 1 + + + + Young + Kyle + + 2 + + + + Hou + Huiyi + + 1 + + + http://orcid.org/0000-0003-3094-438X + + Kudo + Kye + + 1 + + + + McCann + Alex J. + + 1 + + + + Durisic + Nela + + 3 + + + http://orcid.org/0000-0002-4533-0455 + + Joensuu + Merja + + 1 + 5 + + + http://orcid.org/0000-0001-6981-4350 + + Oelz + Dietmar + + 2 + + + + Nguyen + Hien + + 2 + + + http://orcid.org/0000-0003-1604-0253 + + Gormal + Rachel S. + + 1 + m + + + http://orcid.org/0000-0001-6400-1107 + + Meunier + Frédéric A. + + 1 + 4 + n + + + + + grid.1003.2 + 0000 0000 9320 7537 + Clem Jones Centre for Ageing Dementia Research, Queensland Brain Institute + The University of Queensland + + 4072 + Brisbane + QLD + Australia + + + + + grid.1003.2 + 0000 0000 9320 7537 + School of Mathematics and Physics + The University of Queensland + + 4072 + Brisbane + QLD + Australia + + + + + grid.1003.2 + 0000 0000 9320 7537 + Queensland Brain Institute + The University of Queensland + + 4072 + Brisbane + QLD + Australia + + + + + grid.1003.2 + 0000 0000 9320 7537 + School of Biomedical Sciences + The University of Queensland + + 4072 + Brisbane + QLD + Australia + + + + + grid.1003.2 + 0000 0000 9320 7537 + Australian Institute for Bioengineering and Nanotechnology + The University of Queensland + + 4072 + Brisbane + QLD + Australia + + + + + + t.wallis@uq.edu.au + + + + r.gormal@uq.edu.au + + + + f.meunier@uq.edu.au + + + + 25 + 7 + 2023 + + + 12 + 2023 + + 14 + 1 + 4468 + + + 20 + 7 + 2023 + + + 25 + 7 + 2023 + + + + © The Author(s) 2023 + 2023 + + + Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit + http://creativecommons.org/licenses/by/4.0/. + + + + + + + publisher-imprint-name + Nature Portfolio + + + volume-issue-count + 1 + + + issue-article-count + 4468 + + + issue-toc-levels + 0 + + + issue-pricelist-year + 2023 + + + issue-copyright-holder + Springer Nature Limited + + + issue-copyright-year + 2023 + + + article-contains-esm + No + + + article-numbering-style + Unnumbered + + + article-registration-date-year + 2023 + + + article-registration-date-month + 7 + + + article-registration-date-day + 20 + + + article-toc-levels + 0 + + + toc-levels + 0 + + + volume-type + Regular + + + journal-product + NonStandardArchiveJournal + + + numbering-style + Unnumbered + + + article-grants-type + OpenChoice + + + metadata-grant + OpenAccess + + + abstract-grant + OpenAccess + + + bodypdf-grant + OpenAccess + + + bodyhtml-grant + OpenAccess + + + bibliography-grant + OpenAccess + + + esm-grant + OpenAccess + + + online-first + false + + + pdf-file-reference + BodyRef/PDF/41467_2023_Article_40261.pdf + + + pdf-type + Typeset + + + target-type + OnlinePDF + + + issue-type + Regular + + + article-type + Erratum + + + journal-subject-primary + Science, Humanities and Social Sciences, multidisciplinary + + + journal-subject-secondary + Science, Humanities and Social Sciences, multidisciplinary + + + journal-subject-secondary + Science, multidisciplinary + + + journal-subject-collection + Science (multidisciplinary) + + + open-access + true + + + + + +

The original article can be found online at + https://doi.org/10.1038/s41467-023-38866-y. +

+ + + + +

Correction to: + Nature Communications + https://doi.org/10.1038/s41467-023-38866-y, published online 08 June 2023 +

+

In this article the grant number R21AG080435 relating to the National Institute on Aging of the National Institutes of Health for Frédéric A. Meunier was omitted. The original article has been corrected.

+ +
diff --git a/tests/stubdata/input/jats_nature_article_pubdatetype_1.xml b/tests/stubdata/input/jats_nature_article_pubdatetype_1.xml new file mode 100644 index 0000000..027c54b --- /dev/null +++ b/tests/stubdata/input/jats_nature_article_pubdatetype_1.xml @@ -0,0 +1,2552 @@ + + +
+ + + + 41467 + 10.1038/41467.2041-1723 + + Nature Communications + Nat Commun + + 2041-1723 + + Nature Publishing Group UK + London + + + + s41467-024-48265-6 + 48265 + 10.1038/s41467-024-48265-6 + + + Article + + + /639/638/403/933 + + + /639/638/549/933 + + + /639/638/77/884 + + + /140/131 + + + /140/146 + + + article + + + + Carbon–nitrogen transmutation in polycyclic arenol skeletons to access + N-heteroarenes + + + + + http://orcid.org/0000-0003-3131-4558 + + Lu + Hong + + 1 + + + + Zhang + Yu + + 1 + + + + Wang + Xiu-Hong + + 1 + + + + Zhang + Ran + + 1 + + + http://orcid.org/0000-0002-5746-758X + + Xu + Peng-Fei + + 2 + e + + + http://orcid.org/0000-0002-7951-683X + + Wei + Hao + + 1 + f + + + + + https://ror.org/00z3td547 + grid.412262.1 + 0000 0004 1761 5538 + Key Laboratory of Synthetic and Natural Functional Molecule of the Ministry of Education, College of Chemistry & Materials Science + Northwest University + + 710069 + Xi’an + China + + + + + grid.32566.34 + 0000 0000 8571 0482 + State Key Laboratory of Applied Organic Chemistry, College of Chemistry and Chemical Engineering + Lanzhou University + + 730000 + Lanzhou + China + + + + + + xupf@lzu.edu.cn + + + + haow@nwu.edu.cn + + + + 4 + 5 + 2024 + + + 12 + 2024 + + 15 + 1 + 3772 + + + 26 + 4 + 2024 + + + 29 + 1 + 2024 + + + 25 + 4 + 2024 + + + 4 + 5 + 2024 + + + + © The Author(s) 2024 + 2024 + + + Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit + http://creativecommons.org/licenses/by/4.0/. + + + + + + Abstract +

Developing skeletal editing tools is not a trivial task, and realizing the corresponding single-atom transmutation in a ring system without altering the ring size is even more challenging. Here, we introduce a skeletal editing strategy that enables polycyclic arenols, a highly prevalent motif in bioactive molecules, to be readily converted into + N-heteroarenes through carbon–nitrogen transmutation. The reaction features selective nitrogen insertion into the C–C bond of the arenol frameworks by azidative dearomatization and aryl migration, followed by ring-opening, and ring-closing (ANRORC) to achieve carbon-to-nitrogen transmutation in the aromatic framework of the arenol. Using widely available arenols as + N-heteroarene precursors, this alternative approach allows the streamlined assembly of complex polycyclic heteroaromatics with broad functional group tolerance. Finally, pertinent transformations of the products, including synthesis complex biheteroarene skeletons, were conducted and exhibited significant potential in materials chemistry. +

+ + +

Developing skeletal editing tools, especially to realize the single-atom transmutation in a ring system without altering the ring size is challenging. Here, the authors introduce a skeletal editing strategy that enables polycyclic arenols to be readily converted into + N-heteroarenes through carbon–nitrogen transmutation. +

+ + + + + + National Natural Science Foundation of China (National Science Foundation of China) + https://doi.org/10.13039/501100001809 + + + 21971205 + 22271231 + + + Wei + Hao + + + + + Wei + Hao + + + + + + + Natural Science Basic Research Plan for Distinguished Young Scholars in Shaanxi Province of China (2022JC-08) + + + + + + + Natural Science Basic Research Plan in Shaanxi Province of China (2023-JC-YB-126) + + + + + + + publisher-imprint-name + Nature Portfolio + + + volume-issue-count + 1 + + + issue-article-count + 4297 + + + issue-toc-levels + 0 + + + issue-pricelist-year + 2024 + + + issue-copyright-holder + Springer Nature Limited + + + issue-copyright-year + 2024 + + + article-contains-esm + Yes + + + article-numbering-style + Unnumbered + + + article-registration-date-year + 2024 + + + article-registration-date-month + 4 + + + article-registration-date-day + 26 + + + article-toc-levels + 0 + + + toc-levels + 0 + + + volume-type + Regular + + + journal-product + NonStandardArchiveJournal + + + numbering-style + Unnumbered + + + article-grants-type + OpenChoice + + + metadata-grant + OpenAccess + + + abstract-grant + OpenAccess + + + bodypdf-grant + OpenAccess + + + bodyhtml-grant + OpenAccess + + + bibliography-grant + OpenAccess + + + esm-grant + OpenAccess + + + online-first + false + + + pdf-file-reference + BodyRef/PDF/41467_2024_Article_48265.pdf + + + pdf-type + Typeset + + + target-type + OnlinePDF + + + issue-type + Regular + + + article-type + OriginalPaper + + + journal-subject-primary + Science, Humanities and Social Sciences, multidisciplinary + + + journal-subject-secondary + Science, Humanities and Social Sciences, multidisciplinary + + + journal-subject-secondary + Science, multidisciplinary + + + journal-subject-collection + Science (multidisciplinary) + + + open-access + true + + + + +

These authors contributed equally: Hong Lu, Yu Zhang.

+ + + + + Introduction +

Organic synthesis underpins the evolution and advancement of broad areas of science, from materials to medicine. Arenes are among the most widely used rings in medicine and natural products. The functionalization of arenes is a particularly attractive tool for the production of pharmaceuticals, natural products, and molecular materials + + 1– + 4 + . However, their application has so far been largely focused on C–H functionalization chemistry (peripheral editing), and the precise modification of the aromatic ring skeleton remains largely unexplored (Fig.  + 1A) + + 5– + 7 + . Single-atom skeletal editing has become an extremely powerful tool for straightforwardly modifying the core skeleton of organic molecules. Recently, a limited number of single–atom insertion or deletion reactions have been developed to reshape the underlying molecular skeletons + + 8– + 21 + . However, the direct modification of valuable core structures by replacing one atom in a ring system without changing the ring size and aromaticity remains elusive + + 22– + 31 + , although it has been recognized as a highly desirable transformation. + + + + Examples of carbon–nitrogen transmutation and our reaction design. +

+ A Molecular editing of aromatic rings. + B Examples of the necessary nitrogen atom effect. + C Conversion of aryl azides to pyridines. + D This study. +

+ +

+ +

+ +

+

One of the most studied among + N-heteroarenes are pyridines, which serve as a bioisosteric replacement of benzene counterparts within the parent molecules + + 32– + 34 + . The replacement of carbon with nitrogen in aromatic ring systems can have several important effects on the molecular and physicochemical properties relevant to multiparameter optimization (Fig.  + 1B). This necessary nitrogen atom effect is a versatile high-impact design element for multiparameter optimization, which has been shown to improve various key pharmacological parameters + + 35 + . Recently, Burns and Levin independently reported groundbreaking methods for the direct conversion of arenes to pyridines via nitrene internalization (Fig.  + 1C) + + 36, + 37 + . In these process, additional steps for installation and isolation of aryl azides are always requried, which indicated that a selective, and straightforward transformation of diverse arenes into + N-heteroarenes remains an important goal + + 38 + . +

+

A key challenge in this transformation is the stability of the aromatic compounds. Our design overcomes this intrinsic challenge using arenols as substrates. Dearomatization of arenols disrupts the stability of the aromatic ring and promotes subsequent skeletal transformations + + 39– + 48 + . Arenol can also act as a selectivity controlling element in site-selective skeletal editing. Our group’s recent work employing this dearomative strategy to promote ring expansion of arenols inspired us to continue investigating this strategy to more complex skeletal editing transformation + + 49 + . In this work, we describe the direct carbon-to-nitrogen transmutations in arenols. This reaction involves two stages: ring expansion and contraction (Fig.  + 1D). In the first stage, the insertion of nitrogen atoms is achieved by azidative dearomatization of an arenol and intramolecular aryl migration. In the second stage, a carbon atom moves out of the ring skeleton through ring-opening, and ring-closing (ANRORC), which ultimately furnishes desired carbon–nitrogen transmutation in polycyclic arenol skeletons + + 50– + 52 + . +

+ + + Results + + Reaction optimization +

We began our investigation using methylphenanthren-9-ol + 1a as the reaction partner. (PhO) + 2POOH, NBS, and N( + nBu) + 4N + 3 were employed as reagents for the in situ formation of the azido ketone intermediate (see Supplementary Information, section  + 2.2.2). For optimization, we observed the formation of desired product + 1 in 80% yield using FeBr + 2 and Cy + 3PO as an effective catalyst–ligand combination in PhCl (Table  + 1, entry 1). A control experiment revealed that an iron salt was essential for obtaining the desired product (Table  + 1, entry 2). Other iron salts, including FeCl + 2, Fe(OTf) + 2, Fe(OAc) + 2, and Fe(acac) + 3, exhibited lower efficiency than inexpensive FeBr + 2 (Table  + 1, entries 3 − 6). Furthermore, when other established metal nitrenoid formation catalysts, including copper, rhodium, cobalt, and ruthenium, were used, the desired product was not obtained satisfyingly (Table  + 1, entries 7–10) + + 53, + 54 + . Further optimization showed that this reaction was slightly improved using Cy + 3PO (Table  + 1, entry 11). The reaction appeared to be less sensitive to solvents, as replacing the PhCl with either toluene or THF furnished + 1 in good yield (Table  + 1, entries 12 and 13). The yield decreased slightly when 10 mol% FeBr + 2 and 15 mol% Cy + 3PO were used (Table  + 1, entry 14). + + + +

Screening of reaction conditions. + a +

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+

+ +

+
+

Entry

+ 		+

Variation from ‘ + standard conditions’ +

+ 		+

Yield (%) + b +

+
+

1

+ 		+

None

+ 		+

80 (61) + c +

+
+

2

+ 		+

w/o FeBr + 2 +

+ 		+

trace

+
+

3

+ 		+

FeCl + 2 instead of FeBr + 2 +

+ 		+

71

+
+

4

+ 		+

Fe(OTf) + 2 instead of FeBr + 2 +

+ 		+

75

+
+

5

+ 		+

Fe(OAc) + 2 instead of FeBr + 2 +

+ 		+

32

+
+

6

+ 		+

Fe(acac) + 3 instead of FeBr + 2 +

+ 		+

10

+
+

7

+ 		+

Cu(OTf) + 2 instead of FeBr + 2 +

+ 		+

<10

+
+

8

+ 		+

[[CH + 3(CH + 2) + 6CO + 2] + 2Rh] + 2 instead of FeBr + 2 +

+ 		+

34

+
+

9

+ 		+

TMOPP-Co instead of FeBr + 2 +

+ 		+

trace

+
+

10

+ 		+

Ru + 3(CO) + 13 instead of FeBr + 2 +

+ 		+

<10

+
+

11

+ 		+

w/o Cy + 3PO +

+ 		+

70

+
+

12

+ 		+

In toluene

+ 		+

75

+
+

13

+ 		+

In THF

+ 		+

70

+
+

14

+ 		+

10 mol% FeBr + 2 and 15 mol% Cy + 3PO instead +

+ 		+

61

+
+ +

+ aUnless otherwise specified, all reactions were carried out using + 1a (0.1 mmol), NBS (0.18 mmol), N( + nBu + 4)N + 3 (0.3 mmol), (PhO) + 2POOH (0.075 mmol), FeBr + 2 (0.015 mmol), and Cy + 3PO (0.02 mmol) in PhCl (1.0 mL) at 100 °C for 36 h. +

+

+ bIsolated yields after chromatography. +

+

+ cScale-up reaction by using 1.0 mmol of + 1a. +

+ + +

+ + + Substrate scope +

Considering the optimal reaction conditions, the substrate scope was determined (Fig.  + 2). Various arenols, including phenanthrol ( + 1– + 10), naphthol ( + 11– + 30), anthranol ( + 33) benzo( + a)anthranol ( + 34), and benzo[ + c]phenanthrol ( + 35), can effectively undergo the desired carbon–nitrogen transmutation. Both electron-rich and electron-deficient aromatic substrates were suitable for the process. It was found that the substituents at the + ortho positions of the arenol are significant. When the substituent was an alkyl group, the corresponding arenols underwent atom transmutation smoothly in moderate-to-good yield and chemoselectivity. The presence of a phenyl group or an electron-withdrawing group such as CO + 2Me at the + ortho-position can inhibit this reaction. However, various functional groups, such as ether ( + 4 and + 5), acetals ( + 6 and + 16), aryl halides ( + 7, + 8, + 17 and + 18), esters ( + 9), trifluoromethyl ( + 10), trimethylsilyl (TMS) ( + 19), alkenes ( + 20), and alkynes ( + 21), were tolerated in this transformation. In addition, several naphthyl-fused rings ( + 22– + 25) were suitable substrates, affording the desired products in moderate-to-good yields. Heterocyclic moieties such as benzofuran ( + 26), furan ( + 27), dibenzofuran ( + 28), quinoline ( + 29), and phenoxathiine ( + 30) were also compatible. Moreover, fused heteroarenols such as naphtho[1,2- + b]thiophene ( + 31) and naphtho[1,2- + b]furan ( + 32) can be incorporated, providing pharmaceutically interesting fused-ring skeletons that are non-trivial to prepare. The structures of + 3 and + 35 were identified using X-ray crystallography. + + + + Substrate scope of the carbon–nitrogen transmutation in polycyclic arenol. +

+ a,b aIsolated yields after chromatography are shown.  + b Reaction conditions: substrate (0.1 mmol), NBS (0.18 mmol), N( + nBu + 4)N + 3 (0.3 mmol), (PhO) + 2POOH (0.075 mmol), FeBr + 2 (0.015 mmol), and Cy + 3PO (0.02 mmol) in PhCl (1.0 mL) at 100 °C for 36 h. +

+ +

+ +

+ +

+ + + Synthetic utility +

The successful development of the atom transmutation protocol offers a rapid and modular approach to access complex biheteroarene skeleton, a common structural motif found in bioactive compounds (Fig. 3A). Compound + 37 could be easily transformed to the iridium complexes + 39, which could serve as the red-light-emitting electrochemical cell + + 55, + 56 + . Next, the synthetic versatility of the C-to-N transmutation was demonstrated through the preparation of 3,6-disubstituted quinolines + 42, which could not be obtained from directly electrophilic substitution of quinolines (Fig.  + 3B). Specifically, the successful development of the carbon–nitrogen transmutation offers exciting opportunities to devise more complex skeletal editing transformations via combinations of atom insertions and deletions. Benzo[1,4]diazepine + 43 can be accessed through a C–H azidation and aryl migration sequence from + 11, presently the formal carbon deletion and two nitrogen insertion products of starting naphthol + 11a (Fig.  + 3C). + + + + Application potential of carbon–nitrogen transmutation. +

+ A Applications that allow access to complex biheteroarene skeletons. + B Preparation of unconventionally 3,6-substituted quinolines. + C Sequential skeletal editing transformations of naphthol. +

+ +

+ +

+ +

+ + + Mechanistic considerations +

To elucidate the mechanism of this transformation, series control experiments were first conducted. The reactions without addition of NBS or N( + nBu + 4)N + 3 failed to produce the desired product (Fig.  + 4A, equations 1 and 2). And trace amount of + 11 was observed when (PhO) + 2POOH was absent from the reaction mixture (Fig.  + 4A, equation 3). It’s worth noting that azide ketone + 44 could be isolated in 73% yield in the absense of Fe catalyst after 2 h (Fig.  + 4A, equation 4). These results indicated that the proposed azidative dearomatization of arenol might be involved (Fig.  + 1D) + + 57 + . The azide ketone + 44 was then tested with and without the addition of the Fe catalyst (Fig.  + 4B). It was found that the desired product + 11 was formed in 40% yield, and 35% yield of + 11a was isolated in presence of Fe catalyst, which demonstrated that the proposed azidation is a reversible process via successive single-electron transfer (SET) from Fe(II) to eliminate azide + + 58 + . On the contrary, only trace amount of product + 11 and + 11a was observed without Fe catalyst. And a byproduct + 45 was detected in 42% yield and recovered + 44 in 24% + + 59 + . These results revealed that the Fe catalyst is not only involved in aryl migration, but is also essential for the ring contraction process + + 60 + . + + + + Mechanistic studies. +

+ A Control experiments. + B Control experiments using azide intermediate showing that Fe catalyst is essential for aryl migration and ring contraction process. + C Proposed mechanism. +

+ +

+ +

+ +

+

Based on the literature reports and our observations, a plausible mechanism is proposed (Fig.  + 4C). Initially, the + N-bromosuccinimide-mediated dearomatization of the corresponding naphthol of + 11a afforded the brominated ketone intermediate + A, which subsequently reacted with N( + nBu) + 4N + 3 to generate azido ketone + B. Then iron salt reacted with + B can form metal−nitrene species, which would then undergo 1,2-aryl migration to form ring expansion intermediate + C. Subsequently, addition of hydroxide anion to the imine group of + C induces + N, + O-hemiketal + D. The collapse of + D with assistance of iron salt produces ring-opening amino-ketone intermediate + E + + 61, + 62 + , which undergoes re-cyclization and dehydration to form stable benzoquinoline + 11 and release Fe catalyst. +

+

In conclusion, this study proposed a unique strategy that enables straightforward carbon-to-nitrogen transmutations in arenols through a one-pot ring expansion-contraction sequence. This site-selective atom transformation is based on sequentially combining three transformations in one pot using aryl migration and imine transposition as key steps and opens new opportunities for single-atom skeletal edit design. Further preparation of complex biheteroarene skeleton and unconventionally substituted quinoline highlights the potential of this study. This provides an alternative for the development of + N-heteroarenes and demonstrates significant potential in materials chemistry. +

+ + + + Methods + + General condition for carbon–nitrogen transmutation +

Substrate (0.1 mmol), NBS (0.12 mmol), N( + nBu + 4)N + 3 (0.2 mmol), FeBr + 2 (0.015 mmol), tricyclohexylphosphine oxide (0.02 mmol), (PhO) + 2POOH (0.05 mmol), and PhCl (1.0 mL) was successively added to an 10 mL sealed tube equipped with a Teflon-coated magnetic stir bar. The tube then was sealed with a Teflon screw cap and placed on a hotplate pre-heated to 100 °C with vigorous stirring. After 18 h, the reaction was cooled to room temperature and another portion of NBS (0.06 mmol, 0.6 equiv), N( + nBu + 4)N + 3 (0.1 mmol) and (PhO) + 2POOH (0.025 mmol) was successively added to the sealed tube. The tube then reacted at 100 °C with vigorous stirring. After 18 h, the reaction was cooled to room temperature. The solvent was evaporated and the residue was directly purified by flash column chromatography on silica gel (petroleum ether/ethyl acetate = 20/1) to give the desired products. +

+ + + + + + Acknowledgements +

We are grateful for the financial support from the National Natural Science Foundation of China (22271231, H.W.), Key Research and Invention Program in Shaanxi Province of China (2021SF-299, H.W.), Natural Science Basic Research Program of Shaanxi (2020JQ-574, H.L.), Scientific Research Program of Shaanxi Education Department (20JK0937, H.L.) and Northwest University.

+ + + Author contributions +

H.W. conceived and designed the project and composed the manuscript. H.L., Y.Z., X.W., and R.Z. conducted the experiments and analyzed the data. H.L. and P.X. discussed the experimental results and commented on the manuscript. H.W. conducted general guidance, project directing, and manuscript revisions.

