Analyze Diet
Chemosphere2018; 218; 652-661; doi: 10.1016/j.chemosphere.2018.11.136

Associations between endocrine disrupting chemicals and equine metabolic syndrome phenotypes.

Abstract: Equine Metabolic Syndrome (EMS) is characterized by abnormalities in insulin regulation, increased adiposity and laminitis, and has several similarities to human metabolic syndrome. A large amount of environmental variability in the EMS phenotype is not explained by commonly measured factors (diet, exercise, and season), suggesting that other environmental factors play a role in EMS development. Endocrine disrupting chemicals (EDCs) are associated with metabolic syndrome and other endocrine abnormalities in humans. This led us to hypothesize that EDCs are detectable in horse plasma and play a role in the pathophysiology of EMS. EDCs acting through the aryl hydrocarbon and estrogen receptors, were measured in plasma of 301 horses from 32 farms. The median (range) TEQ (2,3,7,8-TCDD equivalent) and EEQ (17β-estradiol equivalent) were 19.29 pg/g (0.59-536.36) and 10.50 pg/ml (4.35-15000.00), respectively. TEQ was negatively associated with plasma fat extracted and batch analyzed. EEQ was positively associated with pregnancy and batch analyzed, and negatively associated with being male and superfund score ≤100 miles of the farm. Of particular interest, serum glucose and insulin, glucose and insulin post oral sugar challenge, and leptin concentrations were associated with EEQ, and serum triglyceride concentration was associated with TEQ. Overall, we demonstrated that EDCs are present in the plasma of horses and may explain some of the environmental variability in measured EMS phenotypes. This is the first example of EDCs being associated with clinical disease phenotype components in domestic animals.
Publication Date: 2018-11-26 PubMed ID: 30502704PubMed Central: PMC6347404DOI: 10.1016/j.chemosphere.2018.11.136Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research article investigates the role of Endocrine Disrupting Chemicals (EDCs) in the occurrence of Equine Metabolic Syndrome (EMS) in horses. It concludes that EDCs present in a horse’s environment may majorly contribute to EMS development, establishing a new connection between these chemicals and clinical disease symptoms in domestic animals.

Objective of the Research

  • The main purpose of the study was to examine the relationship between Endocrine Disrupting Chemicals (EDCs) and Equine Metabolic Syndrome (EMS) traits. Despite common factors such as diet, exercise, and season being studied, there was still a significant amount of environmental variability unaccounted for in EMS symptoms. The researchers wanted to explore the possibility of the EDCs in the environment taking part in the development of EMS.

Methods Used

  • The research included measuring EDCs in the plasma of 301 horses from 32 farms. The EDCs specifically studied were those that could act through the aryl hydrocarbon and estrogen receptors.
  • The researchers also analyzed other variables like pregnancy status in mares, the gender of the horse, and the superfund score, which assesses environmental pollution levels within a 100-mile radius of the farm.

Results of the Study

  • The study found that EDCs were indeed present in horse plasma and were associated with the serum glucose, insulin, and leptin levels. Particularly, the estrogen equivalent (EEQ) was positively associated with pregnancy and negatively linked with male horses and low superfund scores.
  • Triglyceride concentration, another major metabolic factor, was associated with the 2,3,7,8-TCDD equivalent (TEQ).
  • Also, the batch analysis rendered significant results concerning EDC concentration and association with other variables.

Significance of the Research

  • This research significantly advances the understanding of Equine Metabolic Syndrome by highlighting the potential involvement of Endocrine Disrupting Chemicals in its development.
  • This is the first time EDCs have been associated with clinical disease symptoms in domestic animals, opening a new field of research that could have far-reaching implications for understanding metabolic disorders in both animals and humans.

