{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,13]],"date-time":"2026-01-13T00:02:19Z","timestamp":1768262539900,"version":"3.49.0"},"reference-count":50,"publisher":"Wiley","issue":"4","license":[{"start":{"date-parts":[[2022,9,25]],"date-time":"2022-09-25T00:00:00Z","timestamp":1664064000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/501100001807","name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de S\u00e3o Paulo","doi-asserted-by":"publisher","award":["#2019\/27662\u20100"],"award-info":[{"award-number":["#2019\/27662\u20100"]}],"id":[{"id":"10.13039\/501100001807","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["aap.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Journal of Periodontology"],"published-print":{"date-parts":[[2023,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background<\/jats:title><jats:p>Maternal periodontal disease (PED) and apical periodontitis (AP) are associated insulin resistance (IR), increased tumor necrosis factor\u2010\u03b1 (TNF\u2010\u03b1) levels, and alterations in insulin signaling (IS) in the gastrocnemius muscle (GM) of adult offspring. TNF\u2010\u03b1 stimulates I kappa B kinase (IKK) and c\u2010Jun N\u2010terminal protein kinase (JNK), resulting in IS attenuation. However, studies that investigated the maternal true endodontic\u2010periodontal lesion (EPL) in offspring are scarce, and in this case, the impact could be even higher. This study aimed to evaluate the effects of EPL on the IR, IS, and inflammatory pathways on the offspring GM.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Female Wistar rats were distributed into control, AP, PED, and EPL groups. After 30 days of oral inflammation induction, rats from all groups were allowed to mate with healthy rats. The body weight of the offspring was assessed from birth to 75\u00a0days of age. After 75\u00a0days, the following measurements were performed: glycemia, insulinemia, IR, TNF\u2010\u03b1 content, and IKK\u03b1\/\u03b2, JNK, pp185 (Tyr), and IRS\u20101 (Ser) phosphorylation status in the GM.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Maternal PED and EPL were associated with low birth weights. All maternal oral inflammations promoted IR and IS impairment in the GM and only maternal PED and EPL caused an increase in TNF\u2010\u03b1 content and IKK\u03b1\/\u03b2 phosphorylation status in the GM of offspring. The offspring of the rats with EPL group showed worsening of metabolic changes when compared with offspring of rats with AP or PED.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Association of maternal AP and PED promoted a more pronounced worsening in the health of the adult offspring.<\/jats:p><\/jats:sec>","DOI":"10.1002\/jper.22-0139","type":"journal-article","created":{"date-parts":[[2022,8,22]],"date-time":"2022-08-22T12:23:55Z","timestamp":1661171035000},"page":"487-497","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Effect of maternal true combined endodontic\u2010periodontal lesion on insulin and inflammatory pathway in adult offspring"],"prefix":"10.1002","volume":"94","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5564-8256","authenticated-orcid":false,"given":"Bianca Elvira","family":"Belardi","sequence":"first","affiliation":[{"name":"Programa de P\u00f3s\u2010Gradua\u00e7\u00e3o Multic\u00eantrico em Ci\u00eancias Fisiol\u00f3gicas\u2010SBFis, Department of Basic Sciences School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2288-708X","authenticated-orcid":false,"given":"Maria Sara de Lima Coutinho","family":"Mattera","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s\u2010Gradua\u00e7\u00e3o Multic\u00eantrico em Ci\u00eancias Fisiol\u00f3gicas\u2010SBFis, Department of Basic Sciences School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1708-4071","authenticated-orcid":false,"given":"Tha\u00eds Ver\u00f4nica Saori","family":"Tsosura","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s\u2010Gradua\u00e7\u00e3o Multic\u00eantrico em Ci\u00eancias Fisiol\u00f3gicas\u2010SBFis, Department of Basic Sciences School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5122-275X","authenticated-orcid":false,"given":"Rodrigo Martins","family":"dos Santos","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s\u2010Gradua\u00e7\u00e3o Multic\u00eantrico em Ci\u00eancias Fisiol\u00f3gicas\u2010SBFis, Department of Basic Sciences