+ + + Peer review + + Peer review information +

: + Nature Communications thanks Yuhua Deng and the other anonymous reviewer(s) for their contribution to the peer review of this work. A peer review file is available. +

+ + + + Data availability +

Data relating to the optimization studies, mechanistic studies, general methods, and the characterization data of materials and products, are available in the Supplementary Information. Crystallographic data for the structures reported in this article have been deposited at the Cambridge Crystallographic Data Center, under deposition numbers CCDC 2285580 ( + 3), 2285872 ( + 35), 2310917 ( + 39) and 2308629 ( + 45). Copies of the data can be obtained free of charge via + https://www.ccdc.cam.ac.uk/structures. All data are available from the corresponding author upon request. +

+ + + + Competing interests +

The authors declare no competing interests.

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4159810.1038/41598.2045-2322Scientific ReportsSci Rep2045-2322Nature Publishing Group UKLondons41598-022-10801-z1080110.1038/s41598-022-10801-zArticle/631/443/692/698/1671/1668/692/699/2743/137/1926articleReversal of diabetic-induced myopathy by swimming exercise in pregnant rats: a translational intervention studyCatinelliBruna B.1RossignoliPatrícia S.2FlorianoJuliana F.1CarrAline M.1de OliveiraRafael G.1dos SantosNilton J.34ÚbedaLara C. C.5SpadellaMaria Angélica6HallurRaghavendra L. S.17SobreviaLuis1891011FelisbinoSérgio L.3CalderonIracema M. P.1BarbosaAngélica M. P.12RudgeMarilza V. C.1q1The Diamater Study GroupRudgeM. V. C.1BarbosaA. M. P.12CalderonI. M. P.1SobreviaL.1891011SouzaF. P.12BerghmansB.13ThabaneL.14JungingerB.15GraeffC. F. O.16MagalhãesC. G.17CostaR. A.1LimaS. A. M.18Kron-RodriguesM. R.19FelisbinoS. L.3BarbosaW.20CamposF. J.17BossolanG.1CorrenteJ. E.21NunesH. R. C.17AbbadeJ.17RossignoliP. S.2PedroniC. R.2AtallahA. N.22Di BellaZ. I. K. J.23UchoaS. M. M.24DuarteM. A. H.25MarecoE. A.26SakalemM. E.27MartinhoN.2829HallurL. S. R.17ReyesD. R. A.1AlvesF. C. B.1MarcondesJ. P. C.1PrudencioC. B.1PinheiroF. A.1SartorãoFilhoC. I.1QuirozS. B. C. V.1PasconT.1NunesS. K.1CatinelliB. B.1ReisF. V. D. S.1OliveiraR. G.1BarnezeS.1EnriquezE. M. A.1TakanoL.1CarrA. M.1MagyoriA. B. M.1IamundoL. F.1CarvalhoC. N. F.1JacominM.1AvramidisR. E.1SilvaA. J. B.2OrlandiM. I. G.1DangióT. D.1BassinH. C. M.1TakemotoM. L. S.1CaldeirãoT. D.1SantosN. J.34LourençoI. O.12de SáJ. Marostica12CarusoI. P.12RasmussenL. T.30GarciaG. A.1NavaG. T. A.31MarquesC. P.32BussaneliD. G.33NogueiraV. K. C.33RudgeC. V. C.32PiculoF.34PrataG. M.35BarbosaV. P.36grid.410543.70000 0001 2188 478XPostgraduate Program on Tocogynecology, Department of Gynecology and Obstetrics, Botucatu Medical SchoolSão Paulo State University (UNESP)BotucatuSão PauloBrazilgrid.410543.70000 0001 2188 478XDepartment of Physiotherapy and Occupational Therapy, School of Philosophy and SciencesSão Paulo State University (UNESP)MaríliaSão PauloBrazilgrid.410543.70000 0001 2188 478XLaboratory of Extracellular Matrix Biology, Department of Structural and Functional Biology, Institute of Biosciences of BotucatuSão Paulo State University (UNESP)BotucatuSão PauloBrazilgrid.411087.b0000 0001 0723 2494Department of Structural and Functional Biology, Institute of Biology (IB), UNICAMPUniversity of Campinas (UNICAMP)CampinasSão PauloBrazilUniversity of Marília (UNIMAR)MaríliaSão PauloBrazilHuman Embryology LaboratoryMarília Medical School (FAMEMA)MaríliaSão PauloBrazilgrid.415155.10000 0001 2039 9627Pravara Institute of Medical Sciences (Deemed to be University)Loni, Rahata Taluk413736Ahmednagar DistrictMaharashtraIndiagrid.7870.80000 0001 2157 0406Cellular and Molecular Physiology Laboratory (CMPL), Department of Obstetrics, Division of Obstetrics and Gynaecology, School of Medicine, Faculty of MedicinePontificia Universidad Católica de Chile8330024SantiagoChilegrid.9224.d0000 0001 2168 1229Department of Physiology, Faculty of PharmacyUniversidad de Sevilla41012SevilleSpaingrid.1003.20000 0000 9320 7537University of Queensland Centre for Clinical Research (UQCCR), Faculty of Medicine and Biomedical SciencesUniversity of Queensland4029HerstonQLDAustraliagrid.4494.d0000 0000 9558 4598Division of Pathology, Department of Pathology and Medical BiologyUniversity of Groningen, University Medical Center Groningen (UMCG)9713GZGroningenThe Netherlandsgrid.410543.70000 0001 2188 478XDepartment of Physics, Institute of Biosciences, Letters and Exact Sciences (IBILCE), Multiuser Center for Biomolecular Innovation (CMIB)São Paulo State University “Júlio de Mesquita Filho” (UNESP)15054-000São José do Rio PretoSão PauloBrazilgrid.412966.e0000 0004 0480 1382Pelvic Care Center MaastrichtMaastricht University Medical CenterMaastrichtThe Netherlandsgrid.25073.330000 0004 1936 8227Department of Clinical Epidemiology and BiostatisticsMcMaster UniversityHamiltonONCanadagrid.6363.00000 0001 2218 4662Department of Gynecology, Pelvic Floor Center CharitéCharité University HospitalBerlinGermanygrid.410543.70000 0001 2188 478XPOSMAT-Post-Graduate Program in Materials Science and Technology, School of SciencesSão Paulo State University (UNESP)BauruSão PauloBrazilgrid.410543.70000 0001 2188 478XMedical School of BotucatuSão Paulo State University (UNESP)BotucatuSão PauloBrazilgrid.410543.70000 0001 2188 478XDepartment of Nursing, Botucatu Medical School (FMB)São Paulo State University (UNESP)BotucatuSão PauloBrazilgrid.411869.30000 0000 9186 527XStricto Sensu Graduate Program in Nursing at UNIVERITAS, Guarulhos University (UNG)GuarulhosSão PauloBrazilgrid.410543.70000 0001 2188 478XDepartment of Clinical Medicine, Botucatu Medical SchoolSão Paulo State University (UNESP)Av. Prof. Mário Rubens Guimarães Montenegro, s/n-UNESPBotucatuSão PauloBrazilgrid.410543.70000 0001 2188 478XDepartment of Biostatistics, Botucatu Institute of BiosciencesSão Paulo State University/UNESPSão Paulotistics, Botucatu Institute of BiosciencesBrazilgrid.411249.b0000 0001 0514 7202Discipline of Evidence-Based Medicine, Paulista School of Medicine-Federal University of São Paulo (EPM-UNIFESP)São PauloBrazilgrid.411249.b0000 0001 0514 7202Department of GynecologyFederal University of São Paulo, UNIFESPSão PauloBrazilgrid.441972.d0000 0001 2105 8867Department of Physical TherapyUniversidade Católica de Pernambuco (UNICAP)RecifePEBrazilgrid.11899.380000 0004 1937 0722Department of Operative Dentistry, Endodontics and Dental Materials, Bauru School of DentistryUniversity of São PauloSão PauloBrazilgrid.412294.80000 0000 9007 5698University of Western São Paulo (UNOESTE)Presidente PrudenteSão PauloBrazilgrid.411400.00000 0001 2193 3537Department of Anatomy, CCBState University of Londrina (UEL)Caixa Postal 10011Campus Universitário s/n 86057-970LondrinaParanaBrazilUniversity Center of Associated CollegesSão João da Boa VistaSão PauloBrazilgrid.441751.20000 0000 8820 7559Regional University Center of Espírito Santo do Pinhal, UNIPINHALEspírito Santo do PinhalSão PauloBrazilgrid.412296.a0000 0001 1484 3840Universidade do Sagrado Coração (USC)BauruSão PauloBrazilgrid.410543.70000 0001 2188 478XDepartment of Physical Education, Institute of Biosciences of Rio ClaroSão Paulo State University (UNESP)Rio ClaroSão PauloBrazilIndependent ResearcherAssisSão PauloBrazilgrid.410543.70000 0001 2188 478XDepartment of Morphology and Pediatric Dentistry, Araraquara School of DentistrySão Paulo State University (UNESP)Rua Humaitá, 168014801-903AraraquaraSão PauloBrazilIndependent ResearcherBotucatuSPBrazilgrid.412296.a0000 0001 1484 3840Health Sciences CenterUniversity of the Sacred Heart (USC)BauruSão PauloBrazilgrid.441895.50000 0000 9898 9056Universidade de Marília (UNIMAR)MaríliaSão PauloBrazilmarilzarudge@gmail.com5520221220221217375144202291120212932022552022© The Author(s) 20222022Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. 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Gestational diabetes mellitus (GDM) plus rectus abdominis muscle (RAM) myopathy predicts long-term urinary incontinence (UI). Atrophic and stiff RAM are characteristics of diabetes-induced myopathy (DiM) in pregnant rats. This study aimed to determine whether swimming exercise (SE) has a therapeutic effect in mild hyperglycemic pregnant rats model. We hypothesized that SE training might help to reverse RAM DiM. Mild hyperglycemic pregnant rats model was obtained by a unique subcutaneous injection of 100 mg/kg streptozotocin (diabetic group) or citrate buffer (non-diabetic group) on the first day of life in Wistar female newborns. At 90 days of life, the rats are mated and randomly allocated to remain sedentary or subjected to a SE protocol. The SE protocol started at gestational day 0 and consisted of 60 min/day for 6 days/week in a period of 20 days in a swim tunnel. On day 21, rats were sacrificed, and RAM was collected and studied by picrosirius red, immunohistochemistry, and transmission electron microscopy. The SE protocol increased the fiber area and diameter, and the slow-twitch and fast-twitch fiber area and diameter in the diabetic exercised group, a finding was also seen in control sedentary animals. There was a decreased type I collagen but not type III collagen area and showed a similar type I/type III ratio compared with the control sedentary group. In conclusion, SE during pregnancy reversed the RAM DiM in pregnant rats. These findings may be a potential protocol to consider in patients with RAM damage caused by GDM.

Fundação de Amparo à Pesquisa do Estado de São Paulohttp://dx.doi.org/10.13039/5011000018072018/03361-82017/21783-42018/02979-82016/01743-5CatinelliBruna B.FlorianoJuliana F.HallurRaghavendra L. S.Fondo Nacional de Desarrollo Científico y Tecnológicohttp://dx.doi.org/10.13039/5011000028501190316SobreviaLuispublisher-imprint-nameNature Portfoliovolume-issue-count1issue-article-count7375issue-toc-levels0issue-pricelist-year2022issue-copyright-holderThe Author(s)issue-copyright-year2022article-contains-esmNoarticle-numbering-styleUnnumberedarticle-registration-date-year2022article-registration-date-month4article-registration-date-day14article-toc-levels0toc-levels0volume-typeRegularjournal-productNonStandardArchiveJournalnumbering-styleUnnumberedarticle-grants-typeOpenChoicemetadata-grantOpenAccessabstract-grantOpenAccessbodypdf-grantOpenAccessbodyhtml-grantOpenAccessbibliography-grantOpenAccessesm-grantOpenAccessonline-firstfalsepdf-file-referenceBodyRef/PDF/41598_2022_Article_10801.pdfpdf-typeTypesettarget-typeOnlinePDFissue-typeRegulararticle-typeOriginalPaperjournal-subject-primaryScience, Humanities and Social Sciences, multidisciplinaryjournal-subject-secondaryScience, Humanities and Social Sciences, multidisciplinaryjournal-subject-secondaryScience, multidisciplinaryjournal-subject-collectionScience (multidisciplinary)open-accesstrue

These authors contributed equally: Bruna B. Catinelli and Patrícia S. Rossignoli.

These authors jointly supervised this work: Angélica M. P. Barbosa and Marilza V. C. Rudge.

A list of authors and their affiliations appears at the end of the paper.

Introduction

Gestational diabetes mellitus (GDM) is known as a serious global health problem1. GDM can cause damage to the skeletal muscle and extracellular matrix (ECM) health and function, i.e. maternal hyperglycemic myopathy2–4. Maternal GDM leads to long-term pelvic floor muscle (PFM) dysfunction and urinary incontinence (UI)5–7, having pregnancy specific-urinary incontinence as a risk factor5. It is unknown how this link occurs4 and how swimming exercise (SE) may alleviate this damage in mild hyperglycemic pregnancy (MHP).

Rat models of MHP also revealed myopathy of the PFM and rectus abdominis muscle (RAM) induced by diabetes (DiM). DiM characterized by muscle atrophy, a shift in the maternal fiber type composition, increased collagen deposition, and higher collagen type I/III ratio 8–11. The latter characteristics mimic those found in human hyperglycemic-associated PFM and RAM myopathy and are considered a profile of skeletal muscle injury caused by GDM during pregnancy in humans 11–13. Despite these observations, the link between GDM and maternal hyperglycemic myopathy remains largely unexplored and without an effective treatment 14.

Exercise has beneficial impacts on maternal glycaemia control and several lifestyle interventions have clarified mechanisms underlying GDM for preventing or minimizing this disease’s associated complications 8,9,14–18. However, different exercise patterns improve maternal glucose control in some but not all pregnant women with GDM 19–21. Thus, lifestyle interventions during pregnancy alone may not be sufficient to decrease the risk of developing GDM-associated alterations in maternal health 22–27.

Considering that pregnant women should avoid high-impact exercises with the risk of falling and with the risk of abdominal trauma, SE is considered ideal for pregnant women. Also, SE in a low-moderate intensity is effective in promoting glycemic control and preventing GDM 21,24,27. In addition, SE and resistance training influence the gastrocnemius and soleus muscles myopathy in rat models of type 2 diabetes mellitus (T2DM)28,29. However, there is limited evidence describing the effect of SE on diabetic myopathy in GDM 22,30. There are no studies revealing whether the exercise intervention during pregnancy recovers the muscle damage associated with GDM, even considering the regenerative skeletal muscle fibers potential 31.

The aim of this study was to determine whether SE has a therapeutic effect in MHP rats model resulting in attenuation of RAM DiM. We hypothesized that SE training would mitigate RAM DiM, thus reversing the RAM injury. A potential reversal of RAM DiM by SE may improve the handling of maternal hyperglycemic myopathy in women that developed GDM.

Results

The experimental design included three control groups, i.e., non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), and diabetic sedentary allowing the analysis of the SE intervention in DiM in the authentic study group: the diabetic exercised (Dex). The OGTT showed that Dsed and Dex groups had two or more blood glucose measurements > 140 mg/dl. These data confirm that the generation of MHP rats model was efficient, including the animals in the experimental groups. The aquatic exercise practice during pregnancy did not promote changes in blood glucose levels (Fig. 1).

Oral glucose tolerance test. Blood glucose level before the test and 10, 20, 30, 60 and 120 min after the administration of intragastric glucose solution in Dsed and Dex groups.

The RAM DiM was confirmed in diabetic sedentary rats, demonstrated by the lower total muscle area and the fiber diameter compared with NDsed group (Fig. 2A,B). However, the fiber area was unaltered in Dsed compared with NDsed group.

Histological sections of rat rectus abdominis muscle (RAM), obtained from CellSens Dimension (Olympus Corporation®) Version 1.16 image analysis software—(https://www.olympus-lifescience.com/en/software/cellsens/). (A) RAM samples were taken from non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), diabetic sedentary (Dsed) and diabetic exercised (Dex) rats as described in “Materials and methods”. RAM samples were stained with picrosirius red and immunohistochemistry against myosin heavy chain of slow and fast RAM fibers. (B) Picrosirius red staining for total muscle area, fiber area, and fiber diameter in RAM samples as in (A). (C) Immunohistochemistry for total slow-twitch fiber area,slow-twitch fiber area, and slow-twitch fiber diameter as in (A). (D) Immunohistochemistry for total fast-twitch fiber area,fast-twitch fiber area, and fast-twitch fiber diameter as in (A). Values are means ± S.D. (n = 5 animals/group. *p < 0.05, **p < 0.01, ***p < 0.001 and ****p < 0.0001. Scale bar: 50 µm. Magnification: ×20.

The immunohistochemical analysis showed that the slow-twitch fiber area and diameter (Fig. 2C) were higher in Dsed compared with NDsed group. However, the fast-twitch fiber area and diameter (Fig. 2D) were unaltered in Dsed compared with NDsed group. The total collagen area and collagen I/III ratio (Fig. 3B) were unaltered in Dsed compared with NDsed group. However, type I collagen area and type III collagen area (Fig. 3C) were higher in Dsed compared with NDsed group.

Immunohistochemical sections of rat rectus abdominis muscle (RAM), obtained from CellSens Dimension (Olympus Corporation®) Version 1.16 image analysis software—(https://www.olympus-lifescience.com/en/software/cellsens/). (A) RAM samples were taken from non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), diabetic sedentary (Dsed) and diabetic exercised (Dex) rats as described in Materials and methods. RAM samples were stained with Picrosirius red and immunohistochemistry using antibodies against type I and III collagen on RAM fibers. (B) Picrosirius red staining for total collagen area and immunohistochemistry for type I/III ratio. (C) Immunohistochemistry for type I and III collagen area as in (A). Values are means ± S.D. (n = 5 animals/group. *p < 0.05, **p < 0.01, ***p < 0.001 and ****p < 0.0001. Scale bar: 50 µm. Magnification: ×20.

Electron micrographs of RAM from Dsed group showed disorganized Z lines, sarcomeres disruption areas and an increase in collagen deposition. Also, intermyofibrillar mitochondria, organized triads and myelin figures were observed (Fig. 4).

Electron micrographs of rectus abdominis muscle (RAM). Samples of RAM were obtained from non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), diabetic sedentary (Dsed), and diabetic exercised (Dex) rats. Magnifications (20.000 x) show a detailled area of the micrograph. The micrographs show disorganized Z lines (white arrows), sarcomeres disruption areas (asterisk), intermyofibrillar mitochondria (m), myelin figures (M), organized triads (t) and an increase in collagen deposition ( +). Scale bar: 5 µm.

SE intervention in pregnancy in non-diabetic rats

The diameter of RAM fibers was significantly lower in the NDex group compared with NDsed group. However, there was no significant difference in total muscle area and fiber area between both groups (Fig. 2A,B).

Immunohistochemical analysis showed that the slow-twitch fiber area and diameter were higher in NDex compared with NDsed (Fig. 2C). However, the total fast-twitch fiber area and fast-twitch fiber area and diameter were similar in NDex compared with NDsed (Fig. 2D). There was no difference in the total collagen area and type I/III collagen ratio between the groups (Fig. 3A,B). However, type I but not type III collagen area was increased in NDex compared to NDsed (Fig. 3C).

Electron micrographs of RAM from NDsed group showed disorganized Z lines, intermyofibrillar mitochondria, organized triads, and myelin figures associated with degenerated organelles (Fig. 4). However, the analysis of micrographs in samples from NDex group showed abundant intermyofibrillar mitochondria, organized triads, and myelin figures and organized Z lines.

SE in pregnancy in diabetic rats

In diabetic exercised rats, the fiber area and diameter was higher in Dex compared with Dsed group (Fig. 2A,B). However, the total muscle area was similar in both groups.

The immunohistochemical analysis showed that the slow-twitch fiber area and diameter (Fig. 2C) and the fast-twitch fiber area and diameter (Fig. 2D) were higher in Dex group compared with Dsed group. The total collagen area and type III collagen area were unaltered in Dex compared to Dsed group (Fig. 3A–C). However, type I collagen area and collagen I/III ratio in Dex were lower compared with Dsed group.

Ultrastructural analysis showed that Dex group presents with abundant intermyofibrillar mitochondria, disorganized Z lines, sarcomeres disruption areas, and increase in collagen deposition, as well as organized triads and myelin figures compared with RAM samples from Dsed group (Fig. 4).

SE in pregnancy in Dex, NDsed, NDex and Dsed

The fiber area and diameter were higher in Dex group compared with NDex group (Fig. 2A,B). However, the total muscle area was lower in Dex compared with NDex group.

The immunohistochemical analysis showed that the slow-twitch fiber area and diameter (Fig. 2C) and fast-twitch fiber area and diameter (Fig. 2D) were higher in Dex group compared with NDsed group. The total collagen area, type I collagen and collagen I/III ratio (Fig. 3A–C) were unaltered in Dex compared with Ndsed and NDexgroups. However, type III collagen area were higher in Dex group compared with NDsed group.

These results evidence that MHP rats after SE during the 3 weeks of pregnancy in a swim tunnel for up to 60 min/day, 6 days/week, that the study group (Dex) displays similar fiber area and diameter, slow-twitch, fast-twitch fiber area and diameter, total collagen area and type I/III collagen ratio compared to NDsed group (Figs. 2 and 3).

Discussion

We investigated whether swimming exercise (SE) would alter the RAM DiM in rats. This preclinical study of SE started on the first day in MHP rats detailed the reversal of RAM skeletal atrophic and stiff muscle through an integrative morphological, ultrastructural and extracellular matrix (ECM) assessment. The main findings of the present study are as follows: first, the RAM DiM was confirmed, demonstrated by lower total muscle area and fiber diameter and increased type I collagen and type III collagen deposition in Dsed compared with NDsed group. These findings were already reported by our group. Second, SE during the whole pregnancy in MHP rats model reversed the RAM skeletal atrophy through an increase in fiber area and diameter, slow-twitch fiber area and diameter, fast-twitch fiber area and diameter in Dex group compared with NDsed group; and reduction in type I collagen area and type I/III collagen ratio compared with Dsed. Also, the similarity in total collagen area, type I collagen area and type I/III collagen ratio with NDsed rats were demonstrated. The close resemblance between RAM morphological, and ECM profile of MHP rats model submitted to SE (Dex group) and NDsed, suggest that SE since the beginning of pregnancy reversed the DiM. These findings support the hypothesis that DiM is inhibited by 21 days of SE training program through the entire pregnancy. Indeed, SE training plays a critical role in the reversion of DiM. It may be a sufficient duration and intensity to induce recovery of morphological changes in skeletal muscle.

Women who develop GDM are more likely to develop type 2 diabetes and UI later in life5–7,32. The underlying mechanism linking GDM and long-term UI seems to be diabetic myopathy, characterized by loss of muscle mass and strength 33,34. Many clinical and experimental studies have associated both type 1 and type 2 diabetes to muscle structural changes, including a reduction in myofiber and myofibrilar diameter, reduced muscle mass 3,33, reduced muscle fiber size 35, and decreased capacity to repair from damage 33.

MHP rats is an experimental model that induces structural changes including reduced muscle area and increased slow-twitch fiber in pregnant rats in RAM 10 and in urethral striated muscle 8,9, either in women or in rats 11. These structural harms may be related to functional changes as well as a decline in muscle strength and increased fatigability, which contributes to decreased physical capacity 3,35. Therefore, this damage to muscles involved in urinary continence may contribute to increased incidence of PS-UI, a predictor of long-term UI in previous GDM women 5. These findings allow us to adopt MHP’ rats model for studying the effects of SE on the RAM fiber-ECM structure, as it mimics GDM in women 11. Therefore, further study is necessary to elucidate the influence of exercise types and duration on the muscle fiber cross-sectional area of MHP rats' skeletal muscle.