Cite This Article

APA
Durward-Akhurst SA, Schultz NE, Norton EM, Rendahl AK, Besselink H, Behnisch PA, Brouwer A, Geor RJ, Mickelson JR, McCue ME. (2018). Associations between endocrine disrupting chemicals and equine metabolic syndrome phenotypes. Chemosphere, 218, 652-661. https://doi.org/10.1016/j.chemosphere.2018.11.136

Publication

ISSN: 1879-1298
NlmUniqueID: 0320657
Country: England
Language: English
Volume: 218
Pages: 652-661
PII: S0045-6535(18)32243-4

Researcher Affiliations

Durward-Akhurst, S A
  • Department of Veterinary Population Medicine, 225 Veterinary Medical Center, 1365 Gortner Avenue, St. Paul, MN, 55108, United States. Electronic address: durwa004@umn.edu.
Schultz, N E
  • Department of Veterinary Population Medicine, 225 Veterinary Medical Center, 1365 Gortner Avenue, St. Paul, MN, 55108, United States.
Norton, E M
  • Department of Veterinary Population Medicine, 225 Veterinary Medical Center, 1365 Gortner Avenue, St. Paul, MN, 55108, United States.
Rendahl, A K
  • College of Veterinary Medicine, 1988 Fitch Avenue, St. Paul, 55108, United States.
Besselink, H
  • BioDetection Systems b.v., Science Park 406, 1098 XH Amsterdam, the Netherlands.
Behnisch, P A
  • BioDetection Systems b.v., Science Park 406, 1098 XH Amsterdam, the Netherlands.
Brouwer, A
  • BioDetection Systems b.v., Science Park 406, 1098 XH Amsterdam, the Netherlands.
Geor, R J
  • College of Sciences, B2.13, Science Tower B, Massey University, Palmerston North, New Zealand.
Mickelson, J R
  • Department of Veterinary and Biomedical Sciences, 301 Veterinary Science Building, 1971 Commonwealth Avenue, St. Paul, 55108, United States.
McCue, M E
  • Department of Veterinary Population Medicine, 225 Veterinary Medical Center, 1365 Gortner Avenue, St. Paul, MN, 55108, United States.

MeSH Terms

  • Animals
  • Blood Glucose
  • Endocrine Disruptors / blood
  • Endocrine Disruptors / chemistry
  • Female
  • Horse Diseases / etiology
  • Horse Diseases / metabolism
  • Horses
  • Insulin / blood
  • Leptin / blood
  • Male
  • Metabolic Syndrome / etiology
  • Metabolic Syndrome / metabolism
  • Phenotype
  • Pregnancy

