Skip to main content

Advertisement

SpringerLink
Log in

The association between bisphenol A exposure and type-2 diabetes: a world systematic review

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The present study was conducted to systematically review, analyze, and interpret all the relevant evidence in the literature on the possible link between exposure to bisphenol A (BPA) and the risk of type-2 diabetes mellitus (T2DM). We developed a comprehensive search strategy and used it to search Web of Science, Scopus, PubMed, and Google Scholar up to March 31, 2016, producing 3108 hits, of which 13 original papers were included. Findings of these studies were quite controversial; few studies indicated a significant positive association between BPA exposure and T2DM, while some other failed to detect such a relationship. Overall, it can be suggested that chance is unlikely the plausible explanation for the observed association between BPA exposure and T2DM. This was mainly because even in the negative studies some clues could be found in favor of a statistically significant relationship between BPA and T2DM. Additionally, some of the studies had shortcomings in defining the exposure and outcome measures, which, if present, might have led to underestimating the relationship between BPA exposure and T2DM. The theoretical plausibility of such a relationship found earlier in animal studies also supports this point. However, more definitive answer requires the conduct of future longitudinal studies, in which the possible association between BPA exposure and T2DM is assessed over much longer periods of time with more temporally robust BPA measurements. In addition, it would be quite beneficial if future studies be conducted in areas where data is still lacking (e.g., South America, Australia/Oceania, and Europe).

ᅟ

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aekplakorn W, Chailurkit LO, Ongphiphadhanakul B (2015) Relationship of serum bisphenol A with diabetes in the Thai population, National Health Examination Survey IV, 2009. J Diabetes 7:240

    Article  CAS  Google Scholar 

  • Ahmadkhaniha R et al. (2014) Association of urinary bisphenol A concentration with type-2 diabetes mellitus. J Environ Health Sci Eng 12:64

    Article  Google Scholar 

  • Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A (2006) The estrogenic effect of bisphenol A disrupts pancreatic β-cell function in vivo and induces insulin resistance. Environ Health Perspect 114:106

    Article  CAS  Google Scholar 

  • Alonso-Magdalena P, Vieira E, Soriano S, Menes L, Burks D, Quesada I, Nadal A (2010) Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect 118:1243

    Article  CAS  Google Scholar 

  • Alonso-Magdalena P et al. (2008) Pancreatic insulin content regulation by the estrogen receptor ERα. PLoS One 3:e2069

    Article  Google Scholar 

  • Andra SS, Kalyvas H, Andrianou XD, Charisiadis P, Christophi CA, Makris KC (2015) Preliminary evidence of the association between monochlorinated bisphenol A exposure and type II diabetes mellitus: a pilot study. J Environ Sci Health A Tox Hazard Subst Environ Eng 50:243–259. doi:10.1080/10934529.2015.981111

    Article  CAS  Google Scholar 

  • Arenholt-Bindslev D, Breinholt V, Preiss A, Schmalz G (1999) Time-related bisphenol-A content and estrogenic activity in saliva samples collected in relation to placement of fissure sealants. Clin Oral Invest 3:120–125

    Article  CAS  Google Scholar 

  • Barker DJ (1998) In utero programming of chronic disease. Clin Sci 95:115–128

    Article  CAS  Google Scholar 

  • Barker DJ, Eriksson JG, Forsen T, Osmond C (2002) Fetal origins of adult disease: strength of effects and biological basis. Int J Epidemiol 31:1235–1239

    Article  CAS  Google Scholar 

  • Ben-Jonathan N, Hugo ER, Brandebourg TD (2009) Effects of bisphenol A on adipokine release from human adipose tissue: implications for the metabolic syndrome. Mol Cell Endocrinol 304:49–54

    Article  CAS  Google Scholar 

  • Braun JM et al. (2011) Variability and predictors of urinary bisphenol A concentrations during pregnancy. Environ Health Perspect 119:131

    Article  CAS  Google Scholar 

  • Burridge E (2003) Bisphenol A: product profile. Eur Chem News 78:17

    Google Scholar 

  • Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, Needham LL (2005) Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113:391

    Article  CAS  Google Scholar 

  • Calafat AM, Ye X, Wong L-Y, Reidy JA, Needham LL (2008) Exposure of the US population to bisphenol A and 4-tertiary-octylphenol: 2003–2004. Environ Health Perspect 116:39

    Article  CAS  Google Scholar 

  • Casey MF, Neidell M (2013) Disconcordance in statistical models of bisphenol a and chronic disease outcomes in NHANES 2003-08. PLoS One 8(11):e79944

