Hostname: page-component-77c89778f8-n9wrp Total loading time: 0 Render date: 2024-07-21T02:28:02.707Z Has data issue: false hasContentIssue false
  • English
  • Français

Food contaminants and programming of type 2 diabetes: recent findings from animal studies

Published online by Cambridge University Press:  13 June 2016

S. Firmin ,
N. Bahi-Jaber  and
L. Abdennebi-Najar
S. Firmin
Affiliation:
UP-EGEAL 2012.10.120, Institut Polytechnique laSalle Beauvais, Beauvais, France
N. Bahi-Jaber
Affiliation:
UP-EGEAL 2012.10.120, Institut Polytechnique laSalle Beauvais, Beauvais, France
L. Abdennebi-Najar*
Affiliation:
UP-EGEAL 2012.10.120, Institut Polytechnique laSalle Beauvais, Beauvais, France
*
*Address for correspondence: L. Abdennebi-Najar, UP-EGEAL 2012. 10.120. S. Firmin, UP EGEAL 2012.10.120, Institut Polytechnique laSalle Beauvais, 19 Rue Pierre Waguet, 60000 Beauvais, France. (Emails Latifa.najar@lasalle-beauvais.fr; stephane.firmin@lasalle-beauvais.fr)
Get access Rights & Permissions [Opens in a new window]

Abstract

It is now accepted that the way our health evolves with aging is intimately linked to the quality of our early life. The present review highlights the emerging data of Developmental Origins of Health and Disease field on developmental disruption by toxicants and their subsequent effect on type 2 diabetes. We report adverse neonatal effects of several food contaminants during pregnancy and lactation, among them bisphenol A, chlorpyrifos, perfluorinated chemicals on pancreas integrity and functionality in later life. The described alterations, in conjunction with disruption of β cell mass in early life, can lead to dysregulation of glucose metabolism, insulin synthesis, which facilitates the development of insulin resistance and progression of diabetes in the adult. Despite limited and often inconclusive epidemiologic and experimental data, more recent data clearly show that infants appear to be at increased risk of type 2 diabetes in later life. This may be a result of continued exposure to chemical food contaminants during the critical window of pancreas development. In societies already burdened with increased incidence of non-communicable chronic diseases, there is a clear need for information regarding the potential harmful effects of chemical food contaminants on adult health diseases.