School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4313-7149","authenticated-orcid":false,"given":"Cristiane","family":"Cantiga\u2010Silva","sequence":"additional","affiliation":[{"name":"Department of Preventive and Restorative Dentistry School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2348-7846","authenticated-orcid":false,"given":"Luciano","family":"Tavares \u00c2ngelo Cintra","sequence":"additional","affiliation":[{"name":"Department of Preventive and Restorative Dentistry School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4406-405X","authenticated-orcid":false,"given":"Fernando Yamamoto","family":"Chiba","sequence":"additional","affiliation":[{"name":"Department of Preventive and Restorative Dentistry School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9985-6164","authenticated-orcid":false,"given":"Lara Teschi","family":"Bravo","sequence":"additional","affiliation":[{"name":"Department of Preventive and Restorative Dentistry School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nubia Ramos","family":"Carvalho","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s\u2010Gradua\u00e7\u00e3o Multic\u00eantrico em Ci\u00eancias Fisiol\u00f3gicas\u2010SBFis, Department of Basic Sciences School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0874-2714","authenticated-orcid":false,"given":"Ana Carolina Nascimento","family":"Carnevali","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s\u2010Gradua\u00e7\u00e3o Multic\u00eantrico em Ci\u00eancias Fisiol\u00f3gicas\u2010SBFis, Department of Basic Sciences School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1479-0413","authenticated-orcid":false,"given":"Renan Akira Fujii","family":"de Oliveira","sequence":"additional","affiliation":[{"name":"Department of Preventive and Restorative Dentistry School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4859-0583","authenticated-orcid":false,"given":"Edilson","family":"Ervolino","sequence":"additional","affiliation":[{"name":"Institute of Biosciences, Botucatu, Brazil and Department of Basic Sciences, Division of Histology, School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3753-229X","authenticated-orcid":false,"given":"Doris Hissako","family":"Matsushita","sequence":"additional","affiliation":[{"name":"Programa de P\u00f3s\u2010Gradua\u00e7\u00e3o Multic\u00eantrico em Ci\u00eancias Fisiol\u00f3gicas\u2010SBFis, Department of Basic Sciences School of Dentistry S\u00e3o Paulo State University (UNESP)  Ara\u00e7atuba Brazil"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2022,9,25]]},"reference":[{"key":"e_1_2_9_2_1","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.311.6998.171"},{"key":"e_1_2_9_3_1","doi-asserted-by":"publisher","DOI":"10.1079\/PHN2001145"},{"key":"e_1_2_9_4_1","doi-asserted-by":"publisher","DOI":"10.3390\/nu12123900"},{"key":"e_1_2_9_5_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.2007.070196"},{"key":"e_1_2_9_6_1","doi-asserted-by":"publisher","DOI":"10.1111\/jcpe.12063"},{"key":"e_1_2_9_7_1","doi-asserted-by":"publisher","DOI":"10.1111\/jcpe.12082"},{"key":"e_1_2_9_8_1","doi-asserted-by":"publisher","DOI":"10.1007\/s40496-020-00255-5"},{"key":"e_1_2_9_9_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.2012.110372"},{"key":"e_1_2_9_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.lfs.2016.02.010"},{"key":"e_1_2_9_11_1","doi-asserted-by":"publisher","DOI":"10.1111\/iej.13096"},{"key":"e_1_2_9_12_1","first-page":"1864","article-title":"Serine phosphorylation of insulin receptor substrate\u20101: a novel target for the reversal of insulin resistance","volume":"11","author":"Sykiotis GP","year":"2001","journal-title":"Mol Endocrinol"},{"key":"e_1_2_9_13_1","doi-asserted-by":"publisher","DOI":"10.1038\/nm.2627"},{"key":"e_1_2_9_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.lfs.2020.117304"},{"key":"e_1_2_9_15_1","doi-asserted-by":"publisher","DOI":"10.1002\/JPER.18-0568"},{"key":"e_1_2_9_16_1","doi-asserted-by":"publisher","DOI":"10.1902\/jop.1964.35.1.22"},{"key":"e_1_2_9_17_1","first-page":"154","article-title":"The periodontal\u2010endodontic continuum: a review","volume":"11","author":"Sunitha R","year":"2008","journal-title":"J\u00a0Conserv Dent"},{"key":"e_1_2_9_18_1","first-page":"39","article-title":"Endo\u2010perio dilemma: a brief review","volume":"8","author":"Singh P","year":"2011","journal-title":"Dent Res