Abstract
Objectives
We examined breast milk of mothers and urine of infants before and after introduction of supplementary foods for aflatoxin M1 (AFM1) and the association between AFM1 with maternal and infant diet.
Methods
A prospective cohort study was conducted among mothers and infants ages 0–6 months and 7–12 months from June-October 2014. Sociodemographic, dietary, birth, and health data were collected. A breast milk sample was collected from each mother and a urine sample from each infant at baseline (time point 1) and monthly for 2 time points thereafter; samples collected at baseline and time point 3 were tested for AFM1.
Results
Almost 5% of breast milk and 15.7% of urine samples tested AFM1-positive. The median AFM1 in breast milk was 0.020 ng/mL and in urine 0.077 ng/mg creatinine. At time point 3, infants of 5 of the 6 mothers in each group who were AFM1-positive in breast milk were also AFM1-positive in urine. Mothers’ consumption of cooked maize/maize dough ≥ 3 days per week (OR 2.96, 95% CI = 1.19–7.34) and mothers' consumption of tamales made from maize ≥ 3 days per week (OR 0.28, 95% CI = 0.10–0.73) were significantly associated with AFM1 in infant urine.
Conclusion
This is the first study in Guatemala documenting aflatoxin exposure in both breast milk of lactating mothers and infants´ urine during the first year of life. This may have important implications in understanding the multicausality of the high rates of stunting among children < 5 years old in Guatemala.
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References
Adejumo, O., Atanda, O., Raiola, A., Somorin, Y., Bandyopadhyay, R., & Ritieni, A. (2013). Correlation between aflatoxin M1 content of breast milk, dietary exposure to aflatoxin B1 and socioeconomic status of lactating mothers in Ogun State, Nigeria. Food and Chemical Toxicology, 56, 171–177
Afriyie-Gyawu, E., Ankrah, N. A., Huebner, H. J., Ofosuhene, M., Kumi, J., Johnson, N. M., Tang, L., Xu, L., Jolly, P. E., Ellis, W. O., Ofori-Adjei, D., Williams, J. H., Wang, J. S., & Phillips, T. D. (2008). NovaSil clay intervention in Ghanaians at high risk for aflatoxicosis study design and clinical outcomes. Food additives & contaminants Part A, Chemistry, analysis, control, exposure & risk assessment, 25(1), 76–87. https://doi.org/10.1080/02652030701458105
Black, R. E., Allen, L. H., Bhutta, Z. A., Caulfield, L. E., de Onis, M., Ezzati, M., Mathers, C., Rivera, J., & Maternal and Child Undernutrition Study Group. (2008). Maternal and child undernutrition: global and regional exposures and health consequences. Lancet (London, England), 371(9608), 243–260. https://doi.org/10.1016/S0140-6736(07)61690-0
Brackett, R. E., & Marth, E. H. (1982). Association of aflatoxin M1 with casein. Zeitschrift fur Lebensmittel-Untersuchung und Forschung, 174(6), 439–441
Cantú-Cornelio, F., Aguilar-Toalá, J. E., de León-Rodríguez, C. I., Esparza-Romero, J., Vallejo-Cordoba, B., González-Córdova, A. F., García, H. S., & 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. https://doi.org/10.1016/j.foodcont.2015.10.004
Cardwell, K. F. (2000). Mycotoxin contamination of foods in Africa: Anti-nutritional factors. Food and Nutrition Bulletin, 21(4), 488–492
Doi, A. M., Patterson, P. E., & Gallagher, E. P. (2002). Variability in aflatoxin B(1)-macromolecular binding and relationship to biotransformation enzyme expression in human prenatal and adult liver. Toxicology and applied pharmacology, 181(1), 48–59. https://doi.org/10.1006/taap.2002.9399
Elmore, S.E. (2016). Aflatoxin and Fumonisin Exposure: International Survey and Enterosorption Mitigation Strategy in Humans. Doctoral Dissertation, Texas A&M University.