SE started at the first day of pregnancy in MHP rats may be considered a preclinical study being developed as a prevention strategy of hyperglycemia in pregnancy for long-term UI. Our intention was for longer-lasting interventions leading to significant downstream impact in promoting long-term women’s health. The goals of this early intervention program in pregnancy are related to improving future maternal health in GDM women, one of the United Nation’s Eight Millennium Development Goals (MDGs) 36,37.

Pregnancy is the center of a program established by the International Federation of Gynecology and Obstetrics (FIGO) in the Non-Communicable Disease (NCD)—as early as possible but focusing on the first-trimester and follow-up post-pregnancy for mother and offspring, leading to prevent NCD. Pregnancy, in particular the first trimester, receive not only substantial attention but also many points of intervention, from pre-conception to postpartum 37. However, there are few studies evaluating the impact of hyperglycemia in pregnancy on structural muscles damage involved in urinary continence. This study tested the hypothesis that SE daily, since the beginning of pregnancy in MHP rats could act as a protective non-pharmacological intervention, so we studied its effects on RAM muscle looking at the reversal of muscle atrophy and stiffness.

Increased muscle fiber cross-sectional area, fiber area and diameter in RAM of diabetic pregnant rats after 21 days of SE is similar to the reported after 8 weeks of aerobic training 38. The results of this study revealed that SE daily, since the beginning of pregnancy in MHP rats, reverses the muscle atrophy caused by the maternal hyperglycemia environment. In short, these findings indicated that SE could reverse muscle atrophy in MHP rats, back into the NDsed group profile. In contrast, sarcomeres disruption areas were observed in both diabetic groups, which means that exercise had no impact on this parameter. Previous results demonstrate that RAM exposed to a hyperglycemic environment is characterized by a decrease in the number and area of the fast fiber and an increase in the number of slow fibers 10. In our study, daily SE during all pregnancy had an effect not only on increasing fast-twitch fiber area and diameter but also on slow-twitch fiber area and diameter of RAM muscle in both exercised groups.

The present study shows that both exercised groups regardless of diabetes had increased fast-twitch fiber area and diameter. These findings support the possibility that DiM model is inhibited by exercise training 39. Different SE modalities increased diameter of both slow-twitch and fast-twitch fibers on gastrocnemius and soleus muscles in the type 2 diabetes animal model 28. Thus, the high slow-twitch fiber area and diameter in the RA muscle of both exercised groups regardless of diabetes and high fast-twitch fiber area and diameter in diabetic exercised rats could be attributed to physiological adaptations from aerobic exercise during the whole pregnancy. Consistent with previous studies, we demonstrated that SE training during the whole pregnancy induces an increase not only in the cross-sectional area and slow-twitch fiber, but also the fast-twitch fiber 40,41. Indeed, SE applied in this study showed a significant reversal of muscle atrophy in pregnant hyperglycemic rats.

Exercise training plays an important role in the mitigation of muscular atrophy in DiM. Coherent with previous studies, a resistance training protocol enhanced muscle strength on extensor digitorum longus muscle, gastrocnemius and soleus muscles of male diabetic rats, improving muscle physical and motor function, minimizing the deleterious effect of diabetes on muscles29. Conversely, the fast and slow-twitch fiber area and diameter increase may be related to improved muscle endurance, possibly caused by mitochondrial biogenesis and increased mitochondrial enzymes activities. These findings enhance aerobic capacity and provide muscle contraction with less energy expenditure and greater oxygen uptake 42.

The urethral extracellular matrix also plays a role in the mechanism of urinary continence 43. In prior translational studies in rats, it was shown that diabetes during pregnancy results in damaged extracellular matrix (ECM) and urethral striated muscle suggestive of the high long-term UI prevalence in women 8,9. Other studies examined the relationship between ECM components (particularly collagens) and diabetes, PFDs and pregnancy, although few comparative data are available 18. The results in the present study show that SE in MHP rats did not reduce the total collagen area compared with the three other groups. However, SE in MHP rats decreases type I collagen area to similar levels of non-diabetic sedentary group and maintain high levels of type III collagen similar to SE MHP and SE non-diabetic group. The decrease in collagen type I/III ratio in SE-MHP suggests the reversal of a stiff into a soft healthy skeletal muscle. Our findings complement the results of four previously experimental studies, either in RAM or PFM 8,10,18,43 indicating a complete muscle remodeling. It confirms the importance of this biological approach in DiM. This changeover in collagen type I/III ratio in SE in MHP favors normal soft RAM muscle, with likely normalization of biomechanical properties in muscles involved in urinary continence. All these changes allow suggesting SE for assessment as a potential treatment for maternal UI injured by the maternal hyperglycemic environment.

Although this set of results related to SE in mitigating the negative effects of the maternal hyperglycemic environment on DiM in the transformation into a soft health muscle, the molecular regulations of this gain muscle mass is unclear. It was suggested that distinct mechanisms regulate skeletal muscle mass recovery and hypertrophy 44. Further studies should address this fundamental mechanism. This study as a preclinical model in the obstetrical area, the maternal-placental and fetal (MPF) unit needs to be carefully considered. Although we conducted this experiment by using the same swimming protocol established previously 45–47, the whole MPF unit analysis was not performed. Thus, our successful results with SE in MHP rats environment may be analysed with caution to be considered in GDM women. Also, the present study has limitations regarding the experimental diabetes induction, which represents GDM blood glucose levels, but occurred before pregnancy 47–49. In addition, the guidelines recommend that pregnant women should exercise at least 150 min/week or 30 min/day most days of the week 22,23,25. Also, specific analysis of aerobic capacity and muscle function should be explored.

In conclusion, hyperglycemia exerts an impact on DiM generating an atrophic and stiff muscle. SE intervention training during whole pregnancy in rats imposes a positive influence on DiM being capable of reversing this muscle atrophy and transforming a stiff into a soft healthy skeletal muscle. Therefore, these findings of reversal myopathy suggest that SE training during the whole pregnancy may play a therapeutic role in regulating the damages caused by the maternal hyperglycemic environment and may be considered as a potential treatment for RAM damage caused by GDM.

Materials and methods

This current project corresponds to the translational part of the Diamater Study, a cohort Thematic Project with the financial support of São Paulo Research Foundation (FAPESP 2016/01743-5), a state research foundation in Brazil. The Diamater cohort project has been developed to investigate biomolecular muscle profiles as predictors for long-term urinary incontinence in women with Gestational Diabetes Mellitus 4. According to the requirement to develop innovative treatments for DiM, this translational project was developed.

Ethics and animals

All animal experiments were approved by the Institutional Animal Care and Use Committee, Faculdade de Filosofia e Ciências, São Paulo State University (UNESP), in accordance with the Brazilian Council for Control of Animal Experimentation (CONCEA) (protocol number 007/2016). The study is reported in accordance with the ARRIVE guidelines.

Female and male Wistar rats obtained from ANILAB were housed in a facility with constant temperature (22 ± 2 ˚C) and humidity (55 ± 5%) on a controlled 12 h light–12 h dark cycle with food and water ad libitum, in individual plastic cages during all experimental protocol. The experimental sequence is shown in Fig. 5.

Experimental sequence of groups.

Generation of MHP rats model

The MHP model is the same as previous reports 9–11,46,47. To induce MHP rats’ model, newborn female Wistar received in the first day of life subcutaneously injection of STZ (Sigma®) diluted in citrate buffer (0.1 mol/l pH 4.5) in a dose of 100 mg/kg. Non-diabetic rats received subcutaneous injection of citrate buffer (0.1 mol/l pH 4.5) 50. All female newborn rats were maintained with their mothers until the end of the lactation period (21 days). After this period, the mother rats were euthanized by sodium thiopental injection(Thiopentax®—80 mg/kg). The female newborns were maintained until adulthood. Fasting blood glucose level was determined in adult life, and used for inclusion or exclusion criteria in the study. Diabetic animals should present blood glucose level between 120 mg/dl and 300 mg/dl, and non-diabetic animals blood glucose level < 120 mg/dl 51.

Mating process

At approximately day 90 of age, four diabetic and non-diabetic female rats were housed overnight with one adult male rat. The presence of spermatozoa in the vaginal smear was considered gestational day 0 [52]. After, rats were housed in individual cages until 21º day of pregnancy.

Experimental groups

On gestational day 0, female rats were randomly allocated into four experimental groups according to sedentary lifestyle or swimming exercise: Non-Diabetic Sedentary (NDsed) (n = 13), Non-Diabetic Exercised (NDex) (n = 13), Diabetic Sedentary (Dsed) (n = 13) and Diabetic Exercised (Dex) (n = 13). Dex is the study group and the other three (NDsed, NDex and Dsed) are control groups.

Swimming exercise protocol

The swimming exercise protocol was based on previous studies 45–47 and considered to be a moderate intensity exercise protocol 45. The exercised animals were exposed to water daily temperature 31 ± 1°C for 6 days/week, from gestational day 0 until gestational day 20 on a pool at a depth of 40 cm at the water. The first training session started with 20 min, progressively increasing 10 min/day until 60 min. The sedentary rats were exposed to water daily for 15 min, at a depth of 10 cm at water temperature 31 ± 1 °C for 6 days/week, from gestational day 0 until gestational day 20, aiming not to promote physiological adaptations from exercise practice.

Oral glucose tolerance test (OGTT)

On gestational day 17, an OGTT was performed to confirm the glucose intolerance in diabetics 50. Fasting glycemia and at 10, 20, 30, 60 and 120 min after administration of an intragastric glucose solution (0.2 g/mL) in a dose of 2.0 g/kg were measured. Diabetes diagnosis was confirmed with two or more blood glucose measurements > 140 mg/dL 51.

RAM tissue extraction

At the end of pregnancy (gestational day 21) the dams were euthanized by sodium thiopental injection (Thiopentax, Brazil, 80 mg/kg dose). An abdominal incision was performed for RAM sample collection. The lower third on the right side of RAM was exposed, dissected, and removed for integrative morphological analysis. The fragments had approximately 0.25 cm2. Then, a C-section was performed and fetuses and placentas were separately analyzed in different projects.

Integrative morphological analysis

The samples obtained were selected into separate parts according to methodological procedures. The integrative morphological analysis is composed by morphological, morphometric, immunohistochemistry and ultrastructural RAM analysis.

Morphological analysis

For morphological and morphometric analysis, RAM samples were immersed for 24 h in neutral 10% buffered formaldehyde, transferred to 70% alcohol and maintained at room temperature and then embedded in paraffin. The 4-µm-thick sections were cut in microtome (Reichert-Jung model 820) and fixed on microscope glass slides stained with Hematoxylin & Eosin (H&E) and Picrosirius Red. H&E-stained slides were used to observe the general morphology of the RAM. Picrosirius Red-stained slides were analyzed with the color-segmentation method to determine the red (collagen) and yellow (muscle fiber) -stained tissue in the same section and used to determine muscle, fiber and collagen area and fiber diameter. The slides were analyzed in a light microscope (Olympus Corporation®/BX41TF coupled with DP25-4 digital câmera). The photographs were obtained with cell Sens Ver 1.18 Olympus Corporation® software.

Morphometric analysis

For morphometric analysis of muscle and collagen area, 40 sections/group (5 animals/group, 8 sections/animal) were selected. For morphometric analysis of fiber area and diameter, 100 muscle fibers/group were selected. All analyzes were performed using CellSens Dimension Version 1.16 (Olympus Corporation®) image analysis software (20 × magnification).

Immunohistochemistry

Immunohistochemical analysis was used to stain slow-twitch and fast-twitch muscle fibers and type I and III collagen. For immunohistochemistry (N = 5 samples/group), the samples were immersed for 24 h in neutral 10% buffered formaldehyde, transferred to 70% alcohol and maintained at room temperature and then embedded in paraffin. The 4-µm-thick sections were cut in the microtome. Sections were deparaffinized and incubated with antigenic recovery for 35 min in a pressure cooker. Endogenous peroxidase was blocked using H2O2 in phosphate buffered saline (PBS). After washing, the sections were incubated with bovine serum albumin solution (BSA 3%) for 1 h. The sections were incubated overnight at 4 °C with primary antibodies against myosin heavy chain, slow (Novocastra, NCL-MHCs, #6009289, 1:20) and fast (Novocastra, NCL-MHCf, #6006929, 1:20) muscle fibers, type I Collagen (Sigma Aldrich, SAB4200678, #107M4839V, 1:100) and type III Collagen (Novus Biologicals, COL3A1, #G0809, 1:100). After incubation, the sections were washed three times for five minutes with PBS and incubated with secondary antibodies for 1 h 30 min (Goat Anti-Mouse, Abcam, 1:200). For staining, the sections were incubated with diaminobenzidine for 1 min and hematoxylin for 10 min. The slow-twitch and fast-twitch muscle fibers, and type I and III Collagen were analyzed using a light microscope (Olympus Corporation®/BX41TF coupled with DP25-4 digital câmera) and 40 sections/group (5 animals/group, 8 sections/animal) were selected to quantify the fiber type area and collagen type area. Also, each muscle fiber was manually selected (~ 200 slow fibers/group; ~ 330 fast fibers/group) and fiber type area and diameter were quantified using CellSens Dimension (Olympus Corporation®) Version 1.16 image analysis software (20 × magnification). The fiber type area was quantitatively determined, as described previously10.

Ultrastructural analysis

As previously described, the RAM tissues obtained to ultrastructural analysis (3 samples/group) were cut into small strips and immediately immersed in Karnovsky fixative for 3 h at room temperature and transferred to the refrigerator to post-fixation in 1% osmium tetroxide for 24 h and afterward, the samples were embedded in epoxy resin. Ultra-thin sections were obtained at a longitudinal orientation and stained sections were examined using transmission electron microscopy using (JEM 1400, JEOL®).

Statistical analysis

GraphPad Prism® v.8.0 software was used to analyze the data. Data are expressed as mean ± standard deviation (SD). Comparisons of measurements among groups were performed by two-way ANOVA followed by Tukey’s multiple comparison tests. For all statistical comparisons, p < 0.05 was considered statistically significant.

Acknowledgements

The authors thank the support from researchers and for the access to the infrastructure of UNIPEX (Experimental Research Unit) Botucatu Medical School—UNESP and Physiological Sciences Laboratory—School of Phylosophy and Sciences—UNESP.Special thanks to Augusto Nascimento from the Physiological Science Laboratory (Campus of Marília) and PauloGeorgete from UNIPEX (Campus of Botucatu) and Cirilo (University of Marília). Transmission electron microscopy images were obtained at the Centre of Microscopy and Image (CMI), Piracicaba Dental School, UNICAMP. Technical support of Flavia Sammartino Mariano Rodrigues is appreciated. This study was supported by FAPESP—Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant number 2016/01743-5), CNPq—Conselho Nacional de DesenvolvimentoCientífico e Tecnológico to MVC Rudge (305116/2018-5). BB Catinelli received a master scholarship from FAPESP—Fundação de Amparo à Pesquisa do Estado de São Paulo (2018/03361-8), JF Floriano and RLS Hallur received Posdoc scholarships from FAPESP (Grant numbers 2017/21783-4 and 2018/02979-8). L Sobrevia thanks the support from the Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) (Grant number 1190316), Chile, and International Sabbaticals (University Medical Centre Groningen, University of Groningen, The Netherlands) from the Vicerectorate of Academic Affairs, Academic Development Office of the Pontificia Universidad Católica de Chile.

Author contributions

Conceptualization: M.V.C.R., A.M.P.B. and P.S.R. Data curation: B.B.C., M.V.C.R., A.M.P.B., P.S.R. and M.A.S. Formal analysis: B.B.C., P.S.R., A.M.P.B. and M.V.C.R. Funding acquisition: M.V.C.R., I.M.P.C. and A.M.P.B. Investigation/Methodology/Sample collection: B.B.C., P.S.R., A.M.C., J.F., M.A.S., S.L.F., R.G.O., N.J.S., L.C.C.U. Project administration: B.B.C., M.V.C.R., A.M.P.B., P.S.R. and I.M.P.C. Supervision: M.V.C.R., A.M.P.B. and P.S.R. Writing-original draft: B.B.C., P.S.R., M.A.S., S.L.F. Writing-review & editing: B.B.C., L.S., P.S.R., A.M.C., J.F., S.L.F., R.H., M.A.S., R.G.O., N.J.S., L.C.C.U., I.M.P.C., A.M.P.B., M.V.C.R. The Diamater Study Group designated as authors qualify for authorship as a fundamental part of this study. B.B.C. master scholarship fromFapesp. All authors have approved the final version of the manuscript and agree to be accountable for all aspects of the work.

Data availability

The datasets used and/or analyzed during the present study are available from the corresponding author on request.

Competing interests

The authors declare no competing interests.

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P. + + 36 + + + + + + + + grid.410543.7 + 0000 0001 2188 478X + Postgraduate Program on Tocogynecology, Department of Gynecology and Obstetrics, Botucatu Medical School + São Paulo State University (UNESP) + + Botucatu + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Department of Physiotherapy and Occupational Therapy, School of Philosophy and Sciences + São Paulo State University (UNESP) + + Marília + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Laboratory of Extracellular Matrix Biology, Department of Structural and Functional Biology, Institute of Biosciences of Botucatu + São Paulo State University (UNESP) + + Botucatu + São Paulo + Brazil + + + + + grid.411087.b + 0000 0001 0723 2494 + Department of Structural and Functional Biology, Institute of Biology (IB), UNICAMP + University of Campinas (UNICAMP) + + Campinas + São Paulo + Brazil + + + + + University of Marília (UNIMAR) + + Marília + São Paulo + Brazil + + + + + Human Embryology Laboratory + Marília Medical School (FAMEMA) + + Marília + São Paulo + Brazil + + + + + grid.415155.1 + 0000 0001 2039 9627 + Pravara Institute of Medical Sciences (Deemed to be University) + + Loni, Rahata Taluk + 413736 + Ahmednagar District + Maharashtra + India + + + + + grid.7870.8 + 0000 0001 2157 0406 + Cellular and Molecular Physiology Laboratory (CMPL), Department of Obstetrics, Division of Obstetrics and Gynaecology, School of Medicine, Faculty of Medicine + Pontificia Universidad Católica de Chile + + 8330024 + Santiago + Chile + + + + + grid.9224.d + 0000 0001 2168 1229 + Department of Physiology, Faculty of Pharmacy + Universidad de Sevilla + + 41012 + Seville + Spain + + + + + grid.1003.2 + 0000 0000 9320 7537 + University of Queensland Centre for Clinical Research (UQCCR), Faculty of Medicine and Biomedical Sciences + University of Queensland + + 4029 + Herston + QLD + Australia + + + + + grid.4494.d + 0000 0000 9558 4598 + Division of Pathology, Department of Pathology and Medical Biology + University of Groningen, University Medical Center Groningen (UMCG) + + 9713GZ + Groningen + The Netherlands + + + + + grid.410543.7 + 0000 0001 2188 478X + Department of Physics, Institute of Biosciences, Letters and Exact Sciences (IBILCE), Multiuser Center for Biomolecular Innovation (CMIB) + São Paulo State University “Júlio de Mesquita Filho” (UNESP) + + 15054-000 + São José do Rio Preto + São Paulo + Brazil + + + + + grid.412966.e + 0000 0004 0480 1382 + Pelvic Care Center Maastricht + Maastricht University Medical Center + + Maastricht + The Netherlands + + + + + grid.25073.33 + 0000 0004 1936 8227 + Department of Clinical Epidemiology and Biostatistics + McMaster University + + Hamilton + ON + Canada + + + + + grid.6363.0 + 0000 0001 2218 4662 + Department of Gynecology, Pelvic Floor Center Charité + Charité University Hospital + + Berlin + Germany + + + + + grid.410543.7 + 0000 0001 2188 478X + POSMAT-Post-Graduate Program in Materials Science and Technology, School of Sciences + São Paulo State University (UNESP) + + Bauru + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Medical School of Botucatu + São Paulo State University (UNESP) + + Botucatu + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Department of Nursing, Botucatu Medical School (FMB) + São Paulo State University (UNESP) + + Botucatu + São Paulo + Brazil + + + + + grid.411869.3 + 0000 0000 9186 527X + Stricto Sensu Graduate Program in Nursing at UNIVERITAS, Guarulhos University (UNG) + + Guarulhos + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Department of Clinical Medicine, Botucatu Medical School + São Paulo State University (UNESP) + + Av. Prof. Mário Rubens Guimarães Montenegro, s/n-UNESP + Botucatu + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Department of Biostatistics, Botucatu Institute of Biosciences + São Paulo State University/UNESP + + São Paulo + tistics, Botucatu Institute of Biosciences + Brazil + + + + + grid.411249.b + 0000 0001 0514 7202 + Discipline of Evidence-Based Medicine, Paulista School of Medicine-Federal University of São Paulo (EPM-UNIFESP) + + São Paulo + Brazil + + + + + grid.411249.b + 0000 0001 0514 7202 + Department of Gynecology + Federal University of São Paulo, UNIFESP + + São Paulo + Brazil + + + + + grid.441972.d + 0000 0001 2105 8867 + Department of Physical Therapy + Universidade Católica de Pernambuco (UNICAP) + + Recife + PE + Brazil + + + + + grid.11899.38 + 0000 0004 1937 0722 + Department of Operative Dentistry, Endodontics and Dental Materials, Bauru School of Dentistry + University of São Paulo + + São Paulo + Brazil + + + + + grid.412294.8 + 0000 0000 9007 5698 + University of Western São Paulo (UNOESTE) + + Presidente Prudente + São Paulo + Brazil + + + + + grid.411400.0 + 0000 0001 2193 3537 + Department of Anatomy, CCB + State University of Londrina (UEL) + + Caixa Postal 10011 + Campus Universitário s/n + 86057-970 + Londrina + Parana + Brazil + + + + + University Center of Associated Colleges + + São João da Boa Vista + São Paulo + Brazil + + + + + grid.441751.2 + 0000 0000 8820 7559 + Regional University Center of Espírito Santo do Pinhal, UNIPINHAL + + Espírito Santo do Pinhal + São Paulo + Brazil + + + + + grid.412296.a + 0000 0001 1484 3840 + Universidade do Sagrado Coração (USC) + + Bauru + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Department of Physical Education, Institute of Biosciences of Rio Claro + São Paulo State University (UNESP) + + Rio Claro + São Paulo + Brazil + + + + + Independent Researcher + + Assis + São Paulo + Brazil + + + + + grid.410543.7 + 0000 0001 2188 478X + Department of Morphology and Pediatric Dentistry, Araraquara School of Dentistry + São Paulo State University (UNESP) + + Rua Humaitá, 1680 + 14801-903 + Araraquara + São Paulo + Brazil + + + + + Independent Researcher + + Botucatu + SP + Brazil + + + + + grid.412296.a + 0000 0001 1484 3840 + Health Sciences Center + University of the Sacred Heart (USC) + + Bauru + São Paulo + Brazil + + + + + grid.441895.5 + 0000 0000 9898 9056 + Universidade de Marília (UNIMAR) + + Marília + São Paulo + Brazil + + + + + + marilzarudge@gmail.com + + + + 5 + 5 + 2022 + + + 12 + 2022 + + 12 + 1 + 7375 + + + 14 + 4 + 2022 + + + 9 + 11 + 2021 + + + 29 + 3 + 2022 + + + 5 + 5 + 2022 + + + + © The Author(s) 2022 + 2022 + + + Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. 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Gestational diabetes mellitus (GDM) plus rectus abdominis muscle (RAM) myopathy predicts long-term urinary incontinence (UI). Atrophic and stiff RAM are characteristics of diabetes-induced myopathy (DiM) in pregnant rats. This study aimed to determine whether swimming exercise (SE) has a therapeutic effect in mild hyperglycemic pregnant rats model. We hypothesized that SE training might help to reverse RAM DiM. Mild hyperglycemic pregnant rats model was obtained by a unique subcutaneous injection of 100 mg/kg streptozotocin (diabetic group) or citrate buffer (non-diabetic group) on the first day of life in Wistar female newborns. At 90 days of life, the rats are mated and randomly allocated to remain sedentary or subjected to a SE protocol. The SE protocol started at gestational day 0 and consisted of 60 min/day for 6 days/week in a period of 20 days in a swim tunnel. On day 21, rats were sacrificed, and RAM was collected and studied by picrosirius red, immunohistochemistry, and transmission electron microscopy. The SE protocol increased the fiber area and diameter, and the slow-twitch and fast-twitch fiber area and diameter in the diabetic exercised group, a finding was also seen in control sedentary animals. There was a decreased type I collagen but not type III collagen area and showed a similar type I/type III ratio compared with the control sedentary group. In conclusion, SE during pregnancy reversed the RAM DiM in pregnant rats. These findings may be a potential protocol to consider in patients with RAM damage caused by GDM.