Grant Funding

  • T32 OD010993 / NIH HHS

Conflict of Interest Statement

none

References

This article includes 70 references
  1. Ayotte P, Dewailly E, Lambert GH, Perkins SL, Poon R, Feeley M, Larochelle C, Pereg D. Biomarker measurements in a coastal fish-eating population environmentally exposed to organochlorines.. Environ Health Perspect 2005 Oct;113(10):1318-24.
    pmc: PMC1281273pubmed: 16203240doi: 10.1289/ehp.7970google scholar: lookup
  2. Bailey SR, Habershon-Butcher JL, Ransom KJ, Elliott J, Menzies-Gow NJ. Hypertension and insulin resistance in a mixed-breed population of ponies predisposed to laminitis.. Am J Vet Res 2008 Jan;69(1):122-9.
    pubmed: 18167097doi: 10.2460/ajvr.69.1.122google scholar: lookup
  3. Behnisch P, Besselink H, Malonek L, Limone A, Pizzolante A, Pierri A, Ferro A, Gallo A, Buoperba C, Pierri B, Di Stasio A, Cerino P, Durward-Akhurst S, Schultz N, Norton E, Rendahl A, Geor R, Mickelson J, McCue M, Brouwer A. Blood plasma monitoring of contaminants in human and domestic animals using a panel of CALUX bioassays: three case studies.. Organohalogen Compounds 2018; pp. 92–94.
  4. Bergman A, Heindel JJ, Kasten T, Kidd KA, Jobling S, Neira M, Zoeller RT, Becher G, Bjerregaard P, Bornman R, Brandt I, Kortenkamp A, Muir D, Drisse MN, Ochieng R, Skakkebaek NE, Byléhn AS, Iguchi T, Toppari J, Woodruff TJ. The impact of endocrine disruption: a consensus statement on the state of the science.. Environ Health Perspect 2013 Apr;121(4):A104-6.
    pmc: PMC3620733pubmed: 23548368doi: 10.1289/ehp.1205448google scholar: lookup
  5. Besselink H. Validation of the (anti-) ERα CALUX bioassay U2-OS cells Transcriptional ERalpha CALUX- assay for the detection of estrogenic and anti-estrogenic chemicals for inclusion in TG455.. 2015.
  6. Birnbaum LS. Environmental chemicals: evaluating low-dose effects.. Environ Health Perspect 2012 Apr;120(4):A143-4.
    pmc: PMC3339483pubmed: 22470049doi: 10.1289/ehp.1205179google scholar: lookup
  7. Carter RA, Treiber KH, Geor RJ, Douglass L, Harris PA. Prediction of incipient pasture-associated laminitis from hyperinsulinaemia, hyperleptinaemia and generalised and localised obesity in a cohort of ponies.. Equine Vet J 2009 Feb;41(2):171-8.
    pubmed: 19418747doi: 10.2746/042516408x342975google scholar: lookup
  8. Cartmill JA, Thompson DL Jr, Storer WA, Gentry LR, Huff NK. Endocrine responses in mares and geldings with high body condition scores grouped by high vs. low resting leptin concentrations.. J Anim Sci 2003 Sep;81(9):2311-21.
    pubmed: 12968707doi: 10.2527/2003.8192311xgoogle scholar: lookup
  9. Casals-Casas C, Desvergne B. Endocrine disruptors: from endocrine to metabolic disruption.. Annu Rev Physiol 2011;73:135-62.
  10. Chou IC, Lee WJ, Wang LC, Chang-Chien GP, Lee WS, Lee H. Validation of the CALUX bioassay as a screening and semi-quantitative method for PCDD/F levels in cow's milk.. J Hazard Mater 2008 Jun 15;154(1-3):1166-72.
    pubmed: 18191892doi: 10.1016/j.jhazmat.2007.11.023google scholar: lookup
  11. Cranmer M, Louie S, Kennedy RH, Kern PA, Fonseca VA. Exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) is associated with hyperinsulinemia and insulin resistance.. Toxicol Sci 2000 Aug;56(2):431-6.
    pubmed: 10911003doi: 10.1093/toxsci/56.2.431google scholar: lookup
  12. Elobeid MA, Padilla MA, Brock DW, Ruden DM, Allison DB. Endocrine disruptors and obesity: an examination of selected persistent organic pollutants in the NHANES 1999-2002 data.. Int J Environ Res Public Health 2010 Jul;7(7):2988-3005.
    pmc: PMC2922741pubmed: 20717554doi: 10.3390/ijerph7072988google scholar: lookup