  • Dekant W, Völkel W (2008) Human exposure to bisphenol A by biomonitoring: methods, results and assessment of environmental exposures. Toxicol Appl Pharmacol 228:114–134

    Article  CAS  Google Scholar 

  • Howe SR, Borodinsky L, Lyon RS (1998) Potential exposure to bisphenol A from food-contact use of epoxy coated cans. J Coat Tech 70:69–74

    Article  CAS  Google Scholar 

  • Hugo ER, Brandebourg TD, Woo JG, Loftus J, Alexander JW, Ben-Jonathan N (2008) Bisphenol A at environmentally relevant doses inhibits adiponectin release from human adipose tissue explants and adipocytes. Environ Health Perspect 116:1642–1647

    Article  CAS  Google Scholar 

  • Khan KS, Kunz R, Kleijen J, Antes G (2003) Systematic reviews to support evidence-based medicine: how to write and apply findings of healthcare research. Royal Society of Medicine Press, London

    Google Scholar 

  • Kim K, Park H (2013) Association between urinary concentrations of bisphenol A and type 2 diabetes in Korean adults: a population-based cross-sectional study. Int J Hygiene Environ Health 216:467–471

    Article  CAS  Google Scholar 

  • Kuo C-C, Moon K, Thayer KA, Navas-Acien A (2013) Environmental chemicals and type 2 diabetes: an updated systematic review of the epidemiologic evidence. Curr Diab Rep 13:831–849. doi:10.1007/s11892-013-0432-6

    Article  CAS  Google Scholar 

  • LaKind JS, Goodman M, Mattison DR (2014) Bisphenol A and indicators of obesity, glucose metabolism/type 2 diabetes and cardiovascular disease: a systematic review of epidemiologic research. Crit Rev Toxicol 44:121–150. doi:10.3109/10408444.2013.860075

    Article  CAS  Google Scholar 

  • LaKind JS, Goodman M, Naiman DQ (2012) Use of NHANES data to link chemical exposures to chronic diseases: a cautionary tale. PLoS One 7:e51086

    Article  CAS  Google Scholar 

  • Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, Wallace RB, Melzer D (2008) Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300:1303–1310

    Article  CAS  Google Scholar 

  • Livingstone C, Collison M (2002) Sex steroids and insulin resistance. Clin Sci 102:151–166

    Article  CAS  Google Scholar 

  • Loganathan SN, Kannan K (2011) Occurrence of bisphenol A in indoor dust from two locations in the eastern United States and implications for human exposures. Arch Environ Contam Toxicol 61:68–73

    Article  CAS  Google Scholar 

  • Louet J-F, LeMay C, Mauvais-Jarvis F (2004) Antidiabetic actions of estrogen: insight from human and genetic mouse models. Curr Atheroscleros Rep 6:180–185

    Article  Google Scholar 

  • Melzer D, Rice NE, Lewis C, Henley WE, Galloway TS (2010) Association of urinary bisphenol A concentration with heart disease: evidence from NHANES 2003/06. PLoS One 5:e8673

    Article  Google Scholar 

  • Nadal A, Alonso-Magdalena P, Soriano S, Quesada I, Ropero AB (2009a) The pancreatic β-cell as a target of estrogens and xenoestrogens: implications for blood glucose homeostasis and diabetes. Mol Cell Endocrinol 304:63–68

    Article  CAS  Google Scholar 

  • Nadal A, Alonso-Magdalena P, Soriano S, Ropero AB, Quesada I (2009b) The role of oestrogens in the adaptation of islets to insulin resistance. J Physiol 587:5031–5037

    Article  CAS  Google Scholar 

  • Ning G et al. (2011) Relationship of urinary bisphenol A concentration to risk for prevalent type 2 diabetes in Chinese adults: a cross-sectional analysis. Ann Intern Med 155:368–374

    Article  Google Scholar 

  • Rancière F, Lyons JG, Loh VHY, Botton J, Galloway T, Wang T, Shaw JE, Magliano DJ (2015) Bisphenol A and the risk of cardiometabolic disorders: a systematic review with meta-analysis of the epidemiological evidence. Environ Health 14:46

    Article  Google Scholar 

  • Ropero AB, Alonso-Magdalena P, Quesada I, Nadal A (2008) The role of estrogen receptors in the control of energy and glucose homeostasis. Steroids 73:874–879

    Article  CAS  Google Scholar 

  • Sabanayagam C, Teppala S, Shankar A (2013) Relationship between urinary bisphenol A levels and prediabetes among subjects free of diabetes. Acta Diabetol 50:625–631. doi:10.1007/s00592-013-0472-z