Keywords

animal modelsβ cellfood contaminantsdevelopmental programmingtype 2 diabetes
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 5: Themed Issue: Australia/New Zealand 2015 DOHaD Scientific Meeting: Advances and Updates , October 2016 , pp. 505 - 512
Check for updates
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1. Barker, DJ. Fetal origins of coronary heart disease. Br Heart J. 1993; 69, 195–196.Google Scholar
2. Hales, CN, Barker, DJ, Clark, PM, et al. Fetal and infant growth and impaired glucose tolerance at age 64. Br Med J. 1991; 303, 1019–1022.CrossRefGoogle ScholarPubMed
3. Lillycrop, KA, Burdge, GC. Epigenetic mechanisms linking early nutrition to long term health. Best Pract Res Clin Endocrinol Metab. 2015; 26, 667–676.CrossRefGoogle Scholar
4. Attig, L, Djiane, J, Gertler, A, et al. Study of hypothalamic leptin receptor expression in low-birth-weight piglets and effects of leptin supplementation on neonatal growth and development. Am J Physiol Endocrinol Metab. 2008; 295, E1117–E1125.Google Scholar
5. Attig, L, Brisard, D, Larcher, T, et al. Postnatal leptin promotes organ maturation and development in IUGR piglets. PLoS One. 2013; 8, e64616.Google Scholar
6. Mayhoub, F, Berton, T, Bach, V, et al. Self-reported parental exposure to pesticide during pregnancy and birth outcomes: the MecoExpo cohort study. PLoS One. 2014; 9, e99090.Google Scholar
7. Landrigan, PJ. Children’s environmental health: a brief history. Acad Pediatr. 2015; 16, 1–9.CrossRefGoogle ScholarPubMed
8. Lozowicka, B. Health risk for children and adults consuming apples with pesticide residue. Sci Total Environ. 2015; 502, 184–198.CrossRefGoogle ScholarPubMed
9. Landrigan, PJ, Sonawane, B, Mattison, D, McCally, M, Garg, A. Chemical contaminants in breast milk and their impacts on children’s health: an overview. Environ Health Perspect. 2002; 110, A313–A315.Google Scholar
10. LaKind, JS, Amina Wilkins, A, Berlin, CM Jr. Environmental chemicals in human milk: a review of levels, infant exposures and health, and guidance for future research. Toxicol Appl Pharmacol. 2004; 198, 184–208.Google Scholar
11. Zhang, T, Ma, Y, Wang, D, et al. Placental transfer of and infantile exposure to perchlorate. Chemosphere. 2016; 144, 948–954.Google Scholar
12. Barr, DB, Bishop, A, Needham, LL. Concentrations of xenobiotic chemicals in the maternal-fetal unit. Reprod Toxicol. 2007; 23, 260–266.CrossRefGoogle ScholarPubMed
13. Elmhiri, G, Mahmood, DFD, Niquet-Leridon, C, et al. Formula-derived advanced glycation end products are involved in the development of long-term inflammation and oxidative stress in kidney of IUGR piglets. Mol Nutr Food Res. 2015; 59, 939–947.Google Scholar
14. Mostafalou, S, Abdollahi, M. Pesticides and human chronic diseases: evidences, mechanisms, and perspectives. Toxicol Appl Pharmacol. 2013; 268, 157–177.Google Scholar
15. Shapiro, GD, Dodds, L, Arbuckle, TE, et al. Exposure to phthalates, bisphenol A and metals in pregnancy and the association with impaired glucose tolerance and gestational diabetes mellitus: the MIREC study. Environ Int. 2015; 83, 63–71.Google Scholar
16. Lasram, MM, Dhouib, IB, Annabi, A, El Fazaa, S, Gharbi, N. A review on the molecular mechanisms involved in insulin resistance induced by organophosphorus pesticides. Toxicology. 2014; 322, 1–13.Google Scholar
17. Schug, TT, Janesick, A, Blumberg, B, Heindel, JJ. Endocrine disrupting chemicals and disease susceptibility. J Steroid Biochem Mol Biol. 2011; 127, 204–215.Google Scholar
18. Scheuplein, R, Charnley, G, Dourson, M. Differential sensitivity of children and adults to chemical toxicity: I. Biological basis. Regul Toxicol Pharmacol. 2002; 35, 429–447.Google Scholar
19. Jensen, J. Gene regulatory factors in pancreatic development. Dev Dyn. 2004; 229, 176–200.Google Scholar
20. Gregg, BE, Moore, PC, Demozay, D, et al. Formation of a human β-cell population within pancreatic islets is set early in life. J Clin Endocrinol Metab. 2012; 97, 3197–3206.Google Scholar
21. Ackermann, AM, Gannon, M. Molecular regulation of pancreatic β-cell mass development, maintenance, and expansion. J Mol Endocrinol. 2007; 38, 193–206.Google Scholar
22. Meier, JJ, Bonadonna, RC. Role of reduced β-cell mass versus impaired β-cell function in the pathogenesis of type 2 diabetes. Diabetes Care. 2013; 36, S113–S119.Google Scholar
23. Fernandez-Twinn, DS, Ozanne, SE. Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome. Physiol Behav. 2006; 88, 234–243.Google Scholar
24. Aref, A-BM, Ahmed, OM, Ali, LA, Semmler, M. Maternal rat diabetes mellitus deleteriously affects insulin sensitivity and beta-cell function in the offspring. J Diabetes Res. 2013; 2013, 429154.Google Scholar