  13. Feil VJ, Ellis RL. The USDA perspective on dioxin concentrations in dairy and beef.. J Anim Sci 1998 Jan;76(1):152-9.
    pubmed: 9464896doi: 10.2527/1998.761152xgoogle scholar: lookup
  14. Frank N, Bailey S, Bertin F-R, Burns T, de Laat M, Durham A, Kritchevsky J, Menzies-Gow N, Tadros L. Recommendations for the Diagnosis and Treatment of Equine Metabolic Syndrome (EMS).. 2018.
  15. Frank N, Elliott SB, Brandt LE, Keisler DH. Physical characteristics, blood hormone concentrations, and plasma lipid concentrations in obese horses with insulin resistance.. J Am Vet Med Assoc 2006 May 1;228(9):1383-90.
    pubmed: 16649943doi: 10.2460/javma.228.9.1383google scholar: lookup
  16. Frank N, Geor RJ, Bailey SR, Durham AE, Johnson PJ. Equine metabolic syndrome.. J Vet Intern Med 2010 May-Jun;24(3):467-75.
  17. Gentry LR, Thompson DL Jr, Gentry GT Jr, Davis KA, Godke RA, Cartmill JA. The relationship between body condition, leptin, and reproductive and hormonal characteristics of mares during the seasonal anovulatory period.. J Anim Sci 2002 Oct;80(10):2695-703.
    pubmed: 12413093doi: 10.2527/2002.80102695xgoogle scholar: lookup
  18. Gordon JDC, Chu AC, Denison MS, Clark GC. Detection of estrogen receptor endocrine disruptor potency of commonly used organochlorine pesticides using the LUMI-CELL ER bioassay.. Organohalogen compounds 2004;66:2967–2973.
  19. Gregoraszczuk EL, Ptak A. Endocrine-Disrupting Chemicals: Some Actions of POPs on Female Reproduction.. Int J Endocrinol 2013;2013:828532.
    pmc: PMC3674739pubmed: 23762054doi: 10.1155/2013/828532google scholar: lookup
  20. Henneke DR, Potter GD, Kreider JL, Yeates BF. Relationship between condition score, physical measurements and body fat percentage in mares.. Equine Vet J 1983 Oct;15(4):371-2.
  21. Henriksen GL, Ketchum NS, Michalek JE, Swaby JA. Serum dioxin and diabetes mellitus in veterans of Operation Ranch Hand.. Epidemiology 1997 May;8(3):252-8.
  22. Johnson PJ. The equine metabolic syndrome peripheral Cushing's syndrome.. Vet Clin North Am Equine Pract 2002 Aug;18(2):271-93.
    pubmed: 15635908doi: 10.1016/s0749-0739(02)00006-8google scholar: lookup
  23. Johnson PJ, Wiedmeyer CE, LaCarrubba A, Ganjam VK, Messer NT 4th. Diabetes, insulin resistance, and metabolic syndrome in horses.. J Diabetes Sci Technol 2012 May 1;6(3):534-40.
    pmc: PMC3440056pubmed: 22768883doi: 10.1177/193229681200600307google scholar: lookup
  24. Johnson PJ, Wiedmeyer CE, Messer NT, Ganjam VK. Medical implications of obesity in horses--lessons for human obesity.. J Diabetes Sci Technol 2009 Jan;3(1):163-74.
    pmc: PMC2769846pubmed: 20046661doi: 10.1177/193229680900300119google scholar: lookup
  25. Kim MJ, Marchand P, Henegar C, Antignac JP, Alili R, Poitou C, Bouillot JL, Basdevant A, Le Bizec B, Barouki R, Clément K. Fate and complex pathogenic effects of dioxins and polychlorinated biphenyls in obese subjects before and after drastic weight loss.. Environ Health Perspect 2011 Mar;119(3):377-83.
    pmc: PMC3060002pubmed: 21156398doi: 10.1289/ehp.1002848google scholar: lookup
  26. Lee DH, Steffes MW, Sjödin A, Jones RS, Needham LL, Jacobs DR Jr. Low dose organochlorine pesticides and polychlorinated biphenyls predict obesity, dyslipidemia, and insulin resistance among people free of diabetes.. PLoS One 2011 Jan 26;6(1):e15977.
  27. Lee DH, Lee IK, Porta M, Steffes M, Jacobs DR Jr. Relationship between serum concentrations of persistent organic pollutants and the prevalence of metabolic syndrome among non-diabetic adults: results from the National Health and Nutrition Examination Survey 1999-2002.. Diabetologia 2007 Sep;50(9):1841-1851.
    pubmed: 17624515doi: 10.1007/s00125-007-0755-4google scholar: lookup
