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Occurrence of aflatoxin M1 in human breast milk in Bangladesh

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Abstract

Breast milk is the best, most complete form of nutrition for newborns and infants. However, human milk can contain aflatoxin M1 (AFM1) upon ingestion of dietary mycotoxin contaminants, namely, aflatoxin B1 (AFB1), by lactating mothers. AFB1 and its hydroxylated metabolite AFM1 are potent carcinogens and thus an important issue in food safety and public health. This study is the first to explore the presence of AFM1 in breast milk samples from Bangladesh and assess infant exposure to this toxin, as a consequence of maternal mycotoxin intake. A total of 62 breast milk samples were collected from nursing mothers in Sylhet region of Bangladesh. The milk samples were collected between October 2019 and March 2020 and analyzed by a sensitive enzyme-linked immunosorbent assay. AFM1 was detected in 51.6% of the breast milk samples (colostrum, transitional and mature milk), with a mean concentration of 4.42 ± 0.56 pg/mL, and in the range between LOD (4.0 pg/mL) and 6.66 pg/mL. The frequent detection of AFM1 in breast milk indicates widespread dietary exposure to mycotoxins in our cohort. The estimated average daily intake of AFM1 for all nursed infants was 0.49 ng/kg b.w./day. No significant correlations were observed between AFM1 levels in human milk and food items regularly consumed by nursing women. Overall, AFM1 levels in breast milk samples from the Sylhet region of Bangladesh are moderate, and lower than the permissible levels established for AFM1 in dairy milk or infant formulae (50 and 25 ng/kg, respectively). Yet, this first data for AFM1 breast milk contaminant levels just reflect the recent situation in one cohort, and monitoring should be continued.

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References

  • Afshar P, Shokrzadeh M, Kalhori S, Babaee Z, Saravi SS (2013) Occurrence of ochratoxin A and aflatoxin M1 in human breast milk in Sari, Iran. Food Control 31:525–529

    Article  CAS  Google Scholar 

  • Ali N, Blaszkewicz M, Hossain K, Degen GH (2017) Determination of aflatoxin M1 in urine samples indicates frequent dietary exposure to aflatoxin B1 in the Bangladeshi population. Int J Hyg Environ Health 220:271–281

    Article  CAS  Google Scholar 

  • Ali N, Hossain K, Blaszkewicz M, Rahman M, Mohanto NC, Alim A, Degen GH (2016) Occurrence of aflatoxin M1 in urines from rural and urban adult cohorts in Bangladesh. Arch Toxicol 90:1749–1755

    Article  CAS  Google Scholar 

  • Ali N, Manirujjaman M, Rana S, Degen GH (2020) Determination of aflatoxin M1 and deoxynivalenol biomarkers in infants and children urines from Bangladesh. Arch Toxicol 94:3775–3786

    Article  CAS  Google Scholar 

  • BFSA (2017) Bangladesh Food Safety Authority; Food safety regulations. Available at: http://www.bfsa.gov.bd/sites/default/files/files/bfsa.portal.gov.bd/law/81690675_9a69_483b_8915_1fe8f6b2ddd0/Food-Safety-(Contaminants,-Toxins-and-Harmful-Residues)-Regulations,-2017.pdf

  • Bhuiyan MN, Hassan MT, Begum M, Ahan M, Rahim M (2013) Occurrence and seasonal trends of aflatoxin in rice, maize and wheat in Bangladesh. Int J Sustain Agril Tech 9:8–14

    Google Scholar 

  • Cantú-Cornelio F, Aguilar-Toalá JE, de León-Rodríguez CI, Esparza-Romero J, Vallejo-Cordoba B, González-Córdova AF, García HS, Hernández-Mendoza A (2016) Occurrence and factors associated with the presence of aflatoxin M1 in breast milk samples of nursing mothers in central Mexico. Food Control 62:16–22

    Article  Google Scholar 

  • Cherkani-Hassani A, Mojemmi B, Mouane N (2016) Occurrence and levels of mycotoxins and their metabolites in human breast milk associated to dietary habits and other factors: a systematic literature review, 1984–2015. Trends Food Sci Technol 50:56–69

    Article  CAS  Google Scholar 

  • Codex Alimentarius Commission (2001) Comments submitted on the draft maximum level for aflatoxin M1 in milk, in: Codex Committee on Food Additives and Contaminants 33rd Session, Hague, The Netherlands

  • Cotty PJ, Jaime-Garcia R (2007) Influences of climate on aflatoxin producing fungi and aflatoxin contamination. Int J Food Microbiol 119:109–115

    Article  CAS  Google Scholar 

  • EFSA (2020) CONTAM Panel: Scientific opinion – risk assessment of aflatoxins in food. EFSA J 18(3):6040, 112 pp. https://doi.org/10.2903/j.efsa.2020.6040

  • Elzupir AO, Abas AR, Fadul MH, Modwi AK, Ali NM, Jadian AF, Ahmed NA, Adam SY, Ahmed NA, Khairy AA, Khalil EA (2012) Aflatoxin M1 in breast milk of nursing Sudanese mothers. Mycotoxin Res 28:131–134

