{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T13:03:00Z","timestamp":1760101380252,"version":"3.40.5"},"reference-count":49,"publisher":"Public Library of Science (PLoS)","issue":"8","license":[{"start":{"date-parts":[[2022,8,5]],"date-time":"2022-08-05T00:00:00Z","timestamp":1659657600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"This work was supported by a gift received by RSH from Ms. Catherine Adler. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript."}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>The diagnosis of type 1 diabetes mellitus (DM) in humans is associated with high altitude, few sunshine hours, cold climate, and winter. The goals of this study were to investigate seasonal and geographic patterns of DM diagnosis in United States of America (USA) dogs with juvenile and mature onset DM. Data were collected by means of an online survey widely distributed in the USA through breed clubs, academic veterinary institutions, private veterinary referral practices, social media outlets, and the American Kennel Club. Juvenile DM (JDM) and mature onset DM were defined as DM with an age of onset &lt;365 days and DM with an age of onset \u2265365 days, respectively. Meteorological seasons were defined as: winter from December through February, spring from March through May, summer from June through August, and fall from September through November. Four geographic regions were also defined as the West, North, South, and Central regions of the USA. Nonoverlapping 95% confidence intervals (CI) for season, geographic region, and breed specific proportions of dogs with JDM were considered statistically significantly different. The study included 933 dogs with mature onset DM and 27 dogs with JDM. Dogs were diagnosed with DM significantly more in the winter and northern USA compared to all other seasons and all other geographic regions, respectively. The prevalence of JDM among dogs with DM was 2.8%. The proportion of dogs with JDM among pure breeds was not significantly different than the proportion of JDM in mixed breed dogs. It is concluded that winter and cold climate could be shared environmental factors influencing DM expression in dogs and humans. Additionally, pure breed dogs do not appear to be at increased risk for JDM compared to mixed breed dogs, indicating that factors other than genetics could influence spontaneous JDM development in dogs.<\/jats:p>","DOI":"10.1371\/journal.pone.0272297","type":"journal-article","created":{"date-parts":[[2022,8,5]],"date-time":"2022-08-05T17:42:33Z","timestamp":1659721353000},"page":"e0272297","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["Seasonality and geography of diabetes mellitus in United States of America dogs"],"prefix":"10.1371","volume":"17","author":[{"given":"Liang N. 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dogs in the United Kingdom with diabetes mellitus","volume":"156","author":"LJ Davidson","year":"2005","journal-title":"Veterinary Record"},{"issue":"6","key":"pone.0272297.ref014","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.1111\/j.1939-1676.2007.tb01940.x","article-title":"Diabetes mellitus in a population of 180,000 insured dogs: Incidence, survival, and breed distribution","volume":"21","author":"T Fall","year":"2007","journal-title":"Journal of Veterinary Internal Medicine"},{"issue":"5","key":"pone.0272297.ref015","doi-asserted-by":"crossref","first-page":"1926","DOI":"10.1111\/jvim.15570","article-title":"Heritability and complex segregation analysis of diabetes mellitus in American Eskimo Dogs","volume":"33","author":"SV Cai","year":"2019","journal-title":"Journal of Veterinary Internal Medicine"},{"issue":"September 2020","key":"pone.0272297.ref016","first-page":"1","article-title":"Heritability and complex segregation analysis of naturally-occurring diabetes in Australian Terrier Dogs","volume":"15","author":"ML Mui","year":"2020","journal-title":"PLoS ONE"},{"issue":"11","key":"pone.0272297.ref017","first-page":"1243","article-title":"Pet population still on the rise, with fewer pets per household","volume":"259","author":"M. Larkin","year":"2021","journal-title":"J Am Vet Med Assoc"},{"issue":"2","key":"pone.0272297.ref018","first-page":"342","article-title":"Calorigenic effect of insulin in hypothermic dogs","volume":"47","author":"A Therminarias","year":"1979","journal-title":"J Appl Physiol Respir Environ Exerc Physiol"},{"issue":"7","key":"pone.0272297.ref019","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1007\/BF01967958","article-title":"Independence of circulating insulin levels of the increased glucose turnover in shivering dogs","volume":"37","author":"Y Minaire","year":"1981","journal-title":"Experientia"},{"issue":"8","key":"pone.0272297.ref020","doi-asserted-by":"crossref","first-page":"1166","DOI":"10.2460\/javma.2000.217.1166","article-title":"Concurrent