25. Reusens, B, Remacle, C. Programming of the endocrine pancreas by the early nutritional environment. Int J Biochem Cell Biol. 2006; 38, 913–922.Google Scholar
26. Portha, B, Chavey, A, Movassat, J. Early-life origins of type 2 diabetes: fetal programming of the beta-cell mass. Exp Diabetes Res. 2011; 2011, 105076.Google Scholar
27. Lim, S, Ahn, SY, Song, IC, et al. Chronic exposure to the herbicide, atrazine, causes mitochondrial dysfunction and insulin resistance. PLoS One. 2009; 4, 1–11.CrossRefGoogle Scholar
28. Mailloux, R, Fu, A, Florian, M, et al. A Northern contaminant mixture impairs pancreas function in obese and lean JCR rats and inhibits insulin secretion in MIN6 cells. Toxicology. 2015; 334, 81–93.Google Scholar
29. Hectors, TLM, Vanparys, C, Pereira-Fernandes, A, Martens, GA, Blust, R. Evaluation of the INS-1 832/13 cell line as a beta-cell based screening system to assess pollutant effects on beta-cell function. PLoS One. 2013; 8, 1–10.Google Scholar
30. Taylor, KW, Novak, RF, Anderson, HA, et al. Evaluation of the association between persistent organic pollutants (POPS) and diabetes in epidemiological studies: a national toxicology program workshop review. Environ Health Perspect. 2013; 121, 774–783.CrossRefGoogle ScholarPubMed
31. Kuo, C. Environmental chemicals and type 2 diabetes. Curr Diab Rep. 2013; 13, 831–849.Google Scholar
32. Evangelou, E, Ntritsos, G, Chondrogiorgi, M, et al. Exposure to pesticides and diabetes: a systematic review and meta-analysis. Environ Int. 2016; 91, 60–68.Google Scholar
33. Magliano, DJ, Loh, VHY, Harding, JL, Botton, J, Shaw, JE. Persistent organic pollutants and diabetes: a review of the epidemiological evidence. Diabetes Metab. 2014; 40, 1–14.Google Scholar
34. Vaiserman, AM. Early-life exposure to substance abuse and risk of type 2 diabetes in adulthood. Curr Diab Rep. 2015; 15, 1–7.Google Scholar
35. Barouki, R, Gluckman, PD, Grandjean, P, Hanson, M, Heindel, JJ. Developmental origins of non-communicable disease: implications for research and public health. Environ Health. 2012; 11, 1–9.Google Scholar
36. Somm, E, Schwitzgebel, VM, Toulotte, A, et al. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect. 2009; 117, 1549–1555.Google Scholar
37. Angle, BM, Do, RP, Ponzi, D, et al. Metabolic disruption in male mice due to fetal exposure to low but not high doses of bisphenol A (BPA): evidence for effects on body weight, food intake, adipocytes, leptin, adiponectin, insulin and glucose regulation. Reprod Toxicol. 2013; 42, 256–268.Google Scholar
38. Anderson, OS, Peterson, KE, Sanchez, BN, et al. Perinatal bisphenol A exposure promotes hyperactivity, lean body composition, and hormonal responses across the murine life course. FASEB J. 2013; 27, 1784–1792.Google Scholar
39. García-Arevalo, M, Alonso-Magdalena, P, Rebelo Dos Santos, J, et al. Exposure to bisphenol-A during pregnancy partially mimics the effects of a high-fat diet altering glucose homeostasis and gene expression in adult male mice. PLoS One. 2014; 9, e100214.Google Scholar
40. Liu, J, Yu, P, Qian, W, et al. Perinatal bisphenol A exposure and adult glucose homeostasis: identifying critical windows of exposure. PLoS One. 2013; 8, e64143.Google Scholar
41. Alonso-Magdalena, P, Vieira, E, Soriano, S, et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect. 2010; 118, 1243–1250.Google Scholar
42. Wei, J, Lin, Y, Li, Y, et al. Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology. 2011; 152, 3049–3061.Google Scholar
43. Li, G, Chang, H, Xia, W, et al. F0 maternal BPA exposure induced glucose intolerance of F2 generation through DNA methylation change in Gck. Toxicol Lett. 2014; 228, 192–199.Google Scholar
44. Lin, Y, Wei, J, Li, Y, et al. Developmental exposure to di ( 2-ethylhexyl) phthalate impairs endocrine pancreas and leads to long-term adverse effects on glucose homeostasis in the rat. Am J Physiol Endocrinol Metab. 2011; 301, E527–E538.Google Scholar
45. Rajesh, P, Balasubramanian, K. Gestational exposure to di(2-ethylhexyl) phthalate (DEHP) impairs pancreatic β-cell function in F1 rat offspring. Toxicol Lett. 2015; 232, 46–57.Google Scholar
46. Mangala Priya, V, Mayilvanan, C, Akilavalli, N, Rajesh, P, Balasubramanian, K. Lactational exposure of phthalate impairs insulin signaling in the cardiac muscle of F1 female Albino rats. Cardiovasc Toxicol. 2014; 14, 10–20.Google Scholar
47. Rajesh, P, Balasubramanian, K. Phthalate exposure in utero causes epigenetic changes and impairs insulin signalling. J Endocrinol. 2014; 223, 47–66.Google Scholar
48. Bro-Rasmussen, F. Contamination by persistent chemicals in food chain and human health. Sci Total Environ. 1996; 188, S45–S60.CrossRefGoogle ScholarPubMed
