Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Nutrition during the early life cycle

Dietary determinants of aflatoxin B1-lysine adduct among infants in Nepal

Abstract

Background

Aflatoxins are mycotoxins produced by naturally occurring fungi on food, and aflatoxin B1 (AFB1) is carcinogenic, immunotoxic and hepatotoxic. This study assesses the relationship between AFB1 in Nepali infants at 12 months of age and their diet at 9 and 12 months of age.

Methods

The study used data collected from 1329 infants enrolled in the AflaCohort Study. Aflatoxin exposure was assessed at 12 months using serum AFB1-lysine pg/mg albumin biomarker measured using high performance liquid chromatography-fluorescent detection. Dietary data were collected using food frequency questionnaire. We conducted ordinary least squares and quantile regression analyses with backward elimination to assess lagged (9-month diet and 12-month AFB1) and contemporaneous (12-month diet and 12-month AFB1) associations.

Results

Eighty-one percent of children at 12 months had detectable levels of serum AFB1-lysine (geometric mean: 0.79 pg/mg albumin, 95% CI: 0.74–0.83). The levels ranged from 0.4 to 85 pg/mg albumin. Dietary diversity at 9 and 12 months were not associated with serum AFB1-lysine levels. Consumption of fish and groundnuts at both 9 and 12 months and infant formula and cauliflower at 9 months were associated with higher serum AFB1-lysine while consumption of bananas and mangoes at 12 months were negatively associated with serum AFB1-lysine (p < 0.05).

Conclusions

High prevalence of detectable AFB1-lysine among infants, and possible links to their dietary patterns argues for more urgent research into which foods in children’s diets are most contaminated, and into optimal entry points in the food chain that would allow for effective actions to minimize exposure.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Serum AFB1-lysine levels in serum (pg/mg albumin) for 12-month-old children enrolled in the AflaCohort Study.
Fig. 2: Consumption of food groups among children in the past 24 h.

Similar content being viewed by others

Data availability

Data described in the manuscript, codebook, and analytic code will be made available upon request pending approval. Data will be made publicly and freely available without restriction at https://data.usaid.gov/ once all manuscripts related to the study’s original research questions have been published in peer-reviewed journals.

References

  1. International Agency for Research on Cancer. IARC monographs on the evaluation of carcinogenic risks to humans, vol 56, Chemical agents and related occupations. 2012;100F:1–599.

  2. Anttila A, Bhat RV, Bond JA, Borghoff SJ, Bosch FX, Carlson GP, et al. IARC monographs on the evaluation of carcinogenic risks to humans: some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 2002;82.

  3. Shouman BO, El Morsi D, Shabaan S, Abdel-Hamid AH, Mehrim A. Aflatoxin B1 level in relation to child’s feeding and growth. Indian J Pediatrics. 2012;79:56–61.

    Article  Google Scholar 

  4. Gong YY, Cardwell K, Hounsa A, Egal S, Turner P, Hall A, et al. Dietary aflatoxin exposure and impaired growth in young children from Benin and Togo: cross sectional study. BMJ. 2002;325:20–1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Turner PC, Moore SE, Hall AJ, Prentice AM, Wild CP. Modification of immune function through exposure to dietary aflatoxin in Gambian children. Environ Health Perspect. 2003;111:217–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mahdavi R, Nikniaz L, Arefhosseini SR, Jabbari MV. Determination of Aflatoxin M 1 in breast milk samples in Tabriz–Iran. Matern child health J. 2010;14:141.

    Article  CAS  PubMed  Google Scholar 

  7. Mahfuz M, Alam MA, Fahim SM, Gazi MA, Raihan MJ, Hossain M, et al. Aflatoxin exposure in children living in Mirpur, Dhaka: data from MAL-ED companion study. J Expo Sci Environ Epidemiol. 2018;29:655–62.

  8. Lauer JM, Duggan CP, Ausman LM, Griffiths JK, Webb P, Wang J, et al. Maternal aflatoxin exposure during pregnancy and adverse birth outcomes in Uganda. Matern child Nutr. 2019;15:e12701.

    Article  PubMed  Google Scholar 

  9. Andrews-Trevino JY, Webb P, Shively G, Rogers BL, Baral K, Davis D, et al. Relatively low maternal aflatoxin exposure is associated with small-for-gestational-age but not with other birth outcomes in a prospective birth cohort study of Nepalese infants. J Nutr. 2019;149:1818–25.

  10. Strosnider H, Azziz-Baumgartner E, Banziger M, Bhat RV, Breiman R, Brune M-N, et al. Workgroup report: public health strategies for reducing aflatoxin exposure in developing countries. Environ Health Perspect. 2006;114:1898.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. IARC. IARC monographs on the evaluation of carcinogenic risks to humans, some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. 1993;56.