  28. Lee DH, Lee IK, Song K, Steffes M, Toscano W, Baker BA, Jacobs DR Jr. A strong dose-response relation between serum concentrations of persistent organic pollutants and diabetes: results from the National Health and Examination Survey 1999-2002.. Diabetes Care 2006 Jul;29(7):1638-44.
    pubmed: 16801591doi: 10.2337/dc06-0543google scholar: lookup
  29. Lee DH, Steffes MW, Sjödin A, Jones RS, Needham LL, Jacobs DR Jr. Low dose of some persistent organic pollutants predicts type 2 diabetes: a nested case-control study.. Environ Health Perspect 2010 Sep;118(9):1235-42.
    pmc: PMC2944083pubmed: 20444671doi: 10.1289/ehp.0901480google scholar: lookup
  30. Lemaire G, Mnif W, Mauvais P, Balaguer P, Rahmani R. Activation of alpha- and beta-estrogen receptors by persistent pesticides in reporter cell lines.. Life Sci 2006 Aug 15;79(12):1160-9.
    pubmed: 16626760doi: 10.1016/j.lfs.2006.03.023google scholar: lookup
  31. Lenth R. emmeans: Estimated Marginal Means, aka Least-Squares Means.. 2018.
  32. Lindåse S, Nostell K, Bröjer J. A modified oral sugar test for evaluation of insulin and glucose dynamics in horses.. Acta Vet Scand 2016 Oct 20;58(Suppl 1):64.
    pmc: PMC5073908pubmed: 27766982doi: 10.1186/s13028-016-0246-zgoogle scholar: lookup
  33. Lundqvist C, Zuurbier M, Leijs M, Johansson C, Ceccatelli S, Saunders M, Schoeters G, ten Tusscher G, Koppe JG. The effects of PCBs and dioxins on child health.. Acta Paediatr Suppl 2006 Oct;95(453):55-64.
    pubmed: 17000571doi: 10.1080/08035320600886257google scholar: lookup
  34. Magliano DJ, Loh VHY, Harding JL, Botton J, Shaw JE. Persistent organic pollutants and diabetes: a review of the epidemiological evidence.. Diabetes Metab 2014 Feb;40(1):1-14.
    pubmed: 24262435doi: 10.1016/j.diabet.2013.09.006google scholar: lookup
  35. Mandal PK. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology.. J Comp Physiol B 2005 May;175(4):221-30.
    pubmed: 15900503doi: 10.1007/s00360-005-0483-3google scholar: lookup
  36. McCue M, Geor R, Schultz N. Equine metabolic syndrome: a complex disease influenced by genetics and the environment.. Journal of Equine Veterinary Science 2015;35:367–375.
  37. Melnick R, Lucier G, Wolfe M, Hall R, Stancel G, Prins G, Gallo M, Reuhl K, Ho SM, Brown T, Moore J, Leakey J, Haseman J, Kohn M. Summary of the National Toxicology Program's report of the endocrine disruptors low-dose peer review.. Environ Health Perspect 2002 Apr;110(4):427-31.
    pmc: PMC1240807pubmed: 11940462doi: 10.1289/ehp.02110427google scholar: lookup
  38. Menzies-Gow NJ, Harris PA, Elliott J. Prospective cohort study evaluating risk factors for the development of pasture-associated laminitis in the United Kingdom.. Equine Vet J 2017 May;49(3):300-306.
    pubmed: 27363591doi: 10.1111/evj.12606google scholar: lookup
  39. Michalek JE, Akhtar FZ, Kiel JL. Serum dioxin, insulin, fasting glucose, and sex hormone-binding globulin in veterans of Operation Ranch Hand.. J Clin Endocrinol Metab 1999 May;84(5):1540-3.
    pubmed: 10323376doi: 10.1210/jcem.84.5.5663google scholar: lookup
  40. Murk AJL, P E G, Bulder AS, Jonas AS, Rozemeijer MJC, Denison MS. The CALUX (chemical-activated luciferase expression) assay adapted and validated for measuring TCDD equivalents in blood plasma.. Environ Toxicol Chem 1997;16:1583–1589.
  41. Neel BA, Sargis RM. The paradox of progress: environmental disruption of metabolism and the diabetes epidemic.. Diabetes 2011 Jul;60(7):1838-48.
    pmc: PMC3121438pubmed: 21709279doi: 10.2337/db11-0153google scholar: lookup
  42. Norton EM, Schultz NE, Rendahl AK, Mcfarlane D, Geor RJ, Mickelson JR, McCue ME. Heritability of metabolic traits associated with equine metabolic syndrome in Welsh ponies and Morgan horses.. Equine Vet J 2019 Jul;51(4):475-480.