49. Squadrone, S, Ciccotelli, V, Favaro, L, et al. Fish consumption as a source of human exposure to perfluorinated alkyl substances in Italy: analysis of two edible fish from Lake Maggiore. Chemosphere. 2014; 114, 181–186.CrossRefGoogle ScholarPubMed
50. Frederiksen, M, Vorkamp, K, Thomsen, M, Knudsen, LE. Human internal and external exposure to PBDEs – a review of levels and sources. Int J Hyg Environ Health. 2009; 212, 109–134.Google Scholar
51. Dórea, JG. Persistent, bioaccumulative and toxic substances in fish: human health considerations. Sci Total Environ. 2008; 400, 93–114.Google Scholar
52. Arnich, N, Sirot, V, Rivière, G, et al. Dietary exposure to trace elements and health risk assessment in the 2nd French total diet study. Food Chem Toxicol. 2012; 50, 2432–2449.Google Scholar
53. Nougadère, A, Sirot, V, Kadar, A, et al. Total diet study on pesticide residues in France: levels in food as consumed and chronic dietary risk to consumers. Environ Int. 2012; 45, 135–150.Google Scholar
54. Rivière, G, Sirot, V, Tard, A, et al. Food risk assessment for perfluoroalkyl acids and brominated flame retardants in the French population: results from the second French total diet study. Sci Total Environ. 2014; 491–492, 176–183.Google Scholar
55. Konecki, J, Błazejowski, J, Słowiński, J, Helewski, K. Influence of chronic cadmium exposure during pregnancy on DNA synthesis in different organs of rat offspring. Med Sci Monit. 2000; 6, 1077–1081.Google Scholar
56. Faulk, C, Barks, A, Sánchez, BN, et al. Perinatal lead (Pb) exposure results in sex-specific effects on food intake, fat, weight, and insulin response across the murine life-course. PLoS One. 2014; 9, e104273.Google Scholar
57. Hines, EP, White, SS, Stanko, JP, et al. Phenotypic dichotomy following developmental exposure to perfluorooctanoic acid (PFOA) in female CD-1 mice: low doses induce elevated serum leptin and insulin, and overweight in mid-life. Mol Cell Endocrinol. 2009; 304, 97–105.Google Scholar
58. Lv, Z, Li, G, Li, Y, et al. Glucose and lipid homeostasis in adult rat is impaired by early-life exposure to perfluorooctane sulfonate. Environ Toxicol. 2013; 28, 532–542.CrossRefGoogle ScholarPubMed
59. Wan, HT, Zhao, YG, Leung, PY, Wong, CKC. Perinatal exposure to perfluorooctane sulfonate affects glucose metabolism in adult offspring. PLoS One. 2014; 9, 18–20.Google Scholar
60. Suvorov, A, Battista, M-C, Takser, L. Perinatal exposure to low-dose 2,2′,4,4′-tetrabromodiphenyl ether affects growth in rat offspring: what is the role of IGF-1? Toxicology. 2009; 260, 126–131.Google Scholar
61. Slotkin, TA, Brown, KK, Seidler, FJ. Developmental exposure of rats to chlorpyrifos elicits sex-selective hyperlipidemia and hyperinsulinemia in adulthood. Environ Health Perspect. 2005; 113, 1291–1294.Google Scholar
62. Starling, AP, Umbach, DM, Kamel, F, et al. Pesticide use and incident diabetes among wives of farmers in the agricultural health study. Occup Environ Med. 2014; 71, 629–635.Google Scholar
63. La Merrill, M, Karey, E, Moshier, E, et al. Perinatal exposure of mice to the pesticide DDT impairs energy expenditure and metabolism in adult female offspring. PLoS One. 2014; 9, e103337.Google Scholar
64. Armstrong, LE, Driscoll, MV, More, VR, et al. Effects of developmental deltamethrin exposure on white adipose tissue gene expression. J Biochem Mol Toxicol. 2013; 27, 165–171.Google Scholar
65. Araújo, JR, Martel, F, Keating, E. Exposure to non-nutritive sweeteners during pregnancy and lactation: impact in programming of metabolic diseases in the progeny later in life. Reprod Toxicol. 2014; 49, 196–201.Google Scholar
66. Von Poser Toigo, E, Huffell, AP, Mota, CS, et al. Metabolic and feeding behavior alterations provoked by prenatal exposure to aspartame. Appetite. 2015; 87, 168–174.Google Scholar
67. Hectors, TLM, Vanparys, C, van der Ven, K, et al. Environmental pollutants and type 2 diabetes: a review of mechanisms that can disrupt beta cell function. Diabetologia. 2011; 54, 1273–1290.Google Scholar
68. Thompson, LP, Al-Hasan, Y. Impact of oxidative stress in fetal programming. J Pregnancy. 2012; 2012, 582748.Google Scholar
69. Portha, B, Fournier, A, Kioon, MDA, Mezger, V, Movassat, J. Early environmental factors, alteration of epigenetic marks and metabolic disease susceptibility. Biochimie. 2014; 97, 1–15.Google Scholar
70. Elmhiri, G, Hamoudi, D, Dou, S, et al. Antioxidant properties of formula derived maillard reaction products in colon of intrauterine growth restricted pigs. Food Funct. 2016; doi: 10.1039/C5FO01551K.CrossRefGoogle ScholarPubMed
71. Elmhiri, G, Barella, LF, Vieau, D, et al. Acute exposure to a precursor of advanced glycation end products induces a dual effect on the rat pancreatic islet function. Int J Endocrinol. 2014; 2014, 378284.Google Scholar