Food and Nutritional Technical Assistance. (2014, June) Development of Evidence-Based Dietary Recommendations for Children, Pregnant Women, and Lactating Women Living in the Western Highlands in Guatemala. https://www.fantaproject.org/sites/default/files/resources/Guatemala-Optifood-June2014.pdf
Ghiasian, S., & Maghsood, A. (2012). Infants’ exposure to aflatoxin M1 from mother’s breast milk in Iran. Iranian journal of public health, 41(3), 119–126
Gide, S., Warodi, F. A., Alegbe, S. D., & Anas, G. (2019). Exposure assessments of internally displaced infants to aflatoxin M1 through breast milk feeding, in Damaturu Yobe state. Journal of Advances in Microbiology, 14(3), 1–6
Gong, Y. Y., Egal, S., Hounsa, A., Turner, P. C., Hall, A. J., Cardwell, K. F., & Wild, C. P. (2003). Determinants of aflatoxin exposure in young children from benin and togo, West Africa: The critical role of weaning. International Journal of Epidemiology, 32(4), 556–562
Gong, Y., Hounsa, A., Egal, S., Turner, P. C., Sutcliffe, A. E., Hall, A. J., & Wild, C. P. (2004). Postweaning exposure to aflatoxin results in impaired child growth: A longitudinal study in Benin. West Africa. Environmental health perspectives, 112(13), 1334–1338. https://doi.org/10.1289/ehp.6954
Groopman, J. D., & Kensler, T. W. (1993). Molecular biomarkers for human chemical carcinogen exposures. Chemical Research in Toxicology, 6(6), 764–770. https://doi.org/10.1021/tx00036a004
Instituto de Nutrición de Centroamérica y Panamá. (2013). Estudio complementario al análisis secundario de los datos de la Encuesta Nacional de Condiciones de Vida de Guatemala (ENCOVI 2006). http://www.incap.int/index.php/es/publicaciones-incap/119-guatemala-informe-del-estudio-analisis-secundario-de-la-encovi-2006/file.
Ishikawa, A. T., Takabayashi-Yamashita, C. R., Ono, E. Y., Bagatin, A. K., Rigobello, F. F., Kawamura, O., Hirooka, E. Y., & Itano, E. N. (2016). Exposure assessment of infants to aflatoxin M1 through consumption of breast milk and infant powdered milk in Brazil. Toxins, 8(9), 246. https://doi.org/10.3390/toxins8090246
Jiang, Y., Jolly, P. E., Ellis, W. O., Wang, J. S., Phillips, T. D., & Williams, J. H. (2005). Aflatoxin B1 albumin adduct levels and cellular immune status in Ghanaians. International immunology, 17(6), 807–814. https://doi.org/10.1093/intimm/dxh262
Jolly, P. E., Akinyemiju, T. F., Jha, M., Aban, I., Gonzalez-Falero, A., & Joseph, D. (2015). Temporal variation and association of aflatoxin B1 albumin-adduct levels with socio-economic and food consumption Factors in HIV positive adults. Toxins, 7(12), 5129–5140
Jolly, P., Jiang, Y., Ellis, W., Awuah, R., Nnedu, O., Phillips, T., Wang, J. S., Afriyie-Gyawu, E., Tang, L., Person, S., Williams, J., & Jolly, C. (2006). Determinants of aflatoxin levels in Ghanaians: Sociodemographic factors, knowledge of aflatoxin and food handling and consumption practices. International journal of hygiene and environmental health, 209(4), 345–358. https://doi.org/10.1016/j.ijheh.2006.02.002
Kroker-Lobos, M. F., Alvarez, C. S., Rivera-Andrade, A., Smith, J. W., Egner, P., Torres, O., Lazo, M., Freedman, N. D., Guallar, E., Graubard, B. I., McGlynn, K. A., Ramírez-Zea, M., & Groopman, J. D. (2019). Association between aflatoxin-albumin adduct levels and tortilla consumption in Guatemalan adults. Toxicology Reports, 6, 465–471. https://doi.org/10.1016/j.toxrep.2019.05.009
Maki, C. R., Thomas, A. D., Elmore, S. E., Romoser, A. A., Harvey, R. B., Ramirez-Ramirez, H. A., & Phillips, T. D. (2016). Effects of calcium montmorillonite clay and aflatoxin exposure on dry matter intake, milk production, and milk composition. Journal of dairy science, 99(2), 1039–1046. https://doi.org/10.3168/jds.2015-10242
Mendoza, J., Kok, C., Stratton, J., Bianchini, A., & Hallen-Adams, H. (2017). Understanding the mycobiota of maize from the highlands of Guatemala, and implications for maize quality and safety. Crop Protection, 101, 5–11
Orozco, A. (2014). Toxina en maíz afecta a la niñez. Prensa Libre. https://www.prensalibre.com/guatemala/comunitario/toxina-maiz-afecta-ninez-0-1093090719/.