J"},{"key":"e_1_2_9_19_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10735-008-9163-4"},{"key":"e_1_2_9_20_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00784-012-0853-7"},{"key":"e_1_2_9_21_1","doi-asserted-by":"publisher","DOI":"10.1210\/endo.137.1.8536607"},{"key":"e_1_2_9_22_1","doi-asserted-by":"publisher","DOI":"10.4103\/0976-237X.83067"},{"key":"e_1_2_9_23_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.coemr.2020.07.005"},{"key":"e_1_2_9_24_1","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.3008599"},{"key":"e_1_2_9_25_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jri.2014.03.006"},{"key":"e_1_2_9_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/jog.13782"},{"key":"e_1_2_9_27_1","doi-asserted-by":"publisher","DOI":"10.1210\/edrv.18.5.0313"},{"key":"e_1_2_9_28_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-2591.2011.01974.x"},{"key":"e_1_2_9_29_1","first-page":"268","article-title":"Endo\u2010perio lesions","volume":"2","author":"Peeran SW","year":"2013","journal-title":"Int J Sci"},{"key":"e_1_2_9_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.joen.2017.05.021"},{"key":"e_1_2_9_31_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.joen.2014.11.018"},{"key":"e_1_2_9_32_1","doi-asserted-by":"publisher","DOI":"10.1111\/tmi.12579"},{"key":"e_1_2_9_33_1","doi-asserted-by":"publisher","DOI":"10.1590\/2359-3997000000169"},{"key":"e_1_2_9_34_1","doi-asserted-by":"publisher","DOI":"10.1210\/jc.82.2.402"},{"key":"e_1_2_9_35_1","doi-asserted-by":"publisher","DOI":"10.1136\/fn.81.1.F71"},{"key":"e_1_2_9_36_1","doi-asserted-by":"publisher","DOI":"10.1155\/2015\/532984"},{"key":"e_1_2_9_37_1","doi-asserted-by":"publisher","DOI":"10.3810\/pgm.2012.11.2615"},{"key":"e_1_2_9_38_1","doi-asserted-by":"publisher","DOI":"10.1038\/nm1185"},{"key":"e_1_2_9_39_1","volume-title":"2019 IKK\/NF\u2010\u03baB\u2010regulated Inflammatory Pathway in Human Adipocytes: Implication in Subsequent Contribution to Insulin Resistance and Atherosclerosis. Master's Thesis","author":"Bishwokarma B"},{"key":"e_1_2_9_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tcb.2020.12.003"},{"key":"e_1_2_9_41_1","doi-asserted-by":"publisher","DOI":"10.1038\/35104568"},{"key":"e_1_2_9_42_1","doi-asserted-by":"publisher","DOI":"10.1152\/ajpgi.00422.2005"},{"key":"e_1_2_9_43_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.271.5249.665"},{"key":"e_1_2_9_44_1","first-page":"183","article-title":"Insulin resistance associated to obesity: the link TNF\u2010alpha","volume":"3","author":"Nieto\u2010vazquez I","year":"2007","journal-title":"Arch Physiol Biochem"},{"key":"e_1_2_9_45_1","doi-asserted-by":"publisher","DOI":"10.2337\/diabetes.54.10.2939"},{"key":"e_1_2_9_46_1","doi-asserted-by":"publisher","DOI":"10.1172\/JCI29069"},{"key":"e_1_2_9_47_1","doi-asserted-by":"publisher","DOI":"10.1172\/JCI34260"},{"key":"e_1_2_9_48_1","first-page":"12","article-title":"Suppressor of Cytokine Signaling 1 (SOCS\u20101) and SOCS\u20103 cause insulin resistance through inhibition of tyrosine phosphorylation of insulin receptor substrate proteins by discrete mechanisms","volume":"24","author":"Ueki K","year":"2008","journal-title":"Mol Cell Biol"},{"key":"e_1_2_9_49_1","doi-asserted-by":"publisher","DOI":"10.2337\/diabetes.49.1.13"},{"key":"e_1_2_9_50_1","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a009191"},{"key":"e_1_2_9_51_1","doi-asserted-by":"publisher","DOI":"10.1016\/S1074-7613(01)00185-6"}],"container-title":["Journal of Periodontology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/JPER.22-0139","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/JPER.22-0139","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/aap.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/JPER.22-0139","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,19]],"date-time":"2025-10-19T13:41:45Z","timestamp":1760881305000},"score":1,"resource":{"primary":{"URL":"https:\/\/aap.onlinelibrary.wiley.com\/doi\/10.1002\/JPER.22-0139"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,25]]},"references-count":50,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2023,4]]}},"alternative-id":["10.1002\/JPER.22-0139"],"URL":"https:\/\/doi.org\/10.1002\/jper.22-0139","archive":["Portico"],"relation":{},"ISSN":["0022-3492","1943-3670"],"issn-type":[{"value":"0022-3492","type":"print"},{"value":"1943-3670","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,25]]},"assertion":[{"value":"2022-03-01","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-08-11","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-09-25","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}