+ + + + + + Fundação de Amparo à Pesquisa do Estado de São Paulo + http://dx.doi.org/10.13039/501100001807 + + + 2018/03361-8 + 2017/21783-4 + 2018/02979-8 + 2016/01743-5 + + + Catinelli + Bruna B. + + + + + Floriano + Juliana F. + + + + + Hallur + Raghavendra L. S. + + + + + + + + Fondo Nacional de Desarrollo Científico y Tecnológico + http://dx.doi.org/10.13039/501100002850 + + + 1190316 + + + Sobrevia + Luis + + + + + + + publisher-imprint-name + Nature Portfolio + + + volume-issue-count + 1 + + + issue-article-count + 7375 + + + issue-toc-levels + 0 + + + issue-pricelist-year + 2022 + + + issue-copyright-holder + The Author(s) + + + issue-copyright-year + 2022 + + + article-contains-esm + No + + + article-numbering-style + Unnumbered + + + article-registration-date-year + 2022 + + + article-registration-date-month + 4 + + + article-registration-date-day + 14 + + + article-toc-levels + 0 + + + toc-levels + 0 + + + volume-type + Regular + + + journal-product + NonStandardArchiveJournal + + + numbering-style + Unnumbered + + + article-grants-type + OpenChoice + + + metadata-grant + OpenAccess + + + abstract-grant + OpenAccess + + + bodypdf-grant + OpenAccess + + + bodyhtml-grant + OpenAccess + + + bibliography-grant + OpenAccess + + + esm-grant + OpenAccess + + + online-first + false + + + pdf-file-reference + BodyRef/PDF/41598_2022_Article_10801.pdf + + + pdf-type + Typeset + + + target-type + OnlinePDF + + + issue-type + Regular + + + article-type + OriginalPaper + + + journal-subject-primary + Science, Humanities and Social Sciences, multidisciplinary + + + journal-subject-secondary + Science, Humanities and Social Sciences, multidisciplinary + + + journal-subject-secondary + Science, multidisciplinary + + + journal-subject-collection + Science (multidisciplinary) + + + open-access + true + + + + +

These authors contributed equally: Bruna B. Catinelli and Patrícia S. Rossignoli.

+ + +

These authors jointly supervised this work: Angélica M. P. Barbosa and Marilza V. C. Rudge.

+ + +

A list of authors and their affiliations appears at the end of the paper.

+ + + + + Introduction +

Gestational diabetes mellitus (GDM) is known as a serious global health problem + + 1 + . GDM can cause damage to the skeletal muscle and extracellular matrix (ECM) health and function, i.e. maternal hyperglycemic myopathy + + 2– + 4 + . Maternal GDM leads to long-term pelvic floor muscle (PFM) dysfunction and urinary incontinence (UI) + + 5– + 7 + , having pregnancy specific-urinary incontinence as a risk factor + + 5 + . It is unknown how this link occurs + + 4 + and how swimming exercise (SE) may alleviate this damage in mild hyperglycemic pregnancy (MHP). +

+

Rat models of MHP also revealed myopathy of the PFM and rectus abdominis muscle (RAM) induced by diabetes (DiM). DiM characterized by muscle atrophy, a shift in the maternal fiber type composition, increased collagen deposition, and higher collagen type I/III ratio  + + 8– + 11 + . The latter characteristics mimic those found in human hyperglycemic-associated PFM and RAM myopathy and are considered a profile of skeletal muscle injury caused by GDM during pregnancy in humans  + + 11– + 13 + . Despite these observations, the link between GDM and maternal hyperglycemic myopathy remains largely unexplored and without an effective treatment  + + 14 + . +

+

Exercise has beneficial impacts on maternal glycaemia control and several lifestyle interventions have clarified mechanisms underlying GDM for preventing or minimizing this disease’s associated complications  + + 8, + 9, + 14– + 18 + . However, different exercise patterns improve maternal glucose control in some but not all pregnant women with GDM  + + 19– + 21 + . Thus, lifestyle interventions during pregnancy alone may not be sufficient to decrease the risk of developing GDM-associated alterations in maternal health  + + 22– + 27 + . +

+

Considering that pregnant women should avoid high-impact exercises with the risk of falling and with the risk of abdominal trauma, SE is considered ideal for pregnant women. Also, SE in a low-moderate intensity is effective in promoting glycemic control and preventing GDM  + + 21, + 24, + 27 + . In addition, SE and resistance training influence the gastrocnemius and soleus muscles myopathy in rat models of type 2 diabetes mellitus (T2DM) + + 28, + 29 + . However, there is limited evidence describing the effect of SE on diabetic myopathy in GDM  + + 22, + 30 + . There are no studies revealing whether the exercise intervention during pregnancy recovers the muscle damage associated with GDM, even considering the regenerative skeletal muscle fibers potential  + + 31 + . +

+

The aim of this study was to determine whether SE has a therapeutic effect in MHP rats model resulting in attenuation of RAM DiM. We hypothesized that SE training would mitigate RAM DiM, thus reversing the RAM injury. A potential reversal of RAM DiM by SE may improve the handling of maternal hyperglycemic myopathy in women that developed GDM.

+ + + Results +

The experimental design included three control groups, i.e., non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), and diabetic sedentary allowing the analysis of the SE intervention in DiM in the authentic study group: the diabetic exercised (Dex). The OGTT showed that Dsed and Dex groups had two or more blood glucose measurements > 140 mg/dl. These data confirm that the generation of MHP rats model was efficient, including the animals in the experimental groups. The aquatic exercise practice during pregnancy did not promote changes in blood glucose levels (Fig.  + 1). + + + +

Oral glucose tolerance test. Blood glucose level before the test and 10, 20, 30, 60 and 120 min after the administration of intragastric glucose solution in Dsed and Dex groups.

+ +

+ +

+ +

+

The RAM DiM was confirmed in diabetic sedentary rats, demonstrated by the lower total muscle area and the fiber diameter compared with NDsed group (Fig.  + 2A,B). However, the fiber area was unaltered in Dsed compared with NDsed group. + + + +

Histological sections of rat rectus abdominis muscle (RAM), obtained from CellSens Dimension (Olympus Corporation®) Version 1.16 image analysis software—( + https://www.olympus-lifescience.com/en/software/cellsens/). + (A) RAM samples were taken from non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), diabetic sedentary (Dsed) and diabetic exercised (Dex) rats as described in “ + Materials and methods”. RAM samples were stained with picrosirius red and immunohistochemistry against myosin heavy chain of slow and fast RAM fibers. + (B) Picrosirius red staining for total muscle area, fiber area, and fiber diameter in RAM samples as in ( + A). ( + C) Immunohistochemistry for total slow-twitch fiber area,slow-twitch fiber area, and slow-twitch fiber diameter as in ( + A). ( + D) Immunohistochemistry for total fast-twitch fiber area,fast-twitch fiber area, and fast-twitch fiber diameter as in ( + A). Values are means ± S.D. (n = 5 animals/group. *p < 0.05, **p < 0.01, ***p < 0.001 and ****p < 0.0001. Scale bar: 50 µm. Magnification: ×20. +

+ +

+ +

+ +

+

The immunohistochemical analysis showed that the slow-twitch fiber area and diameter (Fig.  + 2C) were higher in Dsed compared with NDsed group. However, the fast-twitch fiber area and diameter (Fig.  + 2D) were unaltered in Dsed compared with NDsed group. The total collagen area and collagen I/III ratio (Fig.  + 3B) were unaltered in Dsed compared with NDsed group. However, type I collagen area and type III collagen area (Fig.  + 3C) were higher in Dsed compared with NDsed group. + + + +

Immunohistochemical sections of rat rectus abdominis muscle (RAM), obtained from CellSens Dimension (Olympus Corporation + ®) Version 1.16 image analysis software—( + https://www.olympus-lifescience.com/en/software/cellsens/). ( + A) RAM samples were taken from non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), diabetic sedentary (Dsed) and diabetic exercised (Dex) rats as described in + Materials and methods. RAM samples were stained with Picrosirius red and immunohistochemistry using antibodies against type I and III collagen on RAM fibers. + (B) Picrosirius red staining for total collagen area and immunohistochemistry for type I/III ratio. ( + C) Immunohistochemistry for type I and III collagen area as in ( + A). Values are means ± S.D. (n = 5 animals/group. *p < 0.05, **p < 0.01, ***p < 0.001 and ****p < 0.0001. Scale bar: 50 µm. Magnification: ×20. +

+ +

+ +

+ +

+

Electron micrographs of RAM from Dsed group showed disorganized Z lines, sarcomeres disruption areas and an increase in collagen deposition. Also, intermyofibrillar mitochondria, organized triads and myelin figures were observed (Fig.  + 4). + + + +

Electron micrographs of rectus abdominis muscle (RAM). Samples of RAM were obtained from non-diabetic sedentary (NDsed), non-diabetic exercised (NDex), diabetic sedentary (Dsed), and diabetic exercised (Dex) rats. Magnifications (20.000 x) show a detailled area of the micrograph. The micrographs show disorganized Z lines (white arrows), sarcomeres disruption areas (asterisk), intermyofibrillar mitochondria (m), myelin figures (M), organized triads (t) and an increase in collagen deposition ( +). Scale bar: 5 µm.

+ +

+ +

+ +

+ + SE intervention in pregnancy in non-diabetic rats +

The diameter of RAM fibers was significantly lower in the NDex group compared with NDsed group. However, there was no significant difference in total muscle area and fiber area between both groups (Fig.  + 2A, + B). +

+

Immunohistochemical analysis showed that the slow-twitch fiber area and diameter were higher in NDex compared with NDsed (Fig.  + 2C). However, the total fast-twitch fiber area and fast-twitch fiber area and diameter were similar in NDex compared with NDsed (Fig.  + 2D). There was no difference in the total collagen area and type I/III collagen ratio between the groups (Fig.  + 3A,B). However, type I but not type III collagen area was increased in NDex compared to NDsed (Fig.  + 3C). +

+

Electron micrographs of RAM from NDsed group showed disorganized Z lines, intermyofibrillar mitochondria, organized triads, and myelin figures associated with degenerated organelles (Fig.  + 4). However, the analysis of micrographs in samples from NDex group showed abundant intermyofibrillar mitochondria, organized triads, and myelin figures and organized Z lines. +

+ + + SE in pregnancy in diabetic rats +

In diabetic exercised rats, the fiber area and diameter was higher in Dex compared with Dsed group (Fig.  + 2A,B). However, the total muscle area was similar in both groups. +

+

The immunohistochemical analysis showed that the slow-twitch fiber area and diameter (Fig.  + 2C) and the fast-twitch fiber area and diameter (Fig.  + 2D) were higher in Dex group compared with Dsed group. The total collagen area and type III collagen area were unaltered in Dex compared to Dsed group (Fig.  + 3A–C). However, type I collagen area and collagen I/III ratio in Dex were lower compared with Dsed group. +

+

Ultrastructural analysis showed that Dex group presents with abundant intermyofibrillar mitochondria, disorganized Z lines, sarcomeres disruption areas, and increase in collagen deposition, as well as organized triads and myelin figures compared with RAM samples from Dsed group (Fig.  + 4). +

+ + + SE in pregnancy in Dex, NDsed, NDex and Dsed +

The fiber area and diameter were higher in Dex group compared with NDex group (Fig.  + 2A,B). However, the total muscle area was lower in Dex compared with NDex group. +

+

The immunohistochemical analysis showed that the slow-twitch fiber area and diameter (Fig.  + 2C) and fast-twitch fiber area and diameter (Fig.  + 2D) were higher in Dex group compared with NDsed group. The total collagen area, type I collagen and collagen I/III ratio (Fig.  + 3A–C) were unaltered in Dex compared with Ndsed and NDexgroups. However, type III collagen area were higher in Dex group compared with NDsed group. +

+

These results evidence that MHP rats after SE during the 3 weeks of pregnancy in a swim tunnel for up to 60 min/day, 6 days/week, that the study group (Dex) displays similar fiber area and diameter, slow-twitch, fast-twitch fiber area and diameter, total collagen area and type I/III collagen ratio compared to NDsed group (Figs. + 2 and + 3). +

+ + + + Discussion +

We investigated whether swimming exercise (SE) would alter the RAM DiM in rats. This preclinical study of SE started on the first day in MHP rats detailed the reversal of RAM skeletal atrophic and stiff muscle through an integrative morphological, ultrastructural and extracellular matrix (ECM) assessment. The main findings of the present study are as follows: first, the RAM DiM was confirmed, demonstrated by lower total muscle area and fiber diameter and increased type I collagen and type III collagen deposition in Dsed compared with NDsed group. These findings were already reported by our group. Second, SE during the whole pregnancy in MHP rats model reversed the RAM skeletal atrophy through an increase in fiber area and diameter, slow-twitch fiber area and diameter, fast-twitch fiber area and diameter in Dex group compared with NDsed group; and reduction in type I collagen area and type I/III collagen ratio compared with Dsed. Also, the similarity in total collagen area, type I collagen area and type I/III collagen ratio with NDsed rats were demonstrated. The close resemblance between RAM morphological, and ECM profile of MHP rats model submitted to SE (Dex group) and NDsed, suggest that SE since the beginning of pregnancy reversed the DiM. These findings support the hypothesis that DiM is inhibited by 21 days of SE training program through the entire pregnancy. Indeed, SE training plays a critical role in the reversion of DiM. It may be a sufficient duration and intensity to induce recovery of morphological changes in skeletal muscle.

+

Women who develop GDM are more likely to develop type 2 diabetes and UI later in life + + 5– + 7, + 32 + . The underlying mechanism linking GDM and long-term UI seems to be diabetic myopathy, characterized by loss of muscle mass and strength  + + 33, + 34 + . Many clinical and experimental studies have associated both type 1 and type 2 diabetes to muscle structural changes, including a reduction in myofiber and myofibrilar diameter, reduced muscle mass  + + 3, + 33 + , reduced muscle fiber size  + + 35 + , and decreased capacity to repair from damage  + + 33 + . +

+

MHP rats is an experimental model that induces structural changes including reduced muscle area and increased slow-twitch fiber in pregnant rats in RAM  + + 10 + and in urethral striated muscle  + + 8, + 9 + , either in women or in rats  + + 11 + . These structural harms may be related to functional changes as well as a decline in muscle strength and increased fatigability, which contributes to decreased physical capacity  + + 3, + 35 + . Therefore, this damage to muscles involved in urinary continence may contribute to increased incidence of PS-UI, a predictor of long-term UI in previous GDM women  + + 5 + . These findings allow us to adopt MHP’ rats model for studying the effects of SE on the RAM fiber-ECM structure, as it mimics GDM in women  + + 11 + . Therefore, further study is necessary to elucidate the influence of exercise types and duration on the muscle fiber cross-sectional area of MHP rats' skeletal muscle. +

+

SE started at the first day of pregnancy in MHP rats may be considered a preclinical study being developed as a prevention strategy of hyperglycemia in pregnancy for long-term UI. Our intention was for longer-lasting interventions leading to significant downstream impact in promoting long-term women’s health. The goals of this early intervention program in pregnancy are related to improving future maternal health in GDM women, one of the United Nation’s Eight Millennium Development Goals (MDGs)  + + 36, + 37 + . +

+

Pregnancy is the center of a program established by the International Federation of Gynecology and Obstetrics (FIGO) in the Non-Communicable Disease (NCD)—as early as possible but focusing on the first-trimester and follow-up post-pregnancy for mother and offspring, leading to prevent NCD. Pregnancy, in particular the first trimester, receive not only substantial attention but also many points of intervention, from pre-conception to postpartum  + + 37 + . However, there are few studies evaluating the impact of hyperglycemia in pregnancy on structural muscles damage involved in urinary continence. This study tested the hypothesis that SE daily, since the beginning of pregnancy in MHP rats could act as a protective non-pharmacological intervention, so we studied its effects on RAM muscle looking at the reversal of muscle atrophy and stiffness. +

+

Increased muscle fiber cross-sectional area, fiber area and diameter in RAM of diabetic pregnant rats after 21 days of SE is similar to the reported after 8 weeks of aerobic training  + + 38 + . The results of this study revealed that SE daily, since the beginning of pregnancy in MHP rats, reverses the muscle atrophy caused by the maternal hyperglycemia environment. In short, these findings indicated that SE could reverse muscle atrophy in MHP rats, back into the NDsed group profile. In contrast, sarcomeres disruption areas were observed in both diabetic groups, which means that exercise had no impact on this parameter. Previous results demonstrate that RAM exposed to a hyperglycemic environment is characterized by a decrease in the number and area of the fast fiber and an increase in the number of slow fibers  + + 10 + . In our study, daily SE during all pregnancy had an effect not only on increasing fast-twitch fiber area and diameter but also on slow-twitch fiber area and diameter of RAM muscle in both exercised groups. +

+

The present study shows that both exercised groups regardless of diabetes had increased fast-twitch fiber area and diameter. These findings support the possibility that DiM model is inhibited by exercise training  + + 39 + . Different SE modalities increased diameter of both slow-twitch and fast-twitch fibers on gastrocnemius and soleus muscles in the type 2 diabetes animal model  + + 28 + . Thus, the high slow-twitch fiber area and diameter in the RA muscle of both exercised groups regardless of diabetes and high fast-twitch fiber area and diameter in diabetic exercised rats could be attributed to physiological adaptations from aerobic exercise during the whole pregnancy. Consistent with previous studies, we demonstrated that SE training during the whole pregnancy induces an increase not only in the cross-sectional area and slow-twitch fiber, but also the fast-twitch fiber  + + 40, + 41 + . Indeed, SE applied in this study showed a significant reversal of muscle atrophy in pregnant hyperglycemic rats. +

+

Exercise training plays an important role in the mitigation of muscular atrophy in DiM. Coherent with previous studies, a resistance training protocol enhanced muscle strength on extensor digitorum longus muscle, gastrocnemius and soleus muscles of male diabetic rats, improving muscle physical and motor function, minimizing the deleterious effect of diabetes on muscles + + 29 + . Conversely, the fast and slow-twitch fiber area and diameter increase may be related to improved muscle endurance, possibly caused by mitochondrial biogenesis and increased mitochondrial enzymes activities. These findings enhance aerobic capacity and provide muscle contraction with less energy expenditure and greater oxygen uptake  + + 42 + . +

+

The urethral extracellular matrix also plays a role in the mechanism of urinary continence  + + 43 + . In prior translational studies in rats, it was shown that diabetes during pregnancy results in damaged extracellular matrix (ECM) and urethral striated muscle suggestive of the high long-term UI prevalence in women  + + 8, + 9 + . Other studies examined the relationship between ECM components (particularly collagens) and diabetes, PFDs and pregnancy, although few comparative data are available  + + 18 + . The results in the present study show that SE in MHP rats did not reduce the total collagen area compared with the three other groups. However, SE in MHP rats decreases type I collagen area to similar levels of non-diabetic sedentary group and maintain high levels of type III collagen similar to SE MHP and SE non-diabetic group. The decrease in collagen type I/III ratio in SE-MHP suggests the reversal of a stiff into a soft healthy skeletal muscle. Our findings complement the results of four previously experimental studies, either in RAM or PFM  + + 8, + 10, + 18, + 43 + indicating a complete muscle remodeling. It confirms the importance of this biological approach in DiM. This changeover in collagen type I/III ratio in SE in MHP favors normal soft RAM muscle, with likely normalization of biomechanical properties in muscles involved in urinary continence. All these changes allow suggesting SE for assessment as a potential treatment for maternal UI injured by the maternal hyperglycemic environment. +

+

Although this set of results related to SE in mitigating the negative effects of the maternal hyperglycemic environment on DiM in the transformation into a soft health muscle, the molecular regulations of this gain muscle mass is unclear. It was suggested that distinct mechanisms regulate skeletal muscle mass recovery and hypertrophy  + + 44 + . Further studies should address this fundamental mechanism. This study as a preclinical model in the obstetrical area, the maternal-placental and fetal (MPF) unit needs to be carefully considered. Although we conducted this experiment by using the same swimming protocol established previously  + + 45– + 47 + , the whole MPF unit analysis was not performed. Thus, our successful results with SE in MHP rats environment may be analysed with caution to be considered in GDM women. Also, the present study has limitations regarding the experimental diabetes induction, which represents GDM blood glucose levels, but occurred before pregnancy  + + 47– + 49 + . In addition, the guidelines recommend that pregnant women should exercise at least 150 min/week or 30 min/day most days of the week  + + 22, + 23, + 25 + . Also, specific analysis of aerobic capacity and muscle function should be explored. +

+

In conclusion, hyperglycemia exerts an impact on DiM generating an atrophic and stiff muscle. SE intervention training during whole pregnancy in rats imposes a positive influence on DiM being capable of reversing this muscle atrophy and transforming a stiff into a soft healthy skeletal muscle. Therefore, these findings of reversal myopathy suggest that SE training during the whole pregnancy may play a therapeutic role in regulating the damages caused by the maternal hyperglycemic environment and may be considered as a potential treatment for RAM damage caused by GDM.

+ + + Materials and methods +

This current project corresponds to the translational part of the Diamater Study, a cohort Thematic Project with the financial support of São Paulo Research Foundation (FAPESP 2016/01743-5), a state research foundation in Brazil. The Diamater cohort project has been developed to investigate biomolecular muscle profiles as predictors for long-term urinary incontinence in women with Gestational Diabetes Mellitus  + + 4 + . According to the requirement to develop innovative treatments for DiM, this translational project was developed. +

+ + Ethics and animals +

All animal experiments were approved by the Institutional Animal Care and Use Committee, Faculdade de Filosofia e Ciências, São Paulo State University (UNESP), in accordance with the Brazilian Council for Control of Animal Experimentation (CONCEA) (protocol number 007/2016). The study is reported in accordance with the ARRIVE guidelines.

+

Female and male Wistar rats obtained from ANILAB were housed in a facility with constant temperature (22 ± 2 ˚C) and humidity (55 ± 5%) on a controlled 12 h light–12 h dark cycle with food and water ad libitum, in individual plastic cages during all experimental protocol. The experimental sequence is shown in Fig.  + 5. + + + +

Experimental sequence of groups.