    Article  CAS  Google Scholar 

  • Sajiki J, Yonekubo J (2003) Leaching of bisphenol A (BPA) to seawater from polycarbonate plastic and its degradation by reactive oxygen species. Chemosphere 51:55–62

    Article  CAS  Google Scholar 

  • Shankar A, Teppala S (2011) Relationship between urinary bisphenol A levels and diabetes mellitus. The J Clin Endocrinol Metabol 96:3822–3826

    Article  CAS  Google Scholar 

  • Silver MK, O’Neill MS, Sowers MR, Park SK (2011) Urinary bisphenol A and type-2 diabetes in US adults: data from NHANES 2003-2008. PLoS One 6:e26868

    Article  CAS  Google Scholar 

  • Song Y, Chou EL, Baecker A, You NCY, Song Y, Sun Q, Liu S (2015) Endocrine-disrupting chemicals, risk of type 2 diabetes, and diabetes-related metabolic traits: a systematic review and meta-analysis. J Diabet. doi:10.1111/1753-0407.12325

    Google Scholar 

  • Sowlat MH, Abdollahi M, Gharibi H, Yunesian M, Rastkari N (2014) Removal of vapor-phase elemental mercury from stack emissions with sulfur-impregnated activated carbon. In: Rev Environ Contam Toxicol volume. Springer, pp 1–34

  • Sun Q et al. (2014) Association of urinary concentrations of bisphenol A and phthalate metabolites with risk of type 2 diabetes: a prospective investigation in the nurses’ health study (NHS) and NHSII cohorts. Environ Health Perspect 122:616–623

    Article  Google Scholar 

  • Sutton AJ, Abrams KR, Jones DR, Sheldon TA, Song F (2000) Methods for meta-analysis in medical research. J. Wiley,

  • Tang W-y, Ho S-m (2007) Epigenetic reprogramming and imprinting in origins of disease. Rev Endocr Metabol Disord 8:173–182

    Article  Google Scholar 

  • Trujillo M, Scherer P (2005) Adiponectin–journey from an adipocyte secretory protein to biomarker of the metabolic syndrome. J Intern Med 257:167–175

    Article  CAS  Google Scholar 

  • Tsai W-T (2006) Human health risk on environmental exposure to bisphenol-A: a review. J Environ Sci Health C 24:225–255

    Article  CAS  Google Scholar 

  • Tu Y-K, Greenwood DC (2012) Modern methods for epidemiology. Springer

  • Vandenberg L, Chahoud I, Heindel JJ, Padmanabhan V, Paumgartten FJ, Schoenfelder G (2010) Urinary, circulating, and tissue biomonitoring studies indicate widespread exposure to bisphenol A. Environ Health Perspect 118:1055–1070

    Article  CAS  Google Scholar 

  • Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24:139–177

    Article  CAS  Google Scholar 

  • Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM (2009) Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr Rev 30:75–95

    Article  CAS  Google Scholar 

  • Whitehead J, Richards A, Hickman I, Macdonald G, Prins J (2006) Adiponectin—a key adipokine in the metabolic syndrome. Diab Obes Metabol 8:264–280

    Article  CAS  Google Scholar 

  • Ye X, Wong L-Y, Bishop AM, Calafat AM (2011) Variability of urinary concentrations of bisphenol A in spot samples, first morning voids, and 24-h collections. Environ Health Perspect 119:983

    Article  CAS  Google Scholar 

Download references

Acknowledgment

The present study was financially supported by the Institute for Environmental Research (IER), Tehran University of Medical Sciences (TUMS).

Author information

Authors and Affiliations

  1. Center for Air Pollution research (CAPR), Institute for Environmental Research (IER), Tehran University of Medical Sciences, Tehran, Iran

    Mohammad H. Sowlat, Masud Yunesian & Noushin Rastkari

  2. Department of Environment and Energy, Science and Research Branch, Islamic Azad University, Tehran, Iran

    Saeedeh Lotfi

  3. Department of Environmental Health Engineering, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

    Masud Yunesian

  4. Department of Human Ecology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

    Reza Ahmadkhaniha

Authors
  1. Mohammad H. Sowlat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saeedeh Lotfi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Masud Yunesian
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Reza Ahmadkhaniha
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Noushin Rastkari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Noushin Rastkari.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sowlat, M.H., Lotfi, S., Yunesian, M. et al. The association between bisphenol A exposure and type-2 diabetes: a world systematic review. Environ Sci Pollut Res 23, 21125–21140 (2016). https://doi.org/10.1007/s11356-016-7525-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7525-0

Keywords

Search

Navigation