  12. Iqbal SZ, Asi MR, Hanif U, Zuber M, Jinap S. The presence of aflatoxins and ochratoxin A in rice and rice products; and evaluation of dietary intake. Food Chem. 2016;210:135–40.

    Article  CAS  PubMed  Google Scholar 

  13. Prandini A, Tansini GI, Sigolo S, Filippi LA, Laporta M, Piva GI. On the occurrence of aflatoxin M1 in milk and dairy products. Food Chem Toxicol. 2009;47:984–91.

    Article  CAS  PubMed  Google Scholar 

  14. Akter A, Rahman M, Hasan M. Effects of Aflatoxin B1 on growth and bioaccumulation in common carp fingerling in Bangladesh. Asia-Pacific J Rural Dev. 2010;20:1–14.

    Article  Google Scholar 

  15. Michelin EC, Massocco MM, Godoy SHS, Baldin JC, Yasui GS, Lima CG, et al. Carryover of aflatoxins from feed to lambari fish (Astyanax altiparanae) tissues. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2017;34:265–72.

    CAS  PubMed  Google Scholar 

  16. El-Sayed YS, Khalil RH. Toxicity, biochemical effects and residue of aflatoxin B1 in marine water-reared sea bass (Dicentrarchus labrax L.). Food Chem Toxicol. 2009;47:1606–9.

    Article  CAS  PubMed  Google Scholar 

  17. Wild CP. Aflatoxin exposure in developing countries: the critical interface of agriculture and health. Food Nutr Bull. 2007;28:S372–80.

    Article  PubMed  Google Scholar 

  18. Gong YY, Watson S, Routledge MN. Aflatoxin exposure and associated human health effects, a review of epidemiological studies. Food Saf. 2016;4:14–27.

    Article  Google Scholar 

  19. FAO. Mycotoxins [Internet]. 2015. http://www.fao.org/3/a-y5499e.pdf.

  20. Andrews-Trevino JY, Webb P, Shively G, Rogers B, Baral K, Davis D, et al. Dietary determinants of aflatoxin B 1-lysine adduct in pregnant women consuming a rice-dominated diet in Nepal. Eur J Clin Nutr. 2020;74:732–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Andrews-Trevino J, Webb P, Baral K, Davis D, Shrestha R, Pokharel A, et al. Early life exposure to mycotoxins and child linear growth in Nepal: methods and design of a prospective birth cohort study. J Food Security. 2020;8:1–19.

    Google Scholar 

  22. Scholl PF, Turner PC, Sutcliffe AE, Sylla A, Diallo MS, Friesen MD, et al. Quantitative comparison of aflatoxin B1 serum albumin adducts in humans by isotope dilution mass spectrometry and ELISA. Cancer Epidemiol Biomark Prev. 2006;15:823–6.

    Article  CAS  Google Scholar 

  23. Jin Y, Hein MJ, Deddens JA, Hines CJ. Analysis of lognormally distributed exposure data with repeated measures and values below the limit of detection using SAS. Ann Occup Hyg. 2010;55:97–112.

    PubMed  Google Scholar 

  24. World Health Organization. Indicators for assessing infant and young child feeding practices: part 1: definitions: conclusions of a consensus meeting held 6–8 November 2007 in Washington DC, USA; 2008.

  25. Ministry of Health and Population, New Era, ICF. Nepal Demographic and Health Survey. 2016.

  26. Rutstein SO. Steps to constructing the new DHS Wealth Index. Rockville, MD: ICF International; 2015.

  27. Up to Himalaya. Different season on Nepal [Internet]. 2019. https://uptohimalaya.com/seasons-in-nepal/.

  28. Koenker R. Quantile regression. New York: Cambridge University Press; 2005;

  29. Hocking RR. A Biometrics invited paper. The analysis and selection of variables in linear regression. Biometrics. 1976;32:1–49.

    Article  Google Scholar 

  30. Watson S, Moore SE, Darboe MK, Chen G, Tu YK, Huang YT, et al. Impaired growth in rural Gambian infants exposed to aflatoxin: a prospective cohort study -374 children. BMC Public Health. 2018;18:1–9.

    Article  Google Scholar 

  31. Shirima CP, Kimanya ME, Routledge MN, Srey C, Kinabo JL. A prospective study of growth and biomarkers of exposure to aflatoxin and fumonisin during early childhood in Tanzania. Children’s Health. 2015;123:173–9.

    Google Scholar 

  32. Mitchell NJ, Riley RT, Egner PA, Groopman JD, Wu F. Chronic aflatoxin exposure in children living in Bhaktapur, Nepal: extension of the MAL-ED study. J Exposure Sci Environ Epidemiol. 2017;27:106–11.

    Article  CAS  Google Scholar 

  33. Wu F, Mitchell NJ, Male D, Kensler TW. Reduced foodborne Toxin exposure is a benefit of improving dietary diversity. Toxicological Sci. 2014;141:329–34.