    Article  CAS  Google Scholar 

  • European Commission (2006) Commission regulation (EC) no 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. Off J Eur Union 364:5e24

  • FAO/WHO (2018) Food and Agriculture Organization of the United Nations/World Health Organization. Aflatoxins. Safety evaluation of certain contaminants in food: prepared by the 83rd meeting of the Joint FAO/WHO Expert Committee on Food Additives (JECFA). WHO Additives Series No 74:2–280. Available at: https://apps.who.int/iris/bitstream/handle/10665/276868/9789241660747-eng.pdf?ua=1

  • Galvano F, Pietri A, Bertuzzi T, Gagliardi L, Ciotti S, Luisi S, Bognanno M, La Fauci L, Iacopino AM, Nigro F, Li Volti G, Vanella L, Giammanco G, Tina GL, Gazzolo D (2008) Maternal dietary habits and mycotoxin occurrence in human mature milk. Mol Nutr Food Res 52:496–501

    Article  CAS  Google Scholar 

  • Giovati L, Magliani W, Ciociola T, Santinoli C, Conti S, Polonelli L (2015) AFM1 in milk: physical, biological, and prophylactic methods to mitigate contamination. Toxins 7:4330–4349

    Article  CAS  Google Scholar 

  • Gong Y, Hounsa A, Egal S, Turner PC, Sutcliffe AE, Hall AJ, Cardwell K, Wild CP (2004) Postweaning exposure to aflatoxin results in impaired child growth: a longitudinal study in Benin, West Africa. Environ Health Perspect 112:1334–1338

    Article  CAS  Google Scholar 

  • Groopman JD, Egner PA, Schulze KJ, Wu LS, Merrill R, Mehra S, Shamim AA, Ali H, Shaikh S, Gernand A, Khatry SK, LeClerq SC, West KP, Christian P (2014) Aflatoxin exposure during the first 1000 days of life in rural South Asia assessed by aflatoxin B1-lysine albumin biomarkers. Food Chem Toxicol 74:184–189

  • IARC (2015) Working Group Report No. 9, Mycotoxin control in low- and middle income countries (Wild CP, Miller JD, Groopman JD, eds). Available at: https://publications.iarc.fr/Book-And-Report-Series/Iarc-Working-Group-Reports/Mycotoxin-Control-In-Low--And-Middle-income-Countries-2015

  • IARC (2012) International Agency for Research on Cancer. Aflatoxins. Chemical agents and related occupations. IARC Monogr Eval Carcinog Risk Chem Hum 100F:225–248. IARC Press, Lyon, France

  • Islam GMR, Hoque MM (2013) Food safety regulation in Bangladesh, chemical hazard and some perception to overcome the dilemma. Int Food Res J 20:47

    CAS  Google Scholar 

  • Kensler TW, Roebuck BD, Wogan GN, Groopman JD (2011) Aflatoxin: a 50-year odyssey of mechanistic and translational toxicology. Toxicol Sci 120:S28–S48

    Article  CAS  Google Scholar 

  • Kent JC, Mitoulas LR, Cregan MD, Ramsay DT, Doherty DA, Hartmann PE (2006) Volume and frequency of breastfeedings and fat content of breast milk throughout the day. Pediatrics 117:e387–e395

    Article  Google Scholar 

  • Liu Y, Wu F (2010) Global burden of aflatoxin-induced hepatocellular carcinoma: a risk assessment. Environ Health Perspect 118:818–824

    Article  CAS  Google Scholar 

  • Lombard MJ (2014) Mycotoxin exposure and infant and young child growth in Africa: what do we know? Ann Nutr Metab 64:42–52

    Article  CAS  Google Scholar 

  • Mahfuz M, Alam MA, Fahim SM, Gazi MA, Raihan MJ, Hossain M, Egner PA, Bessong PO, Petri WA, Groopman JD, Ahmed T (2019) Aflatoxin exposure in children living in Mirpur, Dhaka: data from MAL-ED companion study. J Expo Sci Environ Epidemiol 29:655–662

    Article  CAS  Google Scholar 

  • Marchese S, Polo A, Ariano A, Velotto S, Costantini S, Severino L (2018) Aflatoxin B1 and M1: biological properties and their involvement in cancer development. Toxins 10:214

    Article  Google Scholar 

  • Mehta RV, Wenndt AJ, Girard AW, Taneja S, Ranjan S, Ramakrishnan U, Martorell R, Ryan PB, Rangiah K, Young MF (2021) Risk of dietary and breastmilk exposure to mycotoxins among lactating women and infants 2-4 months in northern India. Matern Child Nutr 17(2):e13100

  • Partanen HA, El-Nezami HS, Leppänen JM, Myllynen PK, Woodhouse HJ, Vähäkangas KH (2010) Aflatoxin B1 transfer and metabolism in human placenta. Toxicol Sci 113:216–225