    pubmed: 30472742doi: 10.1111/evj.13053google scholar: lookup
  43. Novelli M, Piaggi S, De Tata V. 2,3,7,8-Tetrachlorodibenzo-p-dioxin-induced impairment of glucose-stimulated insulin secretion in isolated rat pancreatic islets.. Toxicol Lett 2005 Apr 10;156(2):307-14.
    pubmed: 15737493doi: 10.1016/j.toxlet.2004.12.004google scholar: lookup
  44. OECD. Guideline forTesting of Chemicals. Performance-Based Test Guideline for Stably Transfected Transactivation In Vitro Assays to Detect Estrogen Receptor Agonists and Antagonists (TG455).. 2015.
  45. Opitz CA, Litzenburger UM, Sahm F, Ott M, Tritschler I, Trump S, Schumacher T, Jestaedt L, Schrenk D, Weller M, Jugold M, Guillemin GJ, Miller CL, Lutz C, Radlwimmer B, Lehmann I, von Deimling A, Wick W, Platten M. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor.. Nature 2011 Oct 5;478(7368):197-203.
    pubmed: 21976023doi: 10.1038/nature10491google scholar: lookup
  46. Park WH, Jun DW, Kim JT, Jeong JH, Park H, Chang YS, Park KS, Lee HK, Pak YK. Novel cell-based assay reveals associations of circulating serum AhR-ligands with metabolic syndrome and mitochondrial dysfunction.. Biofactors 2013 Jul-Aug;39(4):494-504.
    pubmed: 23361953doi: 10.1002/biof.1092google scholar: lookup
  47. Pass MA, Pollitt S, Pollitt CC. Decreased glucose metabolism causes separation of hoof lamellae in vitro: a trigger for laminitis?. Equine Vet J Suppl 1998 Sep;(26):133-8.
  48. Pauwels A, Covaci A, Weyler J, Delbeke L, Dhont M, De Sutter P, D'Hooghe T, Schepens PJ. Comparison of persistent organic pollutant residues in serum and adipose tissue in a female population in Belgium, 1996-1998.. Arch Environ Contam Toxicol 2000 Aug;39(2):265-70.
    pubmed: 10871430doi: 10.1007/s002440010104google scholar: lookup
  49. Pedersen M, Halldorsson TI, Mathiesen L, Mose T, Brouwer A, Hedegaard M, Loft S, Kleinjans JCS, Besselink H, Knudsen LE. Dioxin-like exposures and effects on estrogenic and androgenic exposures and micronuclei frequency in mother-newborn pairs.. Environ Int 2010 May;36(4):344-351.
    pubmed: 20189248doi: 10.1016/j.envint.2010.02.002google scholar: lookup
  50. R Core Team. R: A language environment for statistical computing.. 2013.
  51. Reaven GM. Insulin resistance: the link between obesity and cardiovascular disease.. Med Clin North Am 2011 Sep;95(5):875-92.
    pubmed: 21855697doi: 10.1016/j.mcna.2011.06.002google scholar: lookup
  52. Rhind SM. Endocrine disrupting compounds and farm animals: their properties, actions and routes of exposure.. Domest Anim Endocrinol 2002 Jul;23(1-2):179-87.
    pubmed: 12142236doi: 10.1016/s0739-7240(02)00155-8google scholar: lookup
  53. Rychen G, Jurjanz S, Toussaint H, Feidt C. Dairy ruminant exposure to persistent organic pollutants and excretion to milk.. Animal 2008 Feb;2(2):312-23.
    pubmed: 22445026doi: 10.1017/s1751731107001139google scholar: lookup
  54. Schultz N. Characterization of equine metabolic syndrome and mapping of candidate genetic loci.. 2016.
  55. Smith BP. Large animal internal medicine.. 2015.
  56. Sonneveld E, Jansen HJ, Riteco JA, Brouwer A, van der Burg B. Development of androgen- and estrogen-responsive bioassays, members of a panel of human cell line-based highly selective steroid-responsive bioassays.. Toxicol Sci 2005 Jan;83(1):136-48.
    pubmed: 15483189doi: 10.1093/toxsci/kfi005google scholar: lookup
  57. ten Tusscher GW, Koppe JG. Perinatal dioxin exposure and later effects--a review.. Chemosphere 2004 Mar;54(9):1329-36.
    pubmed: 14659426doi: 10.1016/s0045-6535(03)00254-6google scholar: lookup