+ +

+ +

+ +

+ + + Generation of MHP rats model +

The MHP model is the same as previous reports  + + 9– + 11, + 46, + 47 + + . To induce MHP rats’ model, newborn female Wistar received in the first day of life subcutaneously injection of STZ (Sigma + ®) diluted in citrate buffer (0.1 mol/l pH 4.5) in a dose of 100 mg/kg. Non-diabetic rats received subcutaneous injection of citrate buffer (0.1 mol/l pH 4.5)  + + 50 + . All female newborn rats were maintained with their mothers until the end of the lactation period (21 days). After this period, the mother rats were euthanized by sodium thiopental injection(Thiopentax + ®—80 mg/kg). The female newborns were maintained until adulthood. Fasting blood glucose level was determined in adult life, and used for inclusion or exclusion criteria in the study. Diabetic animals should present blood glucose level between 120 mg/dl and 300 mg/dl, and non-diabetic animals blood glucose level < 120 mg/dl  + + 51 + . +

+ + + Mating process +

At approximately day 90 of age, four diabetic and non-diabetic female rats were housed overnight with one adult male rat. The presence of spermatozoa in the vaginal smear was considered gestational day 0 [52]. After, rats were housed in individual cages until 21º day of pregnancy.

+ + + Experimental groups +

On gestational day 0, female rats were randomly allocated into four experimental groups according to sedentary lifestyle or swimming exercise: Non-Diabetic Sedentary (NDsed) (n = 13), Non-Diabetic Exercised (NDex) (n = 13), Diabetic Sedentary (Dsed) (n = 13) and Diabetic Exercised (Dex) (n = 13). Dex is the study group and the other three (NDsed, NDex and Dsed) are control groups.

+ + + Swimming exercise protocol +

The swimming exercise protocol was based on previous studies  + + 45– + 47 + and considered to be a moderate intensity exercise protocol  + + 45 + . The exercised animals were exposed to water daily temperature 31 ± 1°C for 6 days/week, from gestational day 0 until gestational day 20 on a pool at a depth of 40 cm at the water. The first training session started with 20 min, progressively increasing 10 min/day until 60 min. The sedentary rats were exposed to water daily for 15 min, at a depth of 10 cm at water temperature 31 ± 1 °C for 6 days/week, from gestational day 0 until gestational day 20, aiming not to promote physiological adaptations from exercise practice. +

+ + + Oral glucose tolerance test (OGTT) +

On gestational day 17, an OGTT was performed to confirm the glucose intolerance in diabetics  + + 50 + . Fasting glycemia and at 10, 20, 30, 60 and 120 min after administration of an intragastric glucose solution (0.2 g/mL) in a dose of 2.0 g/kg were measured. Diabetes diagnosis was confirmed with two or more blood glucose measurements > 140 mg/dL  + + 51 + . +

+ + + RAM tissue extraction +

At the end of pregnancy (gestational day 21) the dams were euthanized by sodium thiopental injection (Thiopentax, Brazil, 80 mg/kg dose). An abdominal incision was performed for RAM sample collection. The lower third on the right side of RAM was exposed, dissected, and removed for integrative morphological analysis. The fragments had approximately 0.25 cm + 2. Then, a C-section was performed and fetuses and placentas were separately analyzed in different projects. +

+ + + Integrative morphological analysis +

The samples obtained were selected into separate parts according to methodological procedures. The integrative morphological analysis is composed by morphological, morphometric, immunohistochemistry and ultrastructural RAM analysis.

+ + Morphological analysis +

For morphological and morphometric analysis, RAM samples were immersed for 24 h in neutral 10% buffered formaldehyde, transferred to 70% alcohol and maintained at room temperature and then embedded in paraffin. The 4-µm-thick sections were cut in microtome (Reichert-Jung model 820) and fixed on microscope glass slides stained with Hematoxylin & Eosin (H&E) and Picrosirius Red. H&E-stained slides were used to observe the general morphology of the RAM. Picrosirius Red-stained slides were analyzed with the color-segmentation method to determine the red (collagen) and yellow (muscle fiber) -stained tissue in the same section and used to determine muscle, fiber and collagen area and fiber diameter. The slides were analyzed in a light microscope (Olympus Corporation + ®/BX41TF coupled with DP25-4 digital câmera). The photographs were obtained with + cell Sens Ver 1.18 Olympus Corporation + ® software. +

+ + + Morphometric analysis +

For morphometric analysis of muscle and collagen area, 40 sections/group (5 animals/group, 8 sections/animal) were selected. For morphometric analysis of fiber area and diameter, 100 muscle fibers/group were selected. All analyzes were performed using CellSens Dimension Version 1.16 (Olympus Corporation + ®) image analysis software (20 × magnification). +

+ + + Immunohistochemistry +

Immunohistochemical analysis was used to stain slow-twitch and fast-twitch muscle fibers and type I and III collagen. For immunohistochemistry (N = 5 samples/group), the samples were immersed for 24 h in neutral 10% buffered formaldehyde, transferred to 70% alcohol and maintained at room temperature and then embedded in paraffin. The 4-µm-thick sections were cut in the microtome. Sections were deparaffinized and incubated with antigenic recovery for 35 min in a pressure cooker. Endogenous peroxidase was blocked using H + 2O + 2 in phosphate buffered saline (PBS). After washing, the sections were incubated with bovine serum albumin solution (BSA 3%) for 1 h. The sections were incubated overnight at 4 °C with primary antibodies against myosin heavy chain, slow (Novocastra, NCL-MHCs, #6009289, 1:20) and fast (Novocastra, NCL-MHCf, #6006929, 1:20) muscle fibers, type I Collagen (Sigma Aldrich, SAB4200678, #107M4839V, 1:100) and type III Collagen (Novus Biologicals, COL3A1, #G0809, 1:100). After incubation, the sections were washed three times for five minutes with PBS and incubated with secondary antibodies for 1 h 30 min (Goat Anti-Mouse, Abcam, 1:200). For staining, the sections were incubated with diaminobenzidine for 1 min and hematoxylin for 10 min. The slow-twitch and fast-twitch muscle fibers, and type I and III Collagen were analyzed using a light microscope (Olympus Corporation + ®/BX41TF coupled with DP25-4 digital câmera) and 40 sections/group (5 animals/group, 8 sections/animal) were selected to quantify the fiber type area and collagen type area. Also, each muscle fiber was manually selected (~ 200 slow fibers/group; ~ 330 fast fibers/group) and fiber type area and diameter were quantified using CellSens Dimension (Olympus Corporation + ®) Version 1.16 image analysis software (20 × magnification). The fiber type area was quantitatively determined, as described previously + + 10 + . +

+ + + Ultrastructural analysis +

As previously described + , the RAM tissues obtained to ultrastructural analysis (3 samples/group) were cut into small strips and immediately immersed in Karnovsky fixative for 3 h at room temperature and transferred to the refrigerator to post-fixation in 1% osmium tetroxide for 24 h and afterward, the samples were embedded in epoxy resin. Ultra-thin sections were obtained at a longitudinal orientation and stained sections were examined using transmission electron microscopy using (JEM 1400, JEOL®). +

+ + + + Statistical analysis +

GraphPad Prism® v.8.0 software was used to analyze the data. Data are expressed as mean ± standard deviation (SD). Comparisons of measurements among groups were performed by two-way ANOVA followed by Tukey’s multiple comparison tests. For all statistical comparisons, p < 0.05 was considered statistically significant.

+ + + + + + Acknowledgements +

The authors thank the support from researchers and for the access to the infrastructure of UNIPEX (Experimental Research Unit) Botucatu Medical School—UNESP and Physiological Sciences Laboratory—School of Phylosophy and Sciences—UNESP.Special thanks to Augusto Nascimento from the Physiological Science Laboratory (Campus of Marília) and PauloGeorgete from UNIPEX (Campus of Botucatu) and Cirilo (University of Marília). Transmission electron microscopy images were obtained at the Centre of Microscopy and Image (CMI), Piracicaba Dental School, UNICAMP. Technical support of Flavia Sammartino Mariano Rodrigues is appreciated. This study was supported by FAPESP—Fundação de Amparo à Pesquisa do Estado de São Paulo (Grant number 2016/01743-5), CNPq—Conselho Nacional de DesenvolvimentoCientífico e Tecnológico to MVC Rudge (305116/2018-5). BB Catinelli received a master scholarship from FAPESP—Fundação de Amparo à Pesquisa do Estado de São Paulo (2018/03361-8), JF Floriano and RLS Hallur received Posdoc scholarships from FAPESP (Grant numbers 2017/21783-4 and 2018/02979-8). L Sobrevia thanks the support from the Fondo Nacional de Desarrollo Científico y Tecnológico (FONDECYT) (Grant number 1190316), Chile, and International Sabbaticals (University Medical Centre Groningen, University of Groningen, The Netherlands) from the Vicerectorate of Academic Affairs, Academic Development Office of the Pontificia Universidad Católica de Chile.

+ + + Author contributions +

Conceptualization: M.V.C.R., A.M.P.B. and P.S.R. Data curation: B.B.C., M.V.C.R., A.M.P.B., P.S.R. and M.A.S. Formal analysis: B.B.C., P.S.R., A.M.P.B. and M.V.C.R. Funding acquisition: M.V.C.R., I.M.P.C. and A.M.P.B. Investigation/Methodology/Sample collection: B.B.C., P.S.R., A.M.C., J.F., M.A.S., S.L.F., R.G.O., N.J.S., L.C.C.U. Project administration: B.B.C., M.V.C.R., A.M.P.B., P.S.R. and I.M.P.C. Supervision: M.V.C.R., A.M.P.B. and P.S.R. Writing-original draft: B.B.C., P.S.R., M.A.S., S.L.F. Writing-review & editing: B.B.C., L.S., P.S.R., A.M.C., J.F., S.L.F., R.H., M.A.S., R.G.O., N.J.S., L.C.C.U., I.M.P.C., A.M.P.B., M.V.C.R. The Diamater Study Group designated as authors qualify for authorship as a fundamental part of this study. B.B.C. master scholarship fromFapesp. All authors have approved the final version of the manuscript and agree to be accountable for all aspects of the work.

+ + + Data availability +

The datasets used and/or analyzed during the present study are available from the corresponding author on request.

+ + + + Competing interests +

The authors declare no competing interests.

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Exerc. + 2002 + 34 + 149 + 10.1097/00005768-200205001-00834 + + + + + + + + Manchado + FDB + + + Gobatto + CA + + + Contarteze + RVL + + + Papoti + MMM + + + Máxima fase estável de lactato é ergômetro-dependente em modelo experimental utilizando ratos + Rev. Bras. Med. Esporte + 2006 + 6 + 259 + 262 + 10.1590/S1517-86922006000500007 + + + + + + + + Volpato + GT + + + Damasceno + DC + + + Kempinas + WG + + + Rudge + MVC + + + Calderon + IMP + + + Effect of exercise on the reproductive outcome and fetal development of diabetic rats + Reprod. Biomed. Online + 2009 + 19 + 852 + 858 + 1:STN:280:DC%2BD1Mfkt1Gitw%3D%3D + 20031028 + 10.1016/j.rbmo.2009.09.027 + + + + + + + + Damasceno + DC + + + + Mild diabetes models and their maternal-fetal repercussions + J. Diabetes Res. + 2013 + 2013 + 26 + 10.1155/2013/473575 + + + + + + + + Damasceno + DC + + + + Streptozotocin-induced diabetes models : Pathophysiological mechanisms and fetal outcomes + Biomed. Res. Int. + 2014 + 1 + 2014 + + + + + + + + Sinzato + YK + + + Damasceno + DC + + + Laufer-Amorim + R + + + Rodrigues + MMP + + + Oshiiwa + M + + + Taylor + KN + + + Plasma concentrations and placental immunostaining of interleukin-10 and tumornecrosis factor-α as predictors of alterations in the embryo-fetal organism and the placental development of diabetic rats + Braz. J. Med. Biol. Res. + 2011 + 44 + 206 + 211 + 1:CAS:528:DC%2BC3MXlvVSlsrg%3D + 21344139 + 10.1590/S0100-879X2011007500015 + + + + + + + + Iessi + IL + + + + Evaluation of neonatally-induced mild diabetes in rats: Maternal and fetal repercussions + Diabetol. Metab. Syndr. + 2010 + 2 + 1 + 8 + 10.1186/1758-5996-2-37 + 1:CAS:528:DC%2BC3cXnsVCjsb4%3D + + + + + Damasceno, D.C., Kempinas, W.G., Volpato, G.T., Consoni, M., Rudge, M.V.C., Paumgartten, F. + Anomalias Congênitas + : + Estudos Experimentais. (Coopmed, 2008). + + + + + Nascimento, L. Avaliação de diferentes modelos de indução do diabete moderado em ratas Wistar e suas repercussões no organismo materno-fetal. (2014). + + + + + Publisher's note +

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diff --git a/tests/stubdata/input/jats_springer_article_pubdatetype_2.xml b/tests/stubdata/input/jats_springer_article_pubdatetype_2.xml new file mode 100644 index 0000000..7c0a976 --- /dev/null +++ b/tests/stubdata/input/jats_springer_article_pubdatetype_2.xml @@ -0,0 +1,4415 @@ + + +
+ + + 13157 + 10.1007/13157.1943-6246 + + Wetlands + Official Scholarly Journal of the Society of Wetland Scientists + Wetlands + + 0277-5212 + 1943-6246 + + Springer Netherlands + Dordrecht + + + + s13157-023-01762-8 + 1762 + 10.1007/s13157-023-01762-8 + + + Original Research Article + + + + Identifying Internal Distributions and Multi-Scenario Simulation of Ecosystem Service Value in Liaohe Basin Based on Geodetector and PLUS Model + + + + + Jia + Changgeng + + 1 + + + + Fan + Yu + + 1 + + + + Wei + Chaoxiang + + 1 + + + + Luo + Kunyu + + 1 + + + + Li + Sihui + + 1 + + + + Song + Youtao + + 1 + 2 + f + + + + + https://ror.org/03xpwj629 + grid.411356.4 + 0000 0000 9339 3042 + College of Environmental Sciences + Liaoning University + + 110036 + Shenyang + People’s Republic of China + + + + + https://ror.org/018rbtf37 + grid.413109.e + 0000 0000 9735 6249 + College of Marine and Environmental Sciences + Tianjin University of Science & Technology + + 300457 + Tianjin + China + + + + + + youtaosong@sina.com + + + + 18 + 12 + 2023 + + + 1 + 2024 + + 44 + 1 + 7 + + + 5 + 12 + 2023 + + + 17 + 8 + 2023 + + + 5 + 12 + 2023 + + + 18 + 12 + 2023 + + + + © The Author(s), under exclusive licence to Society of Wetland Scientists 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law. + 2023 + + + Abstract +

Ecosystem services value (ESV) can assess the level of basin ecological restoration and provide a basis for ecological management decision-making. This study object selects Liaohe River Basin (LHB), a typical basin in Northeast China. The ecosystem service value variation caused by changes in land use cover and the spatial distribution characteristics was evaluated by employing the benefit transfer method, which is based on data sets for land use over 2000–2020. Meanwhile, geographical detector was employed to investigate the impacts and interactions of various factors driving the ESV, and predicted future changes in land and ESV by PLUS model. The results showed the following: (1) LHB land transformations mainly concentrated in the transformation between grassland, farmland and forestland. ESV in LHB decreased and then increased between 2000 and 2020 (1224 billion-928 billion-1238 billion), (2) Ecosystem service value exhibited a strong positive spatial autocorrelation, high ESV was mainly distributed in the eastern and western regions of LHB, and low ESV in the central region. (3) The variation in ecosystem service value mainly arose from the human activity intensity index of human factors. (4) In the future, the ecological protection priority scenario could improve the ESV in LHB, and the natural development priority and economic development priority scenario was not conducive to the improvement of ESV. The results showed that the ecological restoration effect of the LHB was obvious with the ecosystem service value is significantly improved. In the future, attention should be paid to control human activities and strengthen ecological protection in ESV hotspots.

+ + + Keywords + Basin ecosystem service value + Land use change transition + Spatiotemporal pattern + Drive analysis + Multi-scenario simulation + + + + publisher-imprint-name + Springer + + + volume-issue-count + 8 + + + issue-article-count + 12 + + + issue-toc-levels + 0 + + + issue-pricelist-year + 2024 + + + issue-copyright-holder + Society of Wetland Scientists + + + issue-copyright-year + 2024 + + + article-contains-esm + No + + + article-numbering-style + Unnumbered + + + article-registration-date-year + 2023 + + + article-registration-date-month + 12 + + + article-registration-date-day + 5 + + + article-toc-levels + 0 + + + toc-levels + 0 + + + volume-type + Regular + + + journal-product + NonStandardArchiveJournal + + + numbering-style + Unnumbered + + + article-grants-type + Regular + + + metadata-grant + OpenAccess + + + abstract-grant + OpenAccess + + + bodypdf-grant + Restricted + + + bodyhtml-grant + Restricted + + + bibliography-grant + Restricted + + + esm-grant + OpenAccess + + + online-first + false + + + pdf-file-reference + BodyRef/PDF/13157_2023_Article_1762.pdf + + + pdf-type + Typeset + + + target-type + OnlinePDF + + + issue-online-date-year + 2024 + + + issue-online-date-month + 2 + + + issue-online-date-day + 8 + + + issue-print-date-year + 2024 + + + issue-print-date-month + 2 + + + issue-print-date-day + 8 + + + issue-type + Regular + + + article-type + OriginalPaper + + + journal-subject-primary + Life Sciences + + + journal-subject-secondary + Freshwater & Marine Ecology + + + journal-subject-secondary + Environmental Management + + + journal-subject-secondary + Ecology + + + journal-subject-secondary + Hydrogeology + + + journal-subject-secondary + Coastal Sciences + + + journal-subject-secondary + Landscape Ecology + + + journal-subject-collection + Biomedical and Life Sciences + + + open-access + false + + + + +

Changgeng Jia and Yu Fan are co-first authors.

+ + + Copyright comment +

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

+ + + + + Introduction +

Ecosystem services (ES), the benefits that people obtain directly or indirectly from functioning ecosystems such as freshwater and food, underpin human well-being (Millennium Ecosystem Assessment + 2005; Costanza et al. + 2017). Continuous population growth, urbanization, and industrialization worldwide have imposed considerable pressures on ecosystems, altering the ecosystem services (Cumming et al. + 2014). Over the past several decades, 60% of worldwide ecosystem services have degraded, which has led to remarkable negative influences on human well-being (Costanza et al. + 2014). Therefore, understanding the spatiotemporal patterns of ecosystem services and their drivers has been a central issue for achieving natural resource management and sustainability on multiple scales (Zhang et al. + 2019). +

+

Numerous studies have shown that human activities and climate change are the main driving factors leading to changes in ecosystems and their services (Zhang et al. + 2022). The policies of governments around the world are the key to leading to changes in ecosystem services The human activities brought about by a series of policies have promoted rapid economic development and urbanization process. This has exacerbated global ecological destruction and ecosystem degradation, leading to significant loss of natural habitats and significant loss of ecosystem services (Bai et al. + 2019). This situation is most severe in developing countries, such as China (Brain and Anderson + 2020). For improving the management of preservation initiatives, the Chinese government has implemented a range of ecological restoration programs (ERPs). These ERPs include the Program of Returning Farmland to Forest/Grassland (Bennett + 2008), the Natural Forest Protection Program (Xu et al. + 2006), and the Sloping Land Conversion Program (Yin and Yin + 2010). Numerous researches have demonstrated that the implementation of ERPs can successfully enhance damaged ecosystems. Ecological restoration project is an effective way to slow down ecological degradation, solve environmental problems and restore ecosystem function (Ouyang et al. + 2016). However, the effectiveness of these restoration projects has not been well evaluated, ecosystem service evaluation provides an important basis for solving this problem. Most research on ecosystem service assessment focuses on the impact of ecological destruction, urbanization, and climate change on ecosystem services, including specific administrative regions and natural ecosystems, including urban, woodland, grassland, wetland and other ecosystems (Fan et al. + 2023a; Yang et al. + 2023; Liu et al. + 2023; Zhang et al. + 2022), however, the impact of ecological restoration policies on regional ecosystem services is not yet clear. +

+

Our research case is in the Liaohe River Basin (LHB), the ecological research in the Liaohe River Basin mainly focuses on the water quality, runoff changes, climate change, land change, and water resource carrying capacity of the basin (Lv et al. + 2014; Gong + 2022; Gao et al., + 2022; Zhu et al. + 2023), to our knowledge, the evaluation of ecological restoration effectiveness and ecosystem service value in the Liaohe River Basin is almost in a blank state. Further, information that integrates changes in land cover and ecosystem services is also hampered by a lack of quantitative and spatially explicit data. This information deficiency has limited decision-making for promoting LHB regional economic development and improving human well-being. A comprehensive study focusing on how multiple ecosystem services have changed with land cover changes, impacted by diverse policies, is thus urgently needed for sustainable development in LHB . +

+

The Liaohe River Basin (LHB) is one of the seven major rivers in China with important industrial and agricultural production base. Home to a population of 34.04 million in the LHB. It is also an important base for steel, machinery, building materials, chemical industry, grain production, and animal husbandry in China. The middle and lower reaches of the LHB are one of the most developed industrial and economic regions in China. Since the 1960s, with the acceleration of economic development, industrialization, and urbanization, numerous human activities have caused interference, especially the large discharge of industrial, agricultural, and domestic sewage. A series of problems such as poor water environment quality, river interruption, serious soil erosion, and continuous reduction of biodiversity have made ecological restoration in the LHB urgent. In 2006, the Liaohe River was listed as one of the key rivers for national governance. In 2010, the provincial government has designated the Liaohe River Reserve and established the Liaohe River Reserve Management Bureau to protect and manage the LHB through comprehensive planning, centralized management, and comprehensive protection between 2010 and 2019, the government invested a total of 18.249 billion yuan in water volume regulation, water quality restoration, and watershed ecological restoration (Fig.  + 1). +

+

+ + + +

Ecological restoration investment in the Liaohe River Basin

+ +

+ +

+ +

+

However, due to the lack of reasonable and effective evaluation methods, the effectiveness of ecological restoration is difficult to grasp in a timely manner, resulting in some unreasonable ecological restoration measures being difficult to correct in a timely manner. Not only does this result in a significant waste of human resources and materials, but it also hinders the advancement of ecological restoration and worsens the degradation of the environment. The correct evaluation of the restoration effect of river basin ecosystems has important practical significance in alleviating ecological degradation and promoting sustainable development of regional ecological environment. At the same time, in the context of global change and human interference, the land use mode of the basin has changed frequently, which has caused noticeable damage to its ecological environment. The urgent problem in achieving sustainable development of the basin ecology includes: evaluation of the ecological restoration project in the Liaohe River Basin based on the ecosystem service value; the main driving factors for the destruction and restoration of ecosystem services in the Liaohe River Basin; prediction of future land use and ecosystem services value.

+

To address the above issues, the main objectives of this study are as follows: (1) To test the effectiveness of ecological restoration policies of LHB, we evaluated the changes in ecosystem service value in the LHB from 2000 to 2020 using the equivalent factor method; (2) Based on the method of cold and hot spot analysis, the spatial heterogeneity characteristics of ecosystem service value in river basins were systematically analyzed, revealing the coupling driving mechanism of natural and human factors on the spatial distribution pattern of ecosystem service value; (3) Predicted the ecosystem service value of the LHB under different development scenarios, providing a basis for decision-makers to formulate corresponding land management policies and sustainable development in the LHB.