    Article  CAS  Google Scholar 

  • Polychronaki N, Turner PC, Mykkänen H, Gong Y, Amra H, Abdel-Wahhab M, El-Nezami H (2006) Determinants of aflatoxin M1 in breast milk in a selected group of Egyptian mothers. Food Addit Contam 23:700–708

    Article  CAS  Google Scholar 

  • Radonić JR, Kocić Tanackov SD, Mihajlović IJ, Grujić ZS, Vojinović Miloradov MB, Škrinjar MM, Turk Sekulić MM (2017) Occurrence of aflatoxin M1 in human milk samples in Vojvodina, Serbia: estimation of average daily intake by babies. J Environ Sci Health B 52:59–63

    Article  Google Scholar 

  • Roy M, Harris J, Afreen S, Deak E, Gade L, Balajee SA, Park B, Chiller T, Luby S (2013) Aflatoxin contamination in food commodities in Bangladesh. Food Addit Contam Part B Surveill 6:17–23

    Article  CAS  Google Scholar 

  • Rushing BR, Selim MI (2019) Aflatoxin B1: A review on metabolism, toxicity, occurrence in food, occupational exposure, and detoxification methods. Food Chem Toxicol 124:81–100

    Article  CAS  Google Scholar 

  • Saha Turna N, Wu F (2019) Risk assessment of aflatoxin-related liver cancer in Bangladesh. Food Addit Contam Part A 36:320–326

    Article  CAS  Google Scholar 

  • Sengling Cebin Coppa CF, Khaneghah AM, Alvito P, Assunção R, Martins C, Eş I, Gonçalves BL, de Neeff DV, Sant’Ana AS, Corassin CH, Oliveira CA (2019) The occurrence of mycotoxins in breast milk, fruit products and cereal-based infant formula: a review. Trends Food Sci Technol 92:81–93

    Article  CAS  Google Scholar 

  • Sherif SO, Salama EE, Abdel-Wahhab MA (2009) Mycotoxins and child health: the need for health risk assessment. Int J Hyg Environ Health 212:347–368

    Article  CAS  Google Scholar 

  • Smith LE, Prendergast AJ, Turner PC, Humphrey JH, Stoltzfus RJ (2017) Aflatoxin exposure during pregnancy, maternal anemia, and adverse birth outcomes. Am J Trop Med Hyg 96:770–776

    Article  CAS  Google Scholar 

  • Tarannum N, Nipa MN, Das S, Parveen S (2020) Aflatoxin M1 detection by ELISA in raw and processed milk in Bangladesh. Toxicol Rep 7:1339–1343

    Article  CAS  Google Scholar 

  • Turner PC (2013) The molecular epidemiology of chronic aflatoxin driven impaired child growth. Scientifica (Cairo) 2013:152879

  • Turner PC, Flannery B, Isitt C, Ali M, Pestka J (2012) The role of biomarkers in evaluating human health concerns from fungal contaminants in food. Nutr Res Rev 25:162–79

    Article  CAS  Google Scholar 

  • van Egmond HP, Schothorst RC, Jonker MA (2007) Regulations relating to mycotoxins in food. Anal Bioanal Chem 389:147–157

    Article  CAS  Google Scholar 

  • Wael F, El-Kady NN, Tayel AA (2011) Infants exposure to aflatoxin M1 as a novel foodborne zoonosis. Food Chem Toxicol 49:2816–2819

    Article  Google Scholar 

  • Warth B, Braun D, Ezekiel CN, Turner PC, Degen GH, Marko D (2016) Biomonitoring of mycotoxins in human breast milk: current state and future perspectives. Chem Res Toxicol 29:1087–1097

    Article  CAS  Google Scholar 

  • WHO (2002) World Health Organization. Nutrient adequacy of exclusive breastfeeding for the term infant during the first six months of life. http://apps.who.int/iris/bitstream/10665/42519/1/9241562110.pdf. Accessed 19 June 2015

  • Wild CP, Turner PC (2002) The toxicology of aflatoxins as a basis for public health decisions. Mutagenesis 17:471–481

    Article  CAS  Google Scholar 

  • Zarba A, Wild CP, Hall AJ, Montesano R, Hudson GJ, Groopman JD (1992) Aflatoxin M1 in human breast milk from The Gambia, west Africa, quantified by combined monoclonal antibody immunoaffinity chromatography and HPLC. Carcinogenesis 13:891–894

    Article  CAS  Google Scholar 

  • Zhu JQ, Zhang LS, Hu X, Xiao Y, Chen JS, Xu YC, Fremy J, Chu FS (1987) Correlation of dietary aflatoxin B1 levels with excretion of aflatoxin M1 in human urine. Cancer Res 47:1848–1852

    CAS  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to all volunteers for participating in this study. This study was supported with a small funding as internal.

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Correspondence to Nurshad Ali.

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Islam, F., Das Trisha, A., Hafsa, J.M. et al. Occurrence of aflatoxin M1 in human breast milk in Bangladesh. Mycotoxin Res 37, 241–248 (2021). https://doi.org/10.1007/s12550-021-00436-w

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