disorders in dogs with diabetes mellitus: 221 cases (1993\u20131998)","volume":"217","author":"RS Hess","year":"2000","journal-title":"J Am Vet Med Assoc"},{"issue":"1","key":"pone.0272297.ref021","doi-asserted-by":"crossref","first-page":"12","DOI":"10.1006\/gcen.1994.1154","article-title":"Dietary vitamin D dependence of cat and dog due to inadequate cutaneous synthesis of vitamin D","volume":"96","author":"KL How","year":"1994","journal-title":"Gen Comp Endocrinol"},{"issue":"September","key":"pone.0272297.ref022","first-page":"1","article-title":"Association Between Enterovirus Infection and Type 1 Diabetes Risk: A Meta-Analysis of 38 Case-Control Studies","volume":"12","author":"K Wang","year":"2021","journal-title":"Frontiers in Endocrinology"},{"issue":"11","key":"pone.0272297.ref023","doi-asserted-by":"crossref","first-page":"2344","DOI":"10.1007\/s00125-018-4704-1","article-title":"Unexpected subcellular distribution of a specific isoform of the Coxsackie and adenovirus receptor, CAR-SIV, in human pancreatic beta cells","volume":"61","author":"E Ifie","year":"2018","journal-title":"Diabetologia"},{"issue":"9","key":"pone.0272297.ref024","doi-asserted-by":"crossref","first-page":"e1002267","DOI":"10.1371\/journal.ppat.1002267","article-title":"Exposure to the viral by-product dsRNA or Coxsackievirus B5 triggers pancreatic beta cell apoptosis via a Bim \/ Mcl-1 imbalance","volume":"7","author":"ML Colli","year":"2011","journal-title":"PLoS pathogens"},{"key":"pone.0272297.ref025","doi-asserted-by":"crossref","DOI":"10.1155\/2018\/8475341","article-title":"The Coincidence of Newly Diagnosed Type 1 Diabetes Mellitus with IgM Antibody Positivity to Enteroviruses and Respiratory Tract Viruses","volume":"2018","author":"M Karaoglan","year":"2018","journal-title":"Journal of Diabetes Research"},{"issue":"6","key":"pone.0272297.ref026","doi-asserted-by":"crossref","DOI":"10.3390\/v13061149","article-title":"Current state of knowledge about role of pets in zoonotic transmission of SARS-CoV-2","volume":"13","author":"M Dr\u00f3\u017cd\u017c","year":"2021","journal-title":"Viruses"},{"issue":"6","key":"pone.0272297.ref027","doi-asserted-by":"crossref","first-page":"1322","DOI":"10.1111\/j.1939-1676.2010.0630.x","article-title":"Diabetes mellitus in elkhounds is associated with diestrus and pregnancy","volume":"24","author":"T Fall","year":"2010","journal-title":"J Vet Intern Med"},{"issue":"4","key":"pone.0272297.ref028","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1177\/030098588602300429","article-title":"Polyneuropathy and Hormone Profiles in a Chow Puppy with Hypoplasia of the Islets of Langerhans","volume":"23","author":"PG Anderson","year":"1986","journal-title":"Veterinary Pathology"},{"issue":"6","key":"pone.0272297.ref029","doi-asserted-by":"crossref","first-page":"419","DOI":"10.5326\/JAAHA-MS-6283","article-title":"Juvenile diabetes mellitus and concurrent exocrine pancreatic insufficiency in a labrador retriever: Long-term management","volume":"51","author":"MS Alvarez","year":"2015","journal-title":"J Am Anim Hosp Assoc"},{"issue":"1","key":"pone.0272297.ref030","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1111\/j.1939-1676.2008.0214.x","article-title":"Juvenile pancreatic atrophy in greyhounds: 12 cases (1995\u20132000)","volume":"23","author":"K Brenner","year":"2009","journal-title":"Journal of Veterinary Internal Medicine"},{"issue":"18","key":"pone.0272297.ref031","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1136\/vr.159.18.608-a","article-title":"Canine juvenile diabetes","volume":"159","author":"MV Dale","year":"2006","journal-title":"Veterinary Record"},{"issue":"10","key":"pone.0272297.ref032","doi-asserted-by":"crossref","first-page":"619","DOI":"10.2337\/diab.14.10.619","article-title":"Pathologic anatomy of the pancreas in juvenile diabetes mellitus","volume":"14","author":"W. Gepts","year":"1965","journal-title":"Diabetes"},{"issue":"3","key":"pone.0272297.ref033","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1385\/EP:17:3:283","article-title":"Lymphocytic insulitis in a juvenile dog with diabetes mellitus","volume":"17","author":"G Jouvion","year":"2006","journal-title":"Endocr Pathol"},{"issue":"12","key":"pone.0272297.ref034","doi-asserted-by":"crossref","first-page":"1337","DOI":"10.1292\/jvms.70.1337","article-title":"Juvenile diabetes mellitus accompanied by exocrine pancreatic insufficiency in a dog","volume":"70","author":"JH Kang","year":"2008","journal-title":"Journal of Veterinary Medical Science"},{"issue":"7","key":"pone.0272297.ref035","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1111\/j.1748-5827.1996.tb02406.x","article-title":"Exocrine pancreatic insufficiency