+ + + Materials and Methods + + Study Area +

The area of LHB is 219,000 km + 2, of which 35.7% are mountainous, 23.5% hilly, 34.5% plain and 6.3% sand dune (Fig.  + 2). In the west are the Daxing’an Mountains, Qoltu Mountain and Nuruer Tiger Mountain, with an elevation of 500 ~ 1500 m, and in the east is Jilin Hadaling, Longgang Mountain and Qianshan Mountain, with an elevation of 500 ~ 2000 m. Flow through Hebei, Inner Mongolia, Jilin and Liaoning provinces, the main rivers include Hun River, Taizi River, Daliao River, West Liaohe River, East Liaohe River. The basin’s topography slopes mainly from north to south and from east to west towards the center, forming Liaohe Plain in the middle and lower reaches, with an elevation of less than 200 m. The LHB has a typical temperate monsoon climate type, with average annual temperature of approximately 6 ◦C and annual precipitation of approximately 678 mm. The temperature distribution of LHB, high plain, low mountain, annual average between 4 ~ 9℃, from south to north, each latitude about 0.8℃, the lowest in January, the average between-9 ~ 18℃, the absolute minimum temperature, all below-30℃, July temperature is the highest, the average between 21 ~ 28℃, the absolute highest temperature between 37 ~ 43℃. + + + +

Study area

+ +

+ +

+ +

+ + + Evaluation of ESV +

Costanza et al. ( + 1997) firstly defined the scientific estimation principle and method of ESV, and estimated 17 ESV of 16 ecosystems in the world. Considering the shortcomings and reliable results of previous studies, Xie et al. ( + 2017) used the questionnaire survey based on 200 Chinese ecologists, and made many improvements to methods employed in the study of Costanza et al. ( + 1997). The ecosystem service function was divided into the food production (FP), Raw materials (RM), water resource (WTR), gas regulation (GR), Climate regulation (CR), environmental purification(EP), Water regulation(WR), Soil retention (SR), Nutrient cycling(NC), Biodiversity protection Recreation (BR) and Recreation and culture (RC) (Xie et al. + 2008). According to the study of Xie et al. ( + 2017), the ESV equivalent factor are equal to 1/7 of the average market value of grain production (Table + 1). Hence, using this foundation, this research reevaluated the economic worth of the ESV equivalent factor per unit of land area using the mean grain yield and the average market price of unprocessed grain declared by the respective governmental departments. The formula is as follows: + + + + + + + E + a + + = + + 1 + 7 + + + ∑ + + j + = + 1 + + n + + + + + m + j + + + p + j + + + q + j + + + M + + + + \documentclass[12pt]{minimal} + \usepackage{amsmath} + \usepackage{wasysym} + \usepackage{amsfonts} + \usepackage{amssymb} + \usepackage{amsbsy} + \usepackage{mathrsfs} + \usepackage{upgreek} + \setlength{\oddsidemargin}{-69pt} + \begin{document}$${E}_{a}=\frac{1}{7}\sum\nolimits_{j=1}^{n}\frac{{m}_{j}{p}_{j}{q}_{j}}{M}$$\end{document} + + + +

+

+ Ea is the economic value of unit ecosystem in Yuan / (hm + 2 a); + j is food crop type; + m + + j + is the average price of the + j grain crops in the study area; the unit is Yuan / kg; + P + + j + is the unit in kg/hm + 2; + q + + j + is the + j planting area in hm + 2; + M is the total planting area of grain crops in hm + 2. The results show that the economic value of the unit ecosystem service in the LHB is 3933.15 Yuan / (hm + 2·a) (Table + 1) (Xiao et al. + 2020; Li et al. + 2020). +

+

The ecosystem services value is calculated as follows: + + + + + + E + S + V + = + + ∑ + + i + = + 1 + + n + + + A + i + + × + + + VC + + i + + + + \documentclass[12pt]{minimal} + \usepackage{amsmath} + \usepackage{wasysym} + \usepackage{amsfonts} + \usepackage{amssymb} + \usepackage{amsbsy} + \usepackage{mathrsfs} + \usepackage{upgreek} + \setlength{\oddsidemargin}{-69pt} + \begin{document}$$ESV=\sum\nolimits_{i=1}^{n}{A}_{i}\times {VC}_{i}$$\end{document} + + + + + + + + + + + VC + + i + + = + + ∑ + + j + = + 1 + + k + + + + EC + + j + + × + + E + a + + + + \documentclass[12pt]{minimal} + \usepackage{amsmath} + \usepackage{wasysym} + \usepackage{amsfonts} + \usepackage{amssymb} + \usepackage{amsbsy} + \usepackage{mathrsfs} + \usepackage{upgreek} + \setlength{\oddsidemargin}{-69pt} + \begin{document}$${VC}_{i}=\sum\nolimits_{j=1}^{k}{EC}_{j}\times {E}_{a}$$\end{document} + + + +

+

+ ESV is ecosystem service value, unit is Yuan / a; + i is land use type; + j is ecosystem service type; + Ai is distribution area of land use type, unit is hm + 2; + VC + + i + is ecosystem service value equivalent per unit area of class i in Yuan / (hm + 2·a); + EC + + j + is ecosystem service value equivalent of item + j of land use type; + k is quantity of ecosystem service type; + E + + a + is economic value of 1 unit ecosystem service, unit is Yuan / (hm + 2·a) (Xie et al. + 2017). +

+

+ + + +

Value per unit area of ecosystem service value (yuan)

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+

Primary category

+ 		+

Subcategories

+ 		+

Cultivated land

+ 		+

Forestland

+ 		+

Grassland

+ 		+

Water area

+ 		+

Barren land

+ 		+

Urban land

+
+

Provision services

+ 		+

Food production

+ 		+

3343.24

+ 		+

1140.63

+ 		+

1494.62

+ 		+

3146.58

+ 		+

0.00

+ 		+

0.00

+
+

Raw materials

+ 		+

1573.29

+ 		+

2595.93

+ 		+

2202.61

+ 		+

904.64

+ 		+

0.00

+ 		+

0.00

+
+

Water resource

+ 		+

78.66

+ 		+

1337.30

+ 		+

1219.30

+ 		+

32606.42

+ 		+

0.00

+ 		+

0.00

+
+

Regulation services

+ 		+

Gas regulation

+ 		+

2635.26

+ 		+

8535.09

+ 		+

7748.45

+ 		+

3028.58

+ 		+

78.66

+ 		+

0.00

+
+

Climate regulation

+ 		+

1415.96

+ 		+

25565.95

+ 		+

20492.09

+ 		+

9007.08

+ 		+

0.00

+ 		+

0.00

+
+

Environmental purification

+ 		+

393.32

+ 		+

7591.12

+ 		+

6765.14

+ 		+

21829.39

+ 		+

393.32

+ 		+

0.00

+
+

Water regulation

+ 		+

1061.97

+ 		+

18643.48

+ 		+

15024.91

+ 		+

402132.75

+ 		+

118.00

+ 		+

0.00

+
+

Supporting services

+ 		+

Soil retention

+ 		+

4051.22

+ 		+

10423.04

+ 		+

9439.74

+ 		+

3657.90

+ 		+

78.66

+ 		+

0.00

+
+

Nutrient cycling

+ 		+

471.99

+ 		+

786.64

+ 		+

707.98

+ 		+

275.33

+ 		+

0.00

+ 		+

0.00

+
+

Biodiversity protection

+ 		+

511.32

+ 		+

9479.07

+ 		+

9479.07

+ 		+

10029.72

+ 		+

78.66

+ 		+

0.00

+
+

Cultural services

+ 		+

Recreation and culture

+ 		+

235.99

+ 		+

4169.22

+ 		+

3775.89

+ 		+

7433.79

+ 		+

39.33

+ 		+

0.00

+
+ +

+ + + Identifiation of Spatial Patterns + + Land Use Transfer Matrix +

The LHB undergoes a transformation of land use types due to human or natural factors, which is known as land use transfer. The Stochastic matrix of land use refers to the mutual conversion relationship (area or transfer ratio) between land use types in different periods in the same research area, which can directly reflect the source and destination of each land type (Li et al. + 2021). The formula is as follows: + + + + + + + P + + ij + + + = + + + + + + + P + 11 + + + + ⋯ + + + + P + + 1 + n + + + + + + + + + ⋮ + + + + ⋱ + + + ⋮ + + + + + + + + P + + n + 1 + + + + + + ⋯ + + + + P + + nm + + + + + + + + + + \documentclass[12pt]{minimal} + \usepackage{amsmath} + \usepackage{wasysym} + \usepackage{amsfonts} + \usepackage{amssymb} + \usepackage{amsbsy} + \usepackage{mathrsfs} + \usepackage{upgreek} + \setlength{\oddsidemargin}{-69pt} + \begin{document}$${P}_{ij}=\left[\begin{array}{ccc}{P}_{11}& \cdots & {P}_{1n}\\ \vdots & \ddots & \vdots \\ {P}_{n1}& \cdots & {P}_{nm}\end{array}\right]$$\end{document} + + + +

+ + + Spatial Autocorrelation Analysis +

To examine the spatial distribution of ESV in the LHB, the correlation and clustering patterns were analyzed using Moran’s I. Moran’s I is a widely used statistical measure that determines if there is a significant correlation between attribute values and their neighboring elements. Nonzero values indicate a correlation in the LHB data. According to Liu et al. ( + 2020c), a negative Moran’s I value indicates a negative spatial correlation for LHB,whereas a positive value indicates a positive correlation. +

+ + + Hotspot Analysis of the Selected Ecosystem Services +

Hotspot analysis is a specialized method of spatial analysis that has been utilized to identify regions where there are concentrated high values for a particular variable of significance. It has been extensively employed to pinpoint prime areas that require attention for the preservation of biodiversity and ecosystem services (Li et al. + 2017; Schröter et al. + 2017; Fan et al. + 2023a). To identify areas that can offer substantial ecosystem service provisions, we utilized Gi* statistics,a functionality integrated into ArcGIS 10.3. The process of determining the distribution of hotspots for ecosystem services involved several steps. Initially, zonal statistics were applied to compute the cumulative sum of each chosen ecosystem service type within every county within the LHB region. Subsequently, the Hotspot Analysis (Getis-Ord Gi*) tool was employed to pinpoint the hotspots where ecosystem services are most prominently provided (Wang et al. + 2022; Fan et al., + 2023b). +

+ + + + Geographical Detector +

Driving forces can ascertain the process of land cover transformation and unveil the mechanism behind regional ecological shifts. In particular, geographical detectors refer to a collection of statistical techniques that can identify spatial variations and uncover the concealed factors that drive such changes. Ever since Wang et al. ( + 2010) introduced the geographic detector, which has been extensively employed in driving force analyses (Wu et al. + 2022). +

+

We proposes two types of 8 driving factors from the perspectives of natural environment and socio-economic factors (Zhang et al. + 2021): (1) Natural environment driving factors: DEM (digital Elevation Model), Road distances, River distances, NDVI (normalized vegetation index), Annual precipitation (AP) Annual temperature (AT); (2) Socio-economic factors: GDP, HAI (human active index), Population density (PD). Here, we use the natural discontinuity method to discretization the data. +

+ + + PLUS Model + +

The PLUS model is a new land use simulation model proposed by Liang et al. ( + 2021), which can better simulate the patch level change of multiple classes of land use types, It consists of a new land-use expansion analysis strategy (Land Expansion Analysis Strategy, LEAS) and based on multi-type random plaque seeds (CA based on multi-type random patch seeds, Cellular Automata for CARS) (Cellular Automata, CA) model consists of two major parts. PLUS model combining the advantages of transformation analysis strategy (TAS) and pattern analysis strategy (PAS) can better explore the inducement of various kinds of land use changes, simulate the changes of multiple types of land use patch level, and realize the simulation of multiple land use types. We set three development scenario models, including natural development priority (NDP), ecological protection priority(EPP), economic development priority (EDP). +

+ + + Natural Development Priority (NDP) +

Represented the historical trend of land use and land cover, being calculated based on the initial transfer matrix of LULC from 2000 to 2020. Based on the land use change rate and the driving factors of the base year from 2000 to 2020, the Markov model module in the PLUS model was used to predict the future scale of each category without considering the policy planning restrictions.

+ + + Ecological Protection Priority (EPP) +

Described the local government to strengthen the protection of woodland, grassland, and waters to achieve the harmonious coexistence of man and nature and sustainable development by strictly limiting construction land expansion. These areas were used as spatial constraints, and the conversion of woodland, grassland and waters to construction land and cultivated land was controlled. According to the ecological benefit level of land use type, it was converted in turn: woodland, waters, grassland, and other.

+ + + Economic Development Priority (EDP) +

Described the situation of local priority development of construction land to meet economic development needs. According to the trend of construction land in the study area from 2000 to 2020, the maximum growth of construction land was taken as the goal. The construction land conversion was prioritized according to the principle of one-way conversion of low-to-high-level land: construction land, cultivated land, woodland, grassland and waters (Su et al. + 2023). +

+ + +

Conversion cost matrix. a, b, c, d, e, and f represent cultivated land, woodland, grassland, waters, construction land, and unused land, respectively, the same figure below; 0 means that it cannot be transformed, and 1 means that it allows transformation, the conversion cost matrix was shown in Table  + 2. +

+ + +

+ + + +

Conversion cost matrix

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+ +

EDP

+ 		+

EPP

+ 		+

NDP

+
+ +

a

+ 		+

b

+ 		+

c

+ 		+

d

+ 		+

e

+ 		+

f

+ 		+

a

+ 		+

b

+ 		+

c

+ 		+

d

+ 		+

e

+ 		+

f

+ 		+

a

+ 		+

b

+ 		+

c

+ 		+

d

+ 		+

e

+ 		+

f

+
+

a

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

0

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+
+

b

+ 		+

1

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+
+

c

+ 		+

1

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+
+

d

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

1

+ 		+

0

+ 		+

1

+
+

e

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

0

+ 		+

1

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

0

+ 		+

1

+ 		+

0

+
+

f

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+ 		+

1

+
+ +

+ + +

We simulated the land use cover spatial pattern of LHB in 2020 with 2010 as the starting year. Then, we compared the simulated land use cover with actual land use cover data in 2020 to verify the reliability of the simulation results. The kappa value ( + 5) was used to test the degree of consistency between the simulated and actual ESV grids. +

+ + +

+ + + + + + K + a + p + p + a + = + ( + P + O + - + P + C + ) + / + ( + P + P + - + P + C + ) + + + \documentclass[12pt]{minimal} + \usepackage{amsmath} + \usepackage{wasysym} + \usepackage{amsfonts} + \usepackage{amssymb} + \usepackage{amsbsy} + \usepackage{mathrsfs} + \usepackage{upgreek} + \setlength{\oddsidemargin}{-69pt} + \begin{document}$$Kappa=(PO-PC)/(PP-PC)$$\end{document} + + + +

+ + +

+ PO is the overall classification accuracy, + PC is the actual simulation.accuracy, and + PP is the ideal simulation accuracy (100%). In general, when kappa ≥ 0.75, the agreement between the actual and simulated degree is high. When 0.4 ≤ kappa ≤ 0.75, the agreement is general. When kappa ≤ 0.4, the agreement is low, (Zhao et al. + 2020), By comparing the actual and simulated land use over in 2020 (Fig.  + 3), the Kappa coefficient is 0.788. +

+ + +

+ + + +

Status and simulated land use type in 2020

+ +

+ +

+ +

+ + + + Data Sourcing +

Multiple sources were utilized to acquire spatial and statistical data. Spatial data included: land-use and land-cover (LULC) data from the year of 2000, 2005, 2010, 2015, and 2020, the spatial resolution is set at 30 m. The date is provided by Date Center for Resource and Environment Sciences, Chinese Academy of Science (RESDC) ( + http://www.Resdc.cn). It interpreted from the datasets of USGS Landsat 5 and 8 Surface Reflectance Tier 1. Including forestland (woodland, shrub forest, sparse forest), farmland (paddy field, dry land), grassland, water area (rivers, lakes, reservoir), construction land (urban, mining area), barren land. The combined accuracy exceeded 89%, with Kappa coefficients exceeding 0.85. To calculate terrain factors and slopes, a digital elevation model (DEM) sourced from + https://www.gscloud.cn/ was utilized. Soil data was acquired from the Harmonized World Soil Database (HWSD) available at + http://www.fao.org/. The meteorological station data for the study area were obtained from the China Meteorological Data Service Centre ( + https://data.cma.cn/). To convert the point data into raster data, the monthly precipitation, temperature, and sunshine percentage data from 2000 to 2020 were interpolated using the thin-plate splines method. The statistical data consisted of annual food production, which came from the statistical yearbooks. To ensure consistency, all the data were transformed into a common spatial reference system (WGS1984, UTM Zone 49 N), and the raster data grid was adjusted to a resolution of 30 m × 30 m. +

+ + + + Result and Discussion + + Spatiotemporal Change in Land Use +

The land use change (LUC) dynamics in the LHB area is shown in Fig.  + 4. From 2000 to 2020, the cultivated land area in the LHB was the largest, accounting for approximately 50% of the total area, mainly concentrated in the southeast. Next are forest and grassland, accounting for approximately 17–20% of the total area, mainly distributed in the northwest region. Construction land accounts for approximately 8–12%, mainly concentrated in urban areas. The proportion of wetlands is the lowest, about 2%, mainly distributed in the eastern region. Between 2000 and 2020, the woodland construction land and grassland in LHB area increased, while the cultivated land and water area were significantly degraded (Table  + 3). + + + +

Land use dynamics in the LHB from 2000 to 2020

+ +

+ +

+ + + + +

Changes in the areas of ecosystem types in LHB (2000–2020)

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+

Type

+ 		+

2000

+ 		+

2005

+ 		+

2010

+ 		+

2015

+ 		+

2020

+
+

Farmland

+ 		+

124681.40

+ 		+

120573.46

+ 		+

120399.69

+ 		+

122989.28

+ 		+

117951.33

+
+

Forestland

+ 		+

37045.84

+ 		+

38352.68

+ 		+

38995.67

+ 		+

39917.47

+ 		+

40400.41

+
+

Grassland

+ 		+

77631.03

+ 		+

81163.16

+ 		+

78860.32

+ 		+

74335.21

+ 		+

78441.80

+
+

Water area

+ 		+

1736.63

+ 		+

1718.71

+ 		+

1644.13

+ 		+

1622.82

+ 		+

1492.40

+
+

Barren land

+ 		+

5787.15

+ 		+

4253.69

+ 		+

4823.65

+ 		+

4366.55

+ 		+

4152.91

+
+

Urban land

+ 		+

11463.27

+ 		+

12283.63

+ 		+

13621.88

+ 		+

15114.00

+ 		+

15906.48

+
+ +

+

Figure  + 5 displays that from 2000 to 2020, the main types of land cover transferred out from the LHB were grassland, farmland, and forestland, corresponding to 4,336,863 ha, 3,119,759 ha, and 457,400 ha. From 2000 to 2020, the characteristics of land cover transfer remained consistent according to the three primary types of land transfer. Grassland is the land type with the most land change in the LHB region, and the grassland is mainly converted into farmland, with the transition amount increasing first and then decreasing during 2000–2020. The transition of grassland to forestland is increasing during 2000–2020, which is consistent with the trend of farmland transition. The conversion of farmland to forest land is increasing year by year. The increase in construction land mainly comes from the transition of arable land. The degradation of water area is mainly due to the transformation of water area into farmland. + + + +

Land use transition of LHB during 2000–2020

+ +

+ +

+ +

+ + + Characteristics of ESVs in Different Land Use +

From 2000 to 2020, the ESV in the LHB region showed a trend of first decreasing and then increasing (Fig.  + 6; Table  + 4). From 2000 to 2010, the ESV decreased by 24%, from 1224.42 billion yuan to 928.21 billion yuan. From 2010 to 2020, the ESV increased by 33%, from 928.24 billion yuan to 1238.2 billion yuan. The total ESV increased from 1224.45 billion yuan to 1238.24 billion yuan, with provision service value decreasing from 125.45 billion yuan to 123.25 billion yuan. Both regulatory support services and cultural services are showing an increasing trend. + + + +

Spatial distribution map of the ecosystem service value

+ +

+ +

+ + + + +

Ecosystem services value in the LHB (100 million yuan)

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+

Types of ecosystem services

+ 		+

2000

+ 		+

2005

+ 		+

2010

+ 		+

2010

+ 		+

2020

+
+

ESV

+ 		+

Ratio%

+ 		+

ESV

+ 		+

Ratio%

+ 		+

ESV

+ 		+

Ratio%

+ 		+

ESV

+ 		+

Ratio%

+ 		+

ESV

+ 		+

Ratio%

+
+

Provision services

+ 		+

+ Food production +

+ 		+

580.06

+ 		+

4.74

+ 		+

573.04

+ 		+

4.56

+ 		+

509.99

+ 		+

5.49

+ 		+

572.40

+ 		+

4.71

+ 		+

561.84

+ 		+

4.54

+
+

+ Raw materials +

+ 		+

464.46

+ 		+

3.79

+ 		+

469.15

+ 		+

3.73

+ 		+

377.69

+ 		+

4.07

+ 		+

461.90

+ 		+

3.80

+ 		+

464.15

+ 		+

3.75

+
+

+ water resource +

+ 		+

210.44

+ 		+

1.72

+ 		+

215.58

+ 		+

1.72

+ 		+

162.63

+ 		+

1.75

+ 		+

206.42

+ 		+

1.70

+ 		+

207.42

+ 		+

1.68

+
+

Regulation services

+ 		+

+ Gas regulation +

+ 		+

1250.84

+ 		+

10.22

+ 		+

1278.34

+ 		+

10.17

+ 		+

956.75

+ 		+

10.31

+ 		+

1244.90

+ 		+

10.24

+ 		+

1267.14

+ 		+

10.23

+
+

+ Climate regulation +

+ 		+

2727.61

+ 		+

22.28

+ 		+

2827.34

+ 		+

22.50

+ 		+

1979.53

+ 		+

21.33

+ 		+

2730.07

+ 		+

22.45

+ 		+

2818.19

+ 		+

22.76

+
+

+ Environmental purification +

+ 		+

894.81

+ 		+

7.31

+ 		+

925.98

+ 		+

7.37

+ 		+

644.38

+ 		+

6.94

+ 		+

890.60

+ 		+

7.32

+ 		+

917.12

+ 		+

7.41

+
+

+ Water regulation +

+ 		+

2686.04

+ 		+

21.94

+ 		+

2751.67

+ 		+

21.90

+ 		+

2100.58

+ 		+

22.63

+ 		+

2642.37

+ 		+

21.73

+ 		+

2655.25

+ 		+

21.44

+
+

Supporting services

+ 		+

+ Soil retention +

+ 		+

1629.37

+ 		+

13.31

+ 		+

1659.48

+ 		+

13.21

+ 		+

1267.56

+ 		+

13.66

+ 		+

1620.81

+ 		+

13.33

+ 		+

1643.69

+ 		+

13.27

+
+

+ Nutrient cycling +

+ 		+

143.30

+ 		+

1.17

+ 		+

144.88

+ 		+

1.15

+ 		+

115.46

+ 		+

1.24

+ 		+

142.39

+ 		+

1.17

+ 		+

143.27

+ 		+

1.16

+
+

+ Biodiversity protection +

+ 		+

1167.58

+ 		+

9.54

+ 		+

1211.01

+ 		+

9.64

+ 		+

816.97

+ 		+

8.80

+ 		+

1161.45

+ 		+

9.55

+ 		+

1201.02

+ 		+

9.70

+
+

Cultural services

+ 		+

+ Recreation and culture +

+ 		+

489.69

+ 		+

4.00

+ 		+

507.30

+ 		+

4.04

+ 		+

350.33

+ 		+

3.77

+ 		+

487.92

+ 		+

4.01

+ 		+

503.26

+ 		+

4.06

+
+

Total

+ 		+

12244.20

+ 		+

100.00

+ 		+

12563.76

+ 		+

100.00

+ 		+

9281.87

+ 		+

100.00

+ 		+

12161.23

+ 		+

100.00

+ 		+

12382.36

+ 		+

100.00

+
+ +

+

ESV had clear spatial heterogeneity in the LHB, the ESV increases outward from the LHB center, and high ESV areas are mainly distributed in the western and eastern regions. The coverage of forest and grassland in these areas is relatively high. Among the various land covers in LHB, forest can provide the highest regulatory support and cultural services (Fig.  + 5), while low ESV is mainly distributed in the central region, which is mainly concentrated in construction land and cannot provide ecosystem service value. Other moderate ESV areas are mainly composed of cultivated land, which can provide a large amount of product supply services. +