  58. Terqui M, Palmer E. Oestrogen pattern during early pregnancy in the mare.. J Reprod Fertil Suppl 1979;(27):441-6.
    pubmed: 289820
  59. Thackaberry EA, Bedrick EJ, Goens MB, Danielson L, Lund AK, Gabaldon D, Smith SM, Walker MK. Insulin regulation in AhR-null mice: embryonic cardiac enlargement, neonatal macrosomia, and altered insulin regulation and response in pregnant and aging AhR-null females.. Toxicol Sci 2003 Dec;76(2):407-17.
    pubmed: 12970579doi: 10.1093/toxsci/kfg229google scholar: lookup
  60. Treiber KH, Kronfeld DS, Hess TM, Byrd BM, Splan RK, Staniar WB. Evaluation of genetic and metabolic predispositions and nutritional risk factors for pasture-associated laminitis in ponies.. J Am Vet Med Assoc 2006 May 15;228(10):1538-45.
    pubmed: 16677122doi: 10.2460/javma.228.10.1538google scholar: lookup
  61. United States Environmental Protection Agency. Persistent Organic Pollutants: A Global Issue, A Global Response.. 2013.
  62. Vafeiadi M, Agramunt S, Papadopoulou E, Besselink H, Mathianaki K, Karakosta P, Spanaki A, Koutis A, Chatzi L, Vrijheid M, Kogevinas M. In utero exposure to dioxins and dioxin-like compounds and anogenital distance in newborns and infants.. Environ Health Perspect 2013 Jan;121(1):125-30.
    pmc: PMC3553434pubmed: 23171674doi: 10.1289/ehp.1205221google scholar: lookup
  63. Van Wouwe N, Windal I, Vanderperren H, Eppe G, Xhrouet C, Massart AC, Debacker N, Sasse A, Baeyens W, De Pauw E, Sartor F, Van Oyen H, Goeyens L. Validation of the CALUX bioassay for PCDD/F analyses in human blood plasma and comparison with GC-HRMS.. Talanta 2004 Aug 8;63(5):1157-67.
    pubmed: 18969545doi: 10.1016/j.talanta.2004.05.028google scholar: lookup
  64. Vandenberg LN. Non-monotonic dose responses in studies of endocrine disrupting chemicals: bisphenol a as a case study.. Dose Response 2014 May;12(2):259-76.
  65. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, Shioda T, Soto AM, vom Saal FS, Welshons WV, Zoeller RT, Myers JP. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses.. Endocr Rev 2012 Jun;33(3):378-455.
    pmc: PMC3365860pubmed: 22419778doi: 10.1210/er.2011-1050google scholar: lookup
  66. Verhulst SL, Nelen V, Hond ED, Koppen G, Beunckens C, Vael C, Schoeters G, Desager K. Intrauterine exposure to environmental pollutants and body mass index during the first 3 years of life.. Environ Health Perspect 2009 Jan;117(1):122-6.
    pmc: PMC2627855pubmed: 19165398doi: 10.1289/ehp.0800003google scholar: lookup
  67. Vick MM, Sessions DR, Murphy BA, Kennedy EL, Reedy SE, Fitzgerald BP. Obesity is associated with altered metabolic and reproductive activity in the mare: effects of metformin on insulin sensitivity and reproductive cyclicity.. Reprod Fertil Dev 2006;18(6):609-17.
    pubmed: 16930507doi: 10.1071/rd06016google scholar: lookup
  68. Wielsøe M, Eiberg H, Ghisari M, Kern P, Lind O, Bonefeld-Jørgensen EC. Genetic Variations, Exposure to Persistent Organic Pollutants and Breast Cancer Risk - A Greenlandic Case-Control Study.. Basic Clin Pharmacol Toxicol 2018 Sep;123(3):335-346.
    pubmed: 29510000doi: 10.1111/bcpt.13002google scholar: lookup
  69. Wooldridge AA, Edwards HG, Plaisance EP, Applegate R, Taylor DR, Taintor J, Zhong Q, Judd RL. Evaluation of high-molecular weight adiponectin in horses.. Am J Vet Res 2012 Aug;73(8):1230-40.
    pubmed: 22849684doi: 10.2460/ajvr.73.8.1230google scholar: lookup
  70. Zhou H, Qu Y, Wu H, Liao C, Zheng J, Diao X, Xue Q. Molecular phylogenies and evolutionary behavior of AhR (aryl hydrocarbon receptor) pathway genes in aquatic animals: implications for the toxicology mechanism of some persistent organic pollutants (POPs).. Chemosphere 2010 Jan;78(2):193-205.