combined with insulin-dependent diabetes mellitus in a juvenile German shepherd dog","volume":"37","author":"R Neiger","year":"1996","journal-title":"Journal of Small Animal Practice"},{"issue":"2","key":"pone.0272297.ref036","first-page":"194","article-title":"Inherited early-onset, insulin-requiring diabetes mellitus in keeshond dogs","volume":"105","author":"JW Kramer","year":"1981","journal-title":"American Journal of Pathology"},{"issue":"3","key":"pone.0272297.ref037","first-page":"428","article-title":"Inheritance of diabetes mellitus in Keeshond dogs","volume":"49","author":"JW Kramer","year":"1988","journal-title":"Am J Vet Res"},{"issue":"4","key":"pone.0272297.ref038","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1177\/019262339602400413","article-title":"A Case Report of Superficial Necrolytic Dermatitis in a Beagle Dog with Diabetes Mellitus","volume":"24","author":"M Yoshida","year":"1996","journal-title":"Toxicologic Pathology"},{"issue":"2","key":"pone.0272297.ref039","doi-asserted-by":"crossref","first-page":"164","DOI":"10.1177\/030098589703400212","article-title":"Ductuloendocrine cell proliferation in the pancreas of two young dogs with diabetes mellitus","volume":"34","author":"G Minkus","year":"1997","journal-title":"Vet Pathol"},{"issue":"1","key":"pone.0272297.ref040","first-page":"51","article-title":"Diabetes mellitus concurrent with exocrine pancreatic insufficiency in a young golden retreiever dog: A clinico-pathologic report","volume":"5","author":"T Mamom","year":"2010","journal-title":"J Mahanakorn Vet Med"},{"issue":"9","key":"pone.0272297.ref041","first-page":"1577","article-title":"Morphologic and immunocytochemical study of young dogs with diabetes mellitus associated with pancreatic islet hypoplasia","volume":"49","author":"CE Atkins","year":"1988","journal-title":"Am J Vet Res"},{"issue":"4","key":"pone.0272297.ref042","first-page":"596","article-title":"Insulin kinetics in juvenile canine diabetics after glucose loading","volume":"44","author":"CE Atkins","year":"1983","journal-title":"American Journal of Veterinary Research"},{"issue":"3","key":"pone.0272297.ref043","doi-asserted-by":"crossref","first-page":"E22","DOI":"10.1136\/vr.105467","article-title":"Epidemiological study of dogs with diabetes mellitus attending primary care veterinary clinics in Australia","volume":"187","author":"S Yoon","year":"2020","journal-title":"Veterinary Record"},{"issue":"1","key":"pone.0272297.ref044","first-page":"1","article-title":"Diabetes mellitus in dogs attending UK primary-care practices: frequency, risk factors and survival","volume":"7","author":"O Heeley AM","year":"2020","journal-title":"Canine Medicine and Genetics"},{"issue":"3","key":"pone.0272297.ref045","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1016\/S1090-0233(02)00242-3","article-title":"Time trends and risk factors for diabetes mellitus in dogs: Analysis of Veterinary Medical Data Base records (1970\u20131999)","volume":"165","author":"L Guptill","year":"2003","journal-title":"Veterinary Journal"},{"issue":"9","key":"pone.0272297.ref046","doi-asserted-by":"crossref","first-page":"1414","DOI":"10.2460\/javma.2000.216.1414","article-title":"Breed distribution of dogs with diabetes mellitus admitted to a tertiary care facility","volume":"216","author":"RS Hess","year":"2000","journal-title":"J Am Vet Med Assoc"},{"key":"pone.0272297.ref047","first-page":"740","article-title":"Characterization of naturally occurring diabetes in a colony of Golden Retrievers","volume":"40","author":"D. Malcolm","year":"1981","journal-title":"Fed Proc"},{"issue":"3","key":"pone.0272297.ref048","first-page":"285","article-title":"Urinary organic acids in natural early-onset insulin-dependent diabetic dogs","volume":"30","author":"Y Shigematsu","year":"1988","journal-title":"Acta Paediatrica Japonica"},{"issue":"3","key":"pone.0272297.ref049","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/S2213-8587(19)30412-7","article-title":"Type 1 diabetes-early life origins and changing epidemiology","volume":"8","author":"JM Norris","year":"2020","journal-title":"Lancet Diabetes Endocrinol"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0272297","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,25]],"date-time":"2023-11-25T10:19:29Z","timestamp":1700907569000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0272297"}},"subtitle":[],"editor":[{"given":"Simon","family":"Clegg","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2022,8,5]]},"references-count":49,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,8,5]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0272297","relation":{},"ISSN":["1932-6203"],"issn-type":[{"type":"electronic","value":"1932-6203"}],"subject":[],"published":{"date-parts":[[2022,8,5]]}}}