+ + + Spatial Agglomeration of ESVs +

This study validated the spatial correlation of ecological risk in the research area, Moran’s I scatterplots and global spatial autocorrelation analyses were conducted. The results revealed that the LHB exhibited strong positive spatial correlation across the period of 2000–2020 (Fig. + 7), with Moran’s I values of 0.8113, 0.8103, 0.8119, 0.8082, 0.8096, and 0.8161 (Table + 5), respectively. This significant Moran value indicates a clear clustering pattern in the spatial distribution of LHB, supporting the findings of Liu et al. ( + 2020). +

+

+ + + +

Spatial autocorrelation of ecosystem service in 2000–2020

+ +

+ +

+ +

+

+ + + +

Moran’I index table

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+

Year

+ 		+

Moran + I +

+ 		+

Z(I)

+ 		+

P(I)

+
+

2000

+ 		+

0.7828

+ 		+

117.64

+ 		+

0.00

+
+

2005

+ 		+

0.7809

+ 		+

117.64

+ 		+

0.00

+
+

2010

+ 		+

0.7807

+ 		+

117.31

+ 		+

0.00

+
+

2015

+ 		+

0.7811

+ 		+

117.39

+ 		+

0.00

+
+

2020

+ 		+

0.7791

+ 		+

117.09

+ 		+

0.00

+
+ +

+

Figure + 8 displayed the hotspots for various ecosystem services in 2000 and 2020, indicating their respective confidence levels. It is widely accepted that a confidence level of P < 0.05 (i.e.,95% confidence level) is considered statistically significant (Li et al. + 2017). Therefore, our study primarily focused on hotspots with confidence levels exceeding 95%, as these were deemed crucial for the provision of ecosystem services. The spatial distribution pattern of ecosystem services cold hotspots in the LHB region from 2000 to 2020 is similar, with hotspots mainly distributed in the western and eastern regions. This is because the ecological vegetation coverage in the western and eastern regions is high, with higher elevations and rich terrain. Forests and grasslands are mainly concentrated in this area and can provide various ecosystem services (Du et al. + 2023). The central and eastern regions are where the majority of the cold spot area is found. These areas are mainly composed of grassland and arable land, and their aggregation is relatively scattered. +

+

+ + + +

Hotspots of ecosystem services in LHB

+ +

+ +

+ +

+ + + Mechanisms of Drive Changes in ESVs +

The results from differentiating and detecting factors indicated that the spatial differentiation of ESV in the study region was influenced by multiple factors (Table  + 5). +

+

The Q values were ranked as follows: HAI (0.424) > AP(0.298) > DEM(0.232) > AT(0.211) > other factors (< 0.2). HAI was the main driver of the differences in ecosystem services value (ESV) across the study area. Factors related to human actions had a bigger impact on ESV compared to natural factors. The analysis showed that the combined effects of pairs of factors were more significant than the individual effects of any single factor. These interactions mostly contributed to enhancing the effects of both factors involved (Table  + 6; Fig.  + 9). The factors LA and HAI were strongly influenced by AP and NDVI,as indicated by significant factor interactions (0.796, 0.817). Additionally, the q values for the interactions between LA and other factors,as well as HAI and other factors, were several times higher than the values for the independent actions of these factors. + + + + +

The contributions (Q statistics) of different factors to ESV variation

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+

Factor

+ 		+

Q statistic

+ 		+

P value

+
+

DEM

+ 		+

0.232

+ 		+

0.000

+
+

GDP

+ 		+

0.052

+ 		+

0.000

+
+

Road distances

+ 		+

0.037

+ 		+

0.000

+
+

HAI

+ 		+

0.424

+ 		+

0.000

+
+

River distances

+ 		+

0.018

+ 		+

0.000

+
+

NDVI

+ 		+

0.153

+ 		+

0.000

+
+

Annual precipitation (AP)

+ 		+

0.298

+ 		+

0.000

+
+

Population density (PD)

+ 		+

0.043

+ 		+

0.000

+
+

Annual temperature (AT)

+ 		+

0.211

+ 		+

0.000

+
+ + + + +

Interactive effects between the factors

+ +

+ +

+ +

+

Among the different factors studied,the combined influence of LA and NDVI, AP and AD had the most noteworthy impact on ESV. The average q values for these interactions were consistently above 0.5, indicating their significant effects. Meanwhile, out of all the factors, LA and NDVI had the highest q value of 0.817, highlighting their substantial contribution to the spatial variation of ESV across the study area. Both LA and AP had q values greater than 0.2, indicating that the spatial variation of ESV in the LHB was influenced by a combination of human factors, natural factors. Among these, human factors had the greatest impact.

+ + + Multi-Scenario Simulation of Land Pattern and ESVs +

The land use in the LHB have undergone significant changes under three scenarios (Fig.  + 10). The area of farmland land has decreased under all three scenarios, with the EPP scenario showing the largest decrease of 8011km + 2, while the forest area has increased, the EPP scenario shows the largest increase of 5822km + 2. Under the NDP and EDP scenarios, the grassland area significantly decreased by 7765km + 2 and 7735km + 2, while the grassland increased 1157km + 2 under the EPP senarios. The water area slightly increased under the NDP and EPP scenarios, while decreased under the EDP scenario. The area of barren land significantly decreased in all scenarios, with EDP mode having the highest reduction. The urban land shows an increasing trend, with the smallest increase in urban land under the EPP scenario. +

+

+ + + +

Spatial distribution of land use under three different scenarios in 2060

+ +

+ +

+ +

+

The distribution of ESV in LHB projected under different scenarios was shown in Fig.  + 11. The distribution of ESV in 2026 under various scenarios is similar, with CR being the highest, approaching 300 billion yuan, followed by WR, both exceeding 250 billion yuan. Moreover, the value of WR and CR under the EPP scenario is much higher than that of NDP and EDP. SR, EP, and GR are all between 100 and 200 billion yuan, while other services do not exceed 100 billion yuan, with EPP slightly higher than NDP and EDP, and EDP being the lowest. +

+

+ + + +

The distribution of ESV in LHB projected under different scenarios

+ +

+ +

+ +

+

The value of ESV in LHB projected under different scenarios was shown in Table  + 7, The ESV in the LHB region improved under the EPP scenario, with the ESV in 2060-EPP increasing by 50.74 billion yuan compared to 2020. Regulatory services are the main driving factor, with an increase of 38 billion yuan compared to 2020. Support services and culture services increased by 10.33 billion yuan and 2.78 billion yuan respectively. The ESV under the NDP and EDP scenarios decreased by 25 billion yuan and 36.44 billion yuan respectively compared to 2020. The change in ESV in the NDP scenario is attributed to a decrease in product supply and regulatory services, while the change in ESV in EDP is mainly attributed to a decrease in regulatory and support services. +

+

+ + + +

The value of ESV in LHB projected under different scenarios

+ + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + +
+

Year

+ 		+

2020

+ 		+

2060-NDP

+ 		+

2060-EPP

+ 		+

2060-EDP

+
+ +

ESV

+ 		+

ESV

+ 		+

Change

+ 		+

ESV

+ 		+

Change

+ 		+

ESV

+ 		+

Change

+
+

Provision services

+ 		+

1234.54

+ 		+

1196.27

+ 		+

-38.38

+ 		+

1231.26

+ 		+

-3.38

+ 		+

1187.37

+ 		+

-47.26

+
+

Regulation services

+ 		+

7664.75

+ 		+

7526.47

+ 		+

-138.38

+ 		+

8045.24

+ 		+

380.52

+ 		+

7452.86

+ 		+

-211.94

+
+

Supporting services

+ 		+

2990.77

+ 		+

2965.77

+ 		+

-25

+ 		+

3093.77

+ 		+

103

+ 		+

2899.15

+ 		+

-91.63

+
+

Cultural services

+ 		+

503.78

+ 		+

495.18

+ 		+

-8.69

+ 		+

530.77

+ 		+

27

+ 		+

490.24

+ 		+

-13.53

+
+

Total ESV

+ 		+

12393.79

+ 		+

12143.47

+ 		+

-250.32

+ 		+

12900.82

+ 		+

507.14

+ 		+

12029.46

+ 		+

-364.33

+
+ +

+ + + + Discussion +

The study results showed big overall changes in the land use of the study region, indicating an extremely unstable ecosystem structure in the area (Table + 2; Fig. + 4). Complex dynamic conversions between different land-use categories and different levels within a category occurred during the study period. Throughout the study period,intricate and dynamic shifts were observed between various land-use classifications and within each category. The main conversions primarily took place in agricultural land, which experienced concentrated human activities. This result corresponds to one of the main characteristics of resource use in Northeast China (Mao et al. + 2019a, + b; Jia et al. + 2022). Changes in land use encompass modifications in the intensification and conversion of land utilization, ultimately leading to alterations in ecosystem services value (Song and Deng + 2017). +

+

The results of ESV in the LHB region show a trend of first decreasing and then increasing, which is due to the rapid economic development promoting urbanization, the increase in human activity intensity leading to an increase in construction land, as well as the degradation of water and grassland, which leads to a decrease in ESV in the LHB region. After 2010, ESV significantly increased, mainly due to a significant increase in forest area with ecological restoration, from 38995.67 km + 2 to 39917.47 km + 2. The ESV has increased from 928.18 to 1238.23 billion yuan, which indicates that the governance of the LHB has achieved significant results. This is consistent with the results of the existing relevant studies. Grain-for-Green and Grain-for-Blue Policies of Shandong province has increased net primary productivity and soil erosion service value by 20% and 40% (Song et al., + 2015). The value of ESV in Lishui city increased from 143.28 billion yuan in 2009 to 150.23 billion yuan in 2019 under the ecological restoration policy (Tang et al. + 2022). Ecological restoration of Nature Reserves in Ningxia had a positive effect on the value of ecosystem services during 2000–2010 (Wang et al. + 2014). +

+

In addition, we also explore the spatial distribution of ESVs in the LHB through spatial analysis. The results of spatial autocorrelation analysis in LHB region show that the ESV in the LHB have very high spatial autocorrelation, which indicates that the spatial concentration of ESV in LHB region is very high. The results of the cold hot spot analysis also prove this, as the ESV hot spot area is mainly distributed in the western and eastern regions of the LHB. Ecological degradation of these region could cause a significant decline in multiple ecosystem services (Qiu and Turner + 2013). which poses a serious threat to human well-being. Therefore, these areas should be priority areas for LHB ecological protection to ensure regional ecological security. We predicted the changes in land and ESV under three scenarios based on the PLUS model in 2060, and the results showed that ESV only increased under the environmental protection scenario, while natural development and economic development scenarios reduced ESV. This indicates that the ecological restoration work in the LHB area is not yet complete, and it is necessary to increase the protection of the ecosystem. We should continue to protect and restore hotspots of ecosystem services in the future, this is a long-term process. It is similar to the research results of Wang et al. ( + 2021) that the ecological restoration projects did not increase the value of all ecosystem services in Northeast China, ecological protection policies should be continued in the future. +

+

Additionally, we discovered that the urban region of LHB does not align with the distribution of ecological service hotspots. We also found that the urban area of LHB does not match the distribution of ecosystem service hotspots, which limits the supply of ecosystem services to human society possible interventions include the development of ecological corridors in the region to strengthen the flow of ESV while coordinating with regional economic development. These ecological corridors can also serve as landscape amenities,boosting the economic benefits associated with an improved ecological environment (Luo et al. + 2022). +

+

This study was a quantitative analysis of the relative importance of ESV drivers in the study region, and interactions between factors were identified. The results of the analysis revealed that the spatial differentiation in the ESV of the study region is attributed to the interactions between multiple factors. Among these factors, the HAI for human activities was identified as the primary driver. This result is consistent with those of existing studies on drivers of ecosystem services (Pan et al. + 2021; Luo et al. + 2020), which indicates that ESV in the LHB is most affected by HAI. HAI is used to describe the overall intensity of human activities on the value of land ecosystem services in a certain area. It refers to the impact index of land change caused by human activities on the value of ecosystem services, which also indicates that land change is one of the main driving factors affecting the ESV of LHB ( ). The results of the land transfer matrix also showed that the LHB area experienced significant land changes in the process of destruction and restoration. During the period from 2000 to 2010, the degradation of cultivated land and wetland suppressed the supply of ESV, which reduced the value of ecosystem services such as food production and climate regulation. With the gradual recovery of forestland, the ESV of 2010–2020 increased significantly, and the forestland could provide various ecosystem services, including gas regulation, climate regulation, environmental purification, soil retention, nutrient cycling service. +

+

Rapid socioeconomic development has accelerated the intensity of human exploitation of resources from the natural environment, forcibly converting regional natural landscapes into semi-natural (e.g., farmland) and artificial landscapes (Ma et al. + 2018). Simultaneously, the population has been steadily increasing,resulting in an increased demand for both construction lands and food. Consequently, there has been a continuous reclamation of substantial non-agricultural areas and an intensification of regional land use within this context. Ultimately, this will result in a reduction of ESV. +

+

Even though this study has adjusted the value coefficient based on the current conditions of the study area, there is still a level of uncertainty.

+

This research utilized the equivalent coefficient of ESV per unit area to estimate ESV in the middle and lower sections of the LHB. However, the determination of this equivalent ESV coefficient is subjective, which impacts the precision of the ESV assessment findings (Zhang et al. + 2020. Zheng et al. + 2020). To address these concerns,it is necessary to develop more accurate evaluation models for the research area that can account for these influences. Furthermore, relying solely on economic value to estimate the value of regional ecosystem services fails to capture the worth of intangible services like aesthetic and cultural contributions. Hence, the evaluation results currently fail to accurately depict the full range of service functions and values provided by the study area ecosystem. Consequently, for future research, it is crucial to develop an assessment model that more comprehensively embodies the ecosystem service functions in the study area and aligns with the actual conditions in the study area, for mitigating the influences (Pan et al. + 2021). +

+ + + Conclusions +

This study utilized the benefit transfer method to assess the ESV of the midstream and downstream regions of the Liaohe River Basin (LHB), and the spatiotemporal distribution of ESV was analysed accordingly. Afterwards, the Geographical detector model was used to measure the contributions of factors that drive the ecosystem service value. The primary findings demonstrated that the land use and land cover structure in the study area was not stable as a result of both ecological destruction and restoration, which were marked by significant human activities. Over the course of the 20-year study period, there was a continuous increase in the expansion of forested and grassy areas of land. The total ESV in LHB area decreased first and then increased, which indicates that the restoration of LHB basin was effective. Moreover, the spatial clustering of ESV in LHB is high, with ESV hotspots mainly concentrated in the western and eastern regions. The intensity of human activity is the main driver of ESV variation.

+ + + + + Author Contribution +

Changgeng Jia.

+

Contributions: The idea construction and writing of the paper.

+

Yu Fan.

+

Contributions: Paper guidance and revision.

+

Chaoxiang Wei.

+

Contributions: Value accounting of ecosystem services in the paper.

+

Kunyu Luo.

+

Contributions: Ecological model construction in the paper.

+

Sihui Li.

+

Contributions: Related accounting data support.

+

Youtao Song.

+

Contributions: Paper guidance and revision.

+ + + Funding +

No funding was obtained for this study.

+ + + Data Availability +

The datasets used or analysed during the current study are available from the corresponding author on reasonable request.

+ + + Declarations + + Competing Interests +

The authors declare that there is no conflict of interest.