Citations

This article has been cited 6 times.
  1. Al Naem M, Bourebaba L, Kucharczyk K, Röcken M, Marycz K. Therapeutic mesenchymal stromal stem cells: Isolation, characterization and role in equine regenerative medicine and metabolic disorders. Stem Cell Rev Rep 2020 Apr;16(2):301-322.
    doi: 10.1007/s12015-019-09932-0pubmed: 31797146google scholar: lookup
  2. Norton E, Schultz N, Geor R, McFarlane D, Mickelson J, McCue M. Genome-Wide Association Analyses of Equine Metabolic Syndrome Phenotypes in Welsh Ponies and Morgan Horses. Genes (Basel) 2019 Nov 6;10(11).
    doi: 10.3390/genes10110893pubmed: 31698676google scholar: lookup
  3. Mullen KR, Saklou N, Kiehl A, Ong TC, Strecker GJ, Toro S, VandeWoude S, Brooks IM, Webb TL, Haendel MA. The missing link: electronic health record linkage across species offers opportunities for improving One Health. JAMIA Open 2025 Dec;8(6):ooaf151.
    doi: 10.1093/jamiaopen/ooaf151pubmed: 41245152google scholar: lookup
  4. Nie J, Huang Z, Wen L, Li H, Xie Q, Wang H, Lai Z, Lin C, Jing C. Association between exposure to terpene compounds and risk of metabolic syndrome: exploring the potential mediating role of inflammatory response. Front Endocrinol (Lausanne) 2025;16:1551784.
    doi: 10.3389/fendo.2025.1551784pubmed: 40395814google scholar: lookup
  5. Mullen KR, Saklou N, Kiehl A, Ong TC, Strecker GJ, Toro S, VandeWoude S, Brooks IM, Webb T, Haendel MA. The missing link: Electronic health record linkage across species offers opportunities for improving One Health. medRxiv 2025 Mar 26;.
    doi: 10.1101/2025.03.25.25324490pubmed: 40196252google scholar: lookup
  6. He K, Chen R, Xu S, Ding Y, Wu Z, Bao M, He B, Li S. Environmental endocrine disruptor-induced mitochondrial dysfunction: a potential mechanism underlying diabetes and its complications. Front Endocrinol (Lausanne) 2024;15:1422752.
    doi: 10.3389/fendo.2024.1422752pubmed: 39211449google scholar: lookup