    Article  CAS  Google Scholar 

  34. Smith LE, Mbuya MNN, Prendergast AJ, Turner PC, Ruboko S, Humphrey JH, et al. Determinants of recent aflatoxin exposure among pregnant women in rural Zimbabwe. Mol Nutr Food Res. 2017;61:1–32.

    Article  Google Scholar 

  35. Egner PA, Wang J-B, Zhu Y-R, Zhang B-C, Wu Y, Zhang Q-N, et al. Chlorophyllin intervention reduces aflatoxin–DNA adducts in individuals at high risk for liver cancer. Proc Natl Acad Sci USA. 2001;98:14601–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kensler TW, Egner PA, Wang J-B, Zhu Y-R, Zhang B-C, Lu P-X, et al. Chemoprevention of hepatocellular carcinoma in aflatoxin endemic areas. Gastroenterology. 2004;127:S310–8.

    Article  CAS  PubMed  Google Scholar 

  37. Kensler TW, Roebuck BD, Wogan GN, Groopman JD. Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology. Toxicological Sci. 2010;120:S28–48.

    Article  Google Scholar 

  38. Baydar T, Erkekoglu P, Sipahi H, Sahin G. Aflatoxin B1, M1 and ochratoxin A levels in infant formulae and baby foods marketed in Ankara, Turkey. J Food Drug Anal. 2007;15:89–92.

    CAS  Google Scholar 

  39. Yacine Ware L, Durand N, Nikiema PA, Alter P, Fontana A, Montet D, et al. Occurrence of mycotoxins in commercial infant formulas locally produced in Ouagadougou (Burkina Faso). Food Control. 2017;73:518–23.

    Article  CAS  Google Scholar 

  40. Ismail A, Naeem I, Gong YY, Routledge MN, Akhtar S, Riaz M, et al. Early life exposure to dietary aflatoxins, health impact and control perspectives: a review. Trends Food Sci Technol. 2021;112:212–24.

  41. Ojuri OT, Ezekiel CN, Sulyok M, Ezeokoli OT, Oyedele OA, Ayeni KI, et al. Assessing the mycotoxicological risk from consumption of complementary foods by infants and young children in Nigeria. Food Chem Toxicol. 2018;121:37–50.

    Article  CAS  PubMed  Google Scholar 

  42. FAO. FAO Fishery Country Profile—Nepal [Internet]. 2019. http://www.fao.org/fi/oldsite/FCP/en/npl/profile.htm.

  43. Egal S, Hounsa A, Gong YY, Turner PC, Wild CP, Hall AJ, et al. Dietary exposure to aflatoxin from maize and groundnut in young children from Benin and Togo, West Africa. Int J Food Microbiol. 2005;104:215–24.

    Article  CAS  PubMed  Google Scholar 

  44. Turner PC, Sylla A, Gong YY, Diallo MS, Sutcliffe AE, Hall AJ, et al. Reduction in exposure to carcinogenic aflatoxins by postharvest intervention measures in west Africa: a community-based intervention study. Lancet. 2005;365:1950–6.

    Article  CAS  PubMed  Google Scholar 

  45. Hariprasad P, Durivadivel P, Snigdha M, Venkateswaran G. Natural occurrence of aflatoxin in green leafy vegetables. Food Chem. 2013;138:1908–13.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors express special gratitude to USAID-Nepal Mission, USAID Bureau of Food Security, Dr. Ahmed Kablan, Mr. Debendra Adhikari, Nepalgunj Medical College, District Public Health Office- Banke, Child Health Division, the AflaCohort Study team and the study participants without whom this research would not have been possible.

Funding

Support for this research was provided by the Feed the Future Innovation Lab for Nutrition, which is funded by the United States Agency for International Development (USAID) under grant ID: AID-OAA-L-10-00006 to Tufts University. The opinions expressed herein are solely those of the authors.

Author information

Authors and Affiliations

Authors

Contributions

AL: writing—original draft, formal analysis. PW: conceptualization, methodology, project administration, writing—review and editing. JA-T: writing—review and editing, data curation, project administration. AP: writing—review and editing, formal analysis. SA: data curation, writing—review and editing. RS and DD: writing—review and editing, project administration. KB: conceptualization, project administration. JSW: investigation. KX: investigation, writing—review and editing. KP: conceptualization. SG: conceptualization, methodology, formal analysis, project administration, writing—review and editing.

Corresponding author

Correspondence to Ashish Lamichhane.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lamichhane, A., Webb, P., Andrews-Trevino, J. et al. Dietary determinants of aflatoxin B1-lysine adduct among infants in Nepal. Eur J Clin Nutr 76, 1557–1565 (2022). https://doi.org/10.1038/s41430-022-01142-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41430-022-01142-1

Search

Quick links