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diff --git a/tests/stubdata/output/jats_a+a_subtitle.json b/tests/stubdata/output/jats_a+a_subtitle.json index 3e9fff2..10aa712 100644 --- a/tests/stubdata/output/jats_a+a_subtitle.json +++ b/tests/stubdata/output/jats_a+a_subtitle.json @@ -613,7 +613,13 @@ } ], "pubDate": { - "electrDate": "2023-03-00" + "electrDate": "2023-03-09", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2023-03-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_apj_967_1_35.json b/tests/stubdata/output/jats_apj_967_1_35.json index f0525cb..914cec7 100644 --- a/tests/stubdata/output/jats_apj_967_1_35.json +++ b/tests/stubdata/output/jats_apj_967_1_35.json @@ -158,7 +158,7 @@ } ], "openAccess": { - "license": "\n\nOriginal content from this work may be used under the terms of the\n\t\t\t\t\t\tCreative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.\n\t\t\t\t\t", + "license": "Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, diff --git a/tests/stubdata/output/jats_iop_blank_affil_removed.json b/tests/stubdata/output/jats_iop_blank_affil_removed.json index a294f36..1ca9bdf 100644 --- a/tests/stubdata/output/jats_iop_blank_affil_removed.json +++ b/tests/stubdata/output/jats_iop_blank_affil_removed.json @@ -302,7 +302,7 @@ } ], "openAccess": { - "license": "\n\nOriginal content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", + "license": "Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, diff --git a/tests/stubdata/output/jats_iop_blank_affil_removed2.json b/tests/stubdata/output/jats_iop_blank_affil_removed2.json index 678eb2d..b4b78de 100644 --- a/tests/stubdata/output/jats_iop_blank_affil_removed2.json +++ b/tests/stubdata/output/jats_iop_blank_affil_removed2.json @@ -160,7 +160,7 @@ } ], "openAccess": { - "license": "\n\nOriginal content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", + "license": "Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, diff --git a/tests/stubdata/output/jats_iop_jinst_17_05_P05009.json b/tests/stubdata/output/jats_iop_jinst_17_05_P05009.json index 561bed9..a961b85 100644 --- a/tests/stubdata/output/jats_iop_jinst_17_05_P05009.json +++ b/tests/stubdata/output/jats_iop_jinst_17_05_P05009.json @@ -9519,7 +9519,7 @@ } ], "openAccess": { - "license": "\nPublished by IOP Publishing Ltd on behalf of Sissa Medialab. Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", + "license": "Published by IOP Publishing Ltd on behalf of Sissa Medialab. Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", "licenseURL": "http://creativecommons.org/licenses/by/4.0", "open": true }, diff --git a/tests/stubdata/output/jats_iop_no_orcid_tag.json b/tests/stubdata/output/jats_iop_no_orcid_tag.json index 2232d6e..e4c7448 100644 --- a/tests/stubdata/output/jats_iop_no_orcid_tag.json +++ b/tests/stubdata/output/jats_iop_no_orcid_tag.json @@ -5344,7 +5344,7 @@ } ], "openAccess": { - "license": "\n\nOriginal content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", + "license": "Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, diff --git a/tests/stubdata/output/jats_iop_preprint_in_record.json b/tests/stubdata/output/jats_iop_preprint_in_record.json index eef461f..ff80532 100644 --- a/tests/stubdata/output/jats_iop_preprint_in_record.json +++ b/tests/stubdata/output/jats_iop_preprint_in_record.json @@ -67,7 +67,7 @@ } ], "openAccess": { - "license": "\nPublished by IOP Publishing Ltd on behalf of Sissa Medialab. Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", + "license": "Published by IOP Publishing Ltd on behalf of Sissa Medialab. Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 licence. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.", "licenseURL": "http://creativecommons.org/licenses/by/4.0", "open": true }, diff --git a/tests/stubdata/output/jats_iucr_d-60-02355.json b/tests/stubdata/output/jats_iucr_d-60-02355.json index ae90a25..a764f5d 100644 --- a/tests/stubdata/output/jats_iucr_d-60-02355.json +++ b/tests/stubdata/output/jats_iucr_d-60-02355.json @@ -183,7 +183,7 @@ } ], "openAccess": { - "license": "Prior permission is not required to reproduce short quotations, tables and figures from this article, provided the original authors and\n source are cited. For more information, see http://journals.iucr.org/services/copyrightpolicy.html." + "license": "Prior permission is not required to reproduce short quotations, tables and figures from this article, provided the original authors and source are cited. For more information, see http://journals.iucr.org/services/copyrightpolicy.html." }, "pagination": { "firstPage": "2355", diff --git a/tests/stubdata/output/jats_iucr_d-75-00616.json b/tests/stubdata/output/jats_iucr_d-75-00616.json index b90cf21..2a35c75 100644 --- a/tests/stubdata/output/jats_iucr_d-75-00616.json +++ b/tests/stubdata/output/jats_iucr_d-75-00616.json @@ -34,7 +34,7 @@ } ], "openAccess": { - "license": "Prior permission is not required to reproduce short quotations, tables and figures from this article, provided\n the original authors and source are cited. For more information, see https://journals.iucr.org/services/copyrightpolicy.html." + "license": "Prior permission is not required to reproduce short quotations, tables and figures from this article, provided the original authors and source are cited. For more information, see https://journals.iucr.org/services/copyrightpolicy.html." }, "pagination": { "firstPage": "616", diff --git a/tests/stubdata/output/jats_nature_41467_2023_Article_40261_nlm.json b/tests/stubdata/output/jats_nature_41467_2023_Article_40261_nlm.json index fa41ba5..5d2257c 100644 --- a/tests/stubdata/output/jats_nature_41467_2023_Article_40261_nlm.json +++ b/tests/stubdata/output/jats_nature_41467_2023_Article_40261_nlm.json @@ -318,7 +318,13 @@ } ], "pubDate": { - "electrDate": "2023-12-00" + "electrDate": "2023-07-25", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2023-12-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_nature_article_pubdatetype_1.json b/tests/stubdata/output/jats_nature_article_pubdatetype_1.json new file mode 100644 index 0000000..6017134 --- /dev/null +++ b/tests/stubdata/output/jats_nature_article_pubdatetype_1.json @@ -0,0 +1,310 @@ +{ + "abstract": { + "textEnglish": "Developing skeletal editing tools is not a trivial task, and realizing the corresponding single-atom transmutation in a ring system without altering the ring size is even more challenging. Here, we introduce a skeletal editing strategy that enables polycyclic arenols, a highly prevalent motif in bioactive molecules, to be readily converted into N-heteroarenes through carbon\u2013nitrogen transmutation. The reaction features selective nitrogen insertion into the C\u2013C bond of the arenol frameworks by azidative dearomatization and aryl migration, followed by ring-opening, and ring-closing (ANRORC) to achieve carbon-to-nitrogen transmutation in the aromatic framework of the arenol. Using widely available arenols as N-heteroarene precursors, this alternative approach allows the streamlined assembly of complex polycyclic heteroaromatics with broad functional group tolerance. Finally, pertinent transformations of the products, including synthesis complex biheteroarene skeletons, were conducted and exhibited significant potential in materials chemistry." + }, + "authors": [ + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/00z3td547", + "affIDType": "ROR" + }, + { + "affID": "grid.412262.1", + "affIDType": "GRID" + }, + { + "affID": "0000 0004 1761 5538", + "affIDType": "ISNI" + } + ], + "affPubRaw": "Key Laboratory of Synthetic and Natural Functional Molecule of the Ministry of Education, College of Chemistry & Materials Science, Northwest University, 710069, Xi\u2019an, China" + } + ], + "attrib": { + "orcid": "0000-0003-3131-4558" + }, + "name": { + "given_name": "Hong", + "surname": "Lu" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/00z3td547", + "affIDType": "ROR" + }, + { + "affID": "grid.412262.1", + "affIDType": "GRID" + }, + { + "affID": "0000 0004 1761 5538", + "affIDType": "ISNI" + } + ], + "affPubRaw": "Key Laboratory of Synthetic and Natural Functional Molecule of the Ministry of Education, College of Chemistry & Materials Science, Northwest University, 710069, Xi\u2019an, China" + } + ], + "name": { + "given_name": "Yu", + "surname": "Zhang" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/00z3td547", + "affIDType": "ROR" + }, + { + "affID": "grid.412262.1", + "affIDType": "GRID" + }, + { + "affID": "0000 0004 1761 5538", + "affIDType": "ISNI" + } + ], + "affPubRaw": "Key Laboratory of Synthetic and Natural Functional Molecule of the Ministry of Education, College of Chemistry & Materials Science, Northwest University, 710069, Xi\u2019an, China" + } + ], + "name": { + "given_name": "Xiu-Hong", + "surname": "Wang" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/00z3td547", + "affIDType": "ROR" + }, + { + "affID": "grid.412262.1", + "affIDType": "GRID" + }, + { + "affID": "0000 0004 1761 5538", + "affIDType": "ISNI" + } + ], + "affPubRaw": "Key Laboratory of Synthetic and Natural Functional Molecule of the Ministry of Education, College of Chemistry & Materials Science, Northwest University, 710069, Xi\u2019an, China" + } + ], + "name": { + "given_name": "Ran", + "surname": "Zhang" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "grid.32566.34", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 8571 0482", + "affIDType": "ISNI" + } + ], + "affPubRaw": "State Key Laboratory of Applied Organic Chemistry, College of Chemistry and Chemical Engineering, Lanzhou University, 730000, Lanzhou, China" + } + ], + "attrib": { + "email": "xupf@lzu.edu.cn", + "orcid": "0000-0002-5746-758X" + }, + "name": { + "given_name": "Peng-Fei", + "surname": "Xu" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/00z3td547", + "affIDType": "ROR" + }, + { + "affID": "grid.412262.1", + "affIDType": "GRID" + }, + { + "affID": "0000 0004 1761 5538", + "affIDType": "ISNI" + } + ], + "affPubRaw": "Key Laboratory of Synthetic and Natural Functional Molecule of the Ministry of Education, College of Chemistry & Materials Science, Northwest University, 710069, Xi\u2019an, China" + } + ], + "attrib": { + "email": "haow@nwu.edu.cn", + "orcid": "0000-0002-7951-683X" + }, + "name": { + "given_name": "Hao", + "surname": "Wei" + } + } + ], + "copyright": { + "statement": "\u00a9 The Author(s) 2024", + "status": true + }, + "editorialHistory": { + "acceptedDate": "2024-04-25", + "receivedDates": [ + "2024-01-29" + ] + }, + "funding": [ + { + "agencyid": { + "idschema": "doi", + "idvalue": "https://doi.org/10.13039/501100001809" + }, + "agencyname": "National Natural Science Foundation of China (National Science Foundation of China)", + "awardnumber": "21971205" + }, + { + "agencyname": "Natural Science Basic Research Plan for Distinguished Young Scholars in Shaanxi Province of China (2022JC-08)" + }, + { + "agencyname": "Natural Science Basic Research Plan in Shaanxi Province of China (2023-JC-YB-126)" + } + ], + "openAccess": { + "license": "Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.", + "licenseURL": "http://creativecommons.org/licenses/by/4.0/", + "open": true + }, + "pagination": { + "electronicID": "3772" + }, + "persistentIDs": [ + { + "DOI": "10.1038/s41467-024-48265-6" + } + ], + "pubDate": { + "electrDate": "2024-05-04", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2024-12-00" + } + ] + }, + "publication": { + "ISSN": [ + { + "issnString": "2041-1723", + "pubtype": "epub" + } + ], + "issueNum": "1", + "pubName": "Nature Communications", + "pubYear": "2024", + "publisher": "Nature Publishing Group UK", + "volumeNum": "15" + }, + "publisherIDs": [ + { + "Identifier": "s41467-024-48265-6", + "attribute": "publisher-id" + }, + { + "Identifier": "48265", + "attribute": "manuscript" + } + ], + "recordData": { + "createdTime": "", + "loadFormat": "JATS", + "loadLocation": "", + "loadType": "fromFile", + "parsedTime": "", + "recordOrigin": "" + }, + "references": [ + " Engle KM Mei T-S Wasa M Yu J-Q Weak coordination as a powerful means for developing broadly useful C\u2013H functionalization reactions Acc. 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Chem. \t\t\t\t\t\t2016, 2101\u20132104 (2016). \t\t\t\t\t " + ], + "title": { + "textEnglish": "Carbon\u2013nitrogen transmutation in polycyclic arenol skeletons to access N-heteroarenes" + } +} diff --git a/tests/stubdata/output/jats_nature_natsd_12_7375.json b/tests/stubdata/output/jats_nature_natsd_12_7375.json index 08ee1a7..1244bda 100644 --- a/tests/stubdata/output/jats_nature_natsd_12_7375.json +++ b/tests/stubdata/output/jats_nature_natsd_12_7375.json @@ -2261,7 +2261,13 @@ } ], "pubDate": { - "electrDate": "2022-12-00" + "electrDate": "2022-05-05", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2022-12-00" + } + ] }, "publication": { "ISSN": [ @@ -2295,57 +2301,57 @@ "recordOrigin": "" }, "references": [ - "Standards of Medical Care in DiabetesAmerican Diabetes Association. 2. Classification and diagnosis of diabetesDiabetes Care2019421328", - "Hern\u00e1ndez-ochoaEOLlanosPLannerJTThe underlying mechanisms of diabetic myopathyJ. 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(Los Angeles) 2015 4 1 5 ", + " Krause MP Riddell MC Hawke TJ Effects of type 1 diabetes mellitus on skeletal muscle: Clinical observations and physiological mechanisms Pediatr. Diabetes 2011 12 345 364 1:CAS:528:DC%2BC3MXoslOmu78%3D 20860561 10.1111/j.1399-5448.2010.00699.x ", + " Hanson MA Gluckman PD Ma RCW Matzen P Biesma RG Early life opportunities for prevention of diabetes in low and middle income countries BMC Public Health 2012 12 1 10.1186/1471-2458-12-1025 ", + " Poon LC McIntyre HD Hyett JA da Fonseca EB Hod M The first-trimester of pregnancy\u2014A window of opportunity for prediction and prevention of pregnancy complications and future life Diabetes Res. Clin. Pract. 2018 145 20 30 29852233 10.1016/j.diabres.2018.05.002 ", + " Orleans ED Comparison betweent the effects of swimming and treadmill-based aerobic training protocols in diabetic rats Int. J. Cardiovasc. Sci. 2018 31 610 618 ", + " Soares TS Moraes-Souza RQ Carneiro TB Araujo-Silva VC Schavinski AZ Gratao TB Damasceno DC Volpato GT Maternal-fetal outcomes of exercise applied in rats with mild hyperglycemia after embryonic implantation Birth Defects Res. 2020 113 1 ", + " Harber M Trappe S Single muscle fiber contractile properties of young competitive distance runners J. Appl. Physiol. 2008 105 629 636 18535124 10.1152/japplphysiol.00995.2007 ", + " Fry CS Fibre type-specific satellite cell response to aerobic training in sedentary adults J. Physiol. 2014 592 2625 2635 1:CAS:528:DC%2BC2cXps1Ojs7o%3D 24687582 4080942 10.1113/jphysiol.2014.271288 ", + " Qaisar R Bhaskaran S Remmen HV Free radical biology and medicine muscle fiber type diversi fi cation during exercise and regeneration Free Radic. Biol. Med. 2016 98 56 67 1:CAS:528:DC%2BC28XltlOktbw%3D 27032709 10.1016/j.freeradbiomed.2016.03.025 ", + " Marini G de Rinaldi JC Damasceno DC Felisbino SL Rudge MVC Altera\u00e7\u00f5es da matriz extracelular causadas pelo diabetes: O impacto sobre a contin\u00eancia urin\u00e1ria Rev. Bras. Ginecol. Obs. 2014 36 328 333 10.1590/SO100-720320140005014 ", + " Marangon L Gobatto C de Mello MKE Utilization of an hyperbolic model for the determination of the critical load in swimming rats Med. Sci. Sport. Exerc. 2002 34 149 10.1097/00005768-200205001-00834 ", + " Manchado FDB Gobatto CA Contarteze RVL Papoti MMM M\u00e1xima fase est\u00e1vel de lactato \u00e9 erg\u00f4metro-dependente em modelo experimental utilizando ratos Rev. Bras. Med. Esporte 2006 6 259 262 10.1590/S1517-86922006000500007 ", + " Volpato GT Damasceno DC Kempinas WG Rudge MVC Calderon IMP Effect of exercise on the reproductive outcome and fetal development of diabetic rats Reprod. Biomed. Online 2009 19 852 858 1:STN:280:DC%2BD1Mfkt1Gitw%3D%3D 20031028 10.1016/j.rbmo.2009.09.027 ", + " Damasceno DC Mild diabetes models and their maternal-fetal repercussions J. Diabetes Res. 2013 2013 26 10.1155/2013/473575 ", + " Damasceno DC Streptozotocin-induced diabetes models : Pathophysiological mechanisms and fetal outcomes Biomed. Res. Int. 2014 1 2014 ", + " Sinzato YK Damasceno DC Laufer-Amorim R Rodrigues MMP Oshiiwa M Taylor KN Plasma concentrations and placental immunostaining of interleukin-10 and tumornecrosis factor-\u03b1 as predictors of alterations in the embryo-fetal organism and the placental development of diabetic rats Braz. J. Med. Biol. Res. 2011 44 206 211 1:CAS:528:DC%2BC3MXlvVSlsrg%3D 21344139 10.1590/S0100-879X2011007500015 ", + " Iessi IL Evaluation of neonatally-induced mild diabetes in rats: Maternal and fetal repercussions Diabetol. Metab. Syndr. 2010 2 1 8 10.1186/1758-5996-2-37 1:CAS:528:DC%2BC3cXnsVCjsb4%3D ", + " Damasceno, D.C., Kempinas, W.G., Volpato, G.T., Consoni, M., Rudge, M.V.C., Paumgartten, F. \t\t\t\t\t\tAnomalias Cong\u00eanitas : Estudos Experimentais. (Coopmed, 2008). \t\t\t\t\t ", + " Nascimento, L. Avalia\u00e7\u00e3o de diferentes modelos de indu\u00e7\u00e3o do diabete moderado em ratas Wistar e suas repercuss\u00f5es no organismo materno-fetal. (2014). " ], "title": { "textEnglish": "Reversal of diabetic-induced myopathy by swimming exercise in pregnant rats: a translational intervention study" diff --git a/tests/stubdata/output/jats_no_issue_pagecount.json b/tests/stubdata/output/jats_no_issue_pagecount.json index db88d6d..9eb2985 100644 --- a/tests/stubdata/output/jats_no_issue_pagecount.json +++ b/tests/stubdata/output/jats_no_issue_pagecount.json @@ -172,7 +172,13 @@ } ], "pubDate": { - "electrDate": "2024-00-00" + "electrDate": "2024-07-17", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2024-00-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_springer_Article_collab_nlm.json b/tests/stubdata/output/jats_springer_Article_collab_nlm.json index bd6662d..a9d1cc8 100644 --- a/tests/stubdata/output/jats_springer_Article_collab_nlm.json +++ b/tests/stubdata/output/jats_springer_Article_collab_nlm.json @@ -1409,7 +1409,7 @@ } ], "openAccess": { - "license": "\nOpen Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit\n\t\t\t\t\t\thttp://creativecommons.org/licenses/by/4.0/.\n\t\t\t\t\t", + "license": "Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, @@ -1422,7 +1422,13 @@ } ], "pubDate": { - "electrDate": "2024-12-00" + "electrDate": "2024-05-30", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2024-12-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_springer_EPJC_s10052-023-11699-1.json b/tests/stubdata/output/jats_springer_EPJC_s10052-023-11699-1.json index c7c1125..ae4600b 100644 --- a/tests/stubdata/output/jats_springer_EPJC_s10052-023-11699-1.json +++ b/tests/stubdata/output/jats_springer_EPJC_s10052-023-11699-1.json @@ -73029,7 +73029,7 @@ ] }, "openAccess": { - "license": "\nOpen Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit\n\t\t\t\t\t\thttp://creativecommons.org/licenses/by/4.0/.\n\t\t\t\t\t", + "license": "Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, @@ -73042,7 +73042,13 @@ } ], "pubDate": { - "electrDate": "2023-07-00" + "electrDate": "2023-07-31", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2023-07-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_springer_EPJC_s10052-023-11733-2.json b/tests/stubdata/output/jats_springer_EPJC_s10052-023-11733-2.json index 69501e8..7101c30 100644 --- a/tests/stubdata/output/jats_springer_EPJC_s10052-023-11733-2.json +++ b/tests/stubdata/output/jats_springer_EPJC_s10052-023-11733-2.json @@ -26758,7 +26758,7 @@ ] }, "openAccess": { - "license": "\nOpen Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit\n\t\t\t\t\t\thttp://creativecommons.org/licenses/by/4.0/.\n\t\t\t\t\t", + "license": "Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, @@ -26771,7 +26771,13 @@ } ], "pubDate": { - "electrDate": "2023-07-00" + "electrDate": "2023-07-14", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2023-07-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_springer_JHEP_JHEP07_2023_200.json b/tests/stubdata/output/jats_springer_JHEP_JHEP07_2023_200.json index d7e0489..0d7494a 100644 --- a/tests/stubdata/output/jats_springer_JHEP_JHEP07_2023_200.json +++ b/tests/stubdata/output/jats_springer_JHEP_JHEP07_2023_200.json @@ -20860,7 +20860,7 @@ } ], "openAccess": { - "license": "\nOpen Access. This article is distributed under the terms of the Creative Commons Attribution License (\n\t\t\t\t\t\tCC-BY 4.0), which permits any use, distribution and reproduction in any medium, provided the original author(s) and source are credited.\n\t\t\t\t\t", + "license": "Open Access. This article is distributed under the terms of the Creative Commons Attribution License ( CC-BY 4.0), which permits any use, distribution and reproduction in any medium, provided the original author(s) and source are credited.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, @@ -20873,7 +20873,13 @@ } ], "pubDate": { - "electrDate": "2023-07-00" + "electrDate": "2023-07-26", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2023-07-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_springer_NatCo_s41467-023-40272-3.json b/tests/stubdata/output/jats_springer_NatCo_s41467-023-40272-3.json index bc58de6..9794f2c 100644 --- a/tests/stubdata/output/jats_springer_NatCo_s41467-023-40272-3.json +++ b/tests/stubdata/output/jats_springer_NatCo_s41467-023-40272-3.json @@ -826,7 +826,7 @@ } ], "openAccess": { - "license": "\nOpen Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit\n\t\t\t\t\t\thttp://creativecommons.org/licenses/by/4.0/.\n\t\t\t\t\t", + "license": "Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, @@ -839,7 +839,13 @@ } ], "pubDate": { - "electrDate": "2023-12-00" + "electrDate": "2023-07-28", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2023-12-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_springer_Natur_s41598-023-38673-x.json b/tests/stubdata/output/jats_springer_Natur_s41598-023-38673-x.json index 5cb47df..121b9c4 100644 --- a/tests/stubdata/output/jats_springer_Natur_s41598-023-38673-x.json +++ b/tests/stubdata/output/jats_springer_Natur_s41598-023-38673-x.json @@ -1313,7 +1313,7 @@ } ], "openAccess": { - "license": "\nOpen Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit\n\t\t\t\t\t\thttp://creativecommons.org/licenses/by/4.0/.\n\t\t\t\t\t", + "license": "Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, @@ -1326,7 +1326,13 @@ } ], "pubDate": { - "electrDate": "2023-12-00" + "electrDate": "2023-07-20", + "otherDate": [ + { + "otherDateType": "collection", + "otherDateValue": "2023-12-00" + } + ] }, "publication": { "ISSN": [ diff --git a/tests/stubdata/output/jats_springer_SoPh_s11207-023-02231-5_mathtex.json b/tests/stubdata/output/jats_springer_SoPh_s11207-023-02231-5_mathtex.json index ac45230..f649bdd 100644 --- a/tests/stubdata/output/jats_springer_SoPh_s11207-023-02231-5_mathtex.json +++ b/tests/stubdata/output/jats_springer_SoPh_s11207-023-02231-5_mathtex.json @@ -294,7 +294,7 @@ } ], "openAccess": { - "license": "\nOpen Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit\n\t\t\t\t\t\thttp://creativecommons.org/licenses/by/4.0/.\n\t\t\t\t\t", + "license": "Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article\u2019s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article\u2019s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.", "licenseURL": "http://creativecommons.org/licenses/by/4.0/", "open": true }, diff --git a/tests/stubdata/output/jats_springer_article_pubdatetype_2.json b/tests/stubdata/output/jats_springer_article_pubdatetype_2.json new file mode 100644 index 0000000..73fe40c --- /dev/null +++ b/tests/stubdata/output/jats_springer_article_pubdatetype_2.json @@ -0,0 +1,313 @@ +{ + "abstract": { + "textEnglish": "Ecosystem services value (ESV) can assess the level of basin ecological restoration and provide a basis for ecological management decision-making. This study object selects Liaohe River Basin (LHB), a typical basin in Northeast China. The ecosystem service value variation caused by changes in land use cover and the spatial distribution characteristics was evaluated by employing the benefit transfer method, which is based on data sets for land use over 2000\u20132020. Meanwhile, geographical detector was employed to investigate the impacts and interactions of various factors driving the ESV, and predicted future changes in land and ESV by PLUS model. The results showed the following: (1) LHB land transformations mainly concentrated in the transformation between grassland, farmland and forestland. ESV in LHB decreased and then increased between 2000 and 2020 (1224 billion-928 billion-1238 billion), (2) Ecosystem service value exhibited a strong positive spatial autocorrelation, high ESV was mainly distributed in the eastern and western regions of LHB, and low ESV in the central region. (3) The variation in ecosystem service value mainly arose from the human activity intensity index of human factors. (4) In the future, the ecological protection priority scenario could improve the ESV in LHB, and the natural development priority and economic development priority scenario was not conducive to the improvement of ESV. The results showed that the ecological restoration effect of the LHB was obvious with the ecosystem service value is significantly improved. In the future, attention should be paid to control human activities and strengthen ecological protection in ESV hotspots." + }, + "authors": [ + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/03xpwj629", + "affIDType": "ROR" + }, + { + "affID": "grid.411356.4", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 9339 3042", + "affIDType": "ISNI" + } + ], + "affPubRaw": "College of Environmental Sciences, Liaoning University, 110036, Shenyang, People\u2019s Republic of China" + } + ], + "name": { + "given_name": "Changgeng", + "surname": "Jia" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/03xpwj629", + "affIDType": "ROR" + }, + { + "affID": "grid.411356.4", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 9339 3042", + "affIDType": "ISNI" + } + ], + "affPubRaw": "College of Environmental Sciences, Liaoning University, 110036, Shenyang, People\u2019s Republic of China" + } + ], + "name": { + "given_name": "Yu", + "surname": "Fan" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/03xpwj629", + "affIDType": "ROR" + }, + { + "affID": "grid.411356.4", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 9339 3042", + "affIDType": "ISNI" + } + ], + "affPubRaw": "College of Environmental Sciences, Liaoning University, 110036, Shenyang, People\u2019s Republic of China" + } + ], + "name": { + "given_name": "Chaoxiang", + "surname": "Wei" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/03xpwj629", + "affIDType": "ROR" + }, + { + "affID": "grid.411356.4", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 9339 3042", + "affIDType": "ISNI" + } + ], + "affPubRaw": "College of Environmental Sciences, Liaoning University, 110036, Shenyang, People\u2019s Republic of China" + } + ], + "name": { + "given_name": "Kunyu", + "surname": "Luo" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/03xpwj629", + "affIDType": "ROR" + }, + { + "affID": "grid.411356.4", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 9339 3042", + "affIDType": "ISNI" + } + ], + "affPubRaw": "College of Environmental Sciences, Liaoning University, 110036, Shenyang, People\u2019s Republic of China" + } + ], + "name": { + "given_name": "Sihui", + "surname": "Li" + } + }, + { + "affiliation": [ + { + "affPubID": [ + { + "affID": "https://ror.org/03xpwj629", + "affIDType": "ROR" + }, + { + "affID": "grid.411356.4", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 9339 3042", + "affIDType": "ISNI" + } + ], + "affPubRaw": "College of Environmental Sciences, Liaoning University, 110036, Shenyang, People\u2019s Republic of China" + }, + { + "affPubID": [ + { + "affID": "https://ror.org/018rbtf37", + "affIDType": "ROR" + }, + { + "affID": "grid.413109.e", + "affIDType": "GRID" + }, + { + "affID": "0000 0000 9735 6249", + "affIDType": "ISNI" + } + ], + "affPubRaw": "College of Marine and Environmental Sciences, Tianjin University of Science & Technology, 300457, Tianjin, China" + } + ], + "attrib": { + "email": "youtaosong@sina.com" + }, + "name": { + "given_name": "Youtao", + "surname": "Song" + } + } + ], + "copyright": { + "statement": "\u00a9 The Author(s), under exclusive licence to Society of Wetland Scientists 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.", + "status": true + }, + "editorialHistory": { + "acceptedDate": "2023-12-05", + "receivedDates": [ + "2023-08-17" + ] + }, + "keywords": [ + { + "keyString": "Basin ecosystem service value", + "keySystem": "misc" + }, + { + "keyString": "Land use change transition", + "keySystem": "misc" + }, + { + "keyString": "Spatiotemporal pattern", + "keySystem": "misc" + }, + { + "keyString": "Drive analysis", + "keySystem": "misc" + }, + { + "keyString": "Multi-scenario simulation", + "keySystem": "misc" + } + ], + "pagination": { + "electronicID": "7" + }, + "persistentIDs": [ + { + "DOI": "10.1007/s13157-023-01762-8" + } + ], + "pubDate": { + "electrDate": "2023-12-18", + "printDate": "2024-01-00" + }, + "publication": { + "ISSN": [ + { + "issnString": "0277-5212", + "pubtype": "ppub" + }, + { + "issnString": "1943-6246", + "pubtype": "epub" + } + ], + "issueNum": "1", + "pubName": "Wetlands", + "pubYear": "2024", + "publisher": "Springer Netherlands", + "volumeNum": "44" + }, + "publisherIDs": [ + { + "Identifier": "s13157-023-01762-8", + "attribute": "publisher-id" + }, + { + "Identifier": "1762", + "attribute": "manuscript" + } + ], + "recordData": { + "createdTime": "", + "loadFormat": "JATS", + "loadLocation": "", + "loadType": "fromFile", + "parsedTime": "", + "recordOrigin": "" + }, + "references": [ + " Bai Y Ochuodho TO Yang J Impact of land use and climate change on water related ecosystem services in Kentucky, USA Ecological Indicators 2019 102 51 64 10.1016/j.ecolind.2019.01.079 ", + " Bennett MT China\u2019s sloping land conversion program: institutional innovation or business as usual? 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This article is distributed under the terms of the Creative Commons Attribution License (\n\t\t\t\t\t\tCC-BY 4.0), which permits any use, distribution and reproduction in any medium, provided the original author(s) and source are credited.\n\t\t\t\t\t", + "license": "Open Access. 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