Pan American Health Organization. (2018). Health in the Americas 2017. https://www.paho.org/salud-en-las-americas-2017/
Park, J. W., Kim, E. K., Shon, D. H., & Kim, Y. B. (2002). Natural co-occurrence of aflatoxin B1, fumonisin B1, and ochratoxin A in barley and maize foods from Korea. Food Additives & Contaminants, 19(11), 1073–1080
Sereebutra, P., Solomons, N., Aliyu, M., & Jolly, P. (2006). Sociodemographic and environmental predictors of childhood stunting in rural Guatemala. Nutrition Research, 26(2), 65–70
Shane, S. M. (1994). 23—Economic Issues Associated with Aflatoxins. In D. L. Eaton & J. D. Groopman (Eds.), The Toxicology of Aflatoxins. (pp. 513–527). Elsevier: Academic Press. https://doi.org/10.1016/B978-0-12-228255-3.50028-3
Shuaib, F. M., Jolly, P. E., Ehiri, J. E., Yatich, N., Jiang, Y., Funkhouser, E., Person, S. D., Wilson, C., Ellis, W. O., Wang, J. S., & Williams, J. H. (2010). Association between birth outcomes and aflatoxin B1 biomarker blood levels in pregnant women in Kumasi, Ghana. Tropical medicine & international health TM & IH, 15(2), 160–167. https://doi.org/10.1111/j.1365-3156.2009.02435.x
Torres, O., Matutue, J., Gelineau-van Waes, J., Maddox, J., Gregory, S., Ashley-Koch, A., Showker, J. L., Voss, K. A., & Riley, R. T. (2015). Human health implications from co-exposure to aflatoxins and fumonisins in maize-based foods in Latin America: Guatemala as a case study. World Mycotoxin Journal, 8(2), 143–159
Turner, P. C., Collinson, A. C., Cheung, Y. B., Gong, Y., Hall, A. J., Prentice, A. M., & Wild, C. P. (2007). Aflatoxin exposure in utero causes growth faltering in Gambian infants. International Journal of Epidemiology, 36(5), 1119–1125
Turner, P. C., Moore, S. E., Hall, A. J., Prentice, A. M., & Wild, C. P. (2003). Modification of immune function through exposure to dietary aflatoxin in Gambian children. Environmental health perspectives, 111(2), 217–220. https://doi.org/10.1289/ehp.5753
United States Agency for International Development. (2018). Guatemala Nutrition Profile. https://www.usaid.gov/what-we-do/global-health/nutrition/countries/guatemala-nutrition-profile
Voth-Gaeddert, L. E., Stoker, M., Torres, O., & Oerther, D. B. (2018). Association of aflatoxin exposure and height-for age among young children in Guatemala. International Journal of Environmental Health Research, 28(3), 280–292
Warth, B., Sulyok, M., Fruhmann, P., Mikula, H., Berthiller, F., Schuhmacher, R., Hametner, C., Abia, W. A., Adam, G., Fröhlich, J., & Krska, R. (2012). Development and validation of a rapid multi-biomarker liquid chromatography/tandem mass spectrometry method to assess human exposure to mycotoxins. Rapid communications in mass spectrometry : RCM, 26(13), 1533–1540. https://doi.org/10.1002/rcm.6255
World Health Organization. (2009). WHO child growth standards: Growth velocity based on weight, length and head circumference: Methods and development. World Health Organization. https://apps.who.int/iris/handle/10665/44026
Acknowledgements
We thank the mothers who participated in this study and the clinic staff who helped to facilitate the study. This study was supported by the Minority Health International Research Training (MHIRT), grant no. T37-MD001448, from the National Institute on Minority Health and Health Disparities, National Institutes of Health (NIH), Bethesda, MD, USA.
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The study protocol was reviewed and approved by the Institutional Review Board of the University of Alabama at Birmingham and the Ethics Committee of the Institute of Nutrition for Central America and Panamá, Guatemala. Written informed consent was obtained from each mother.
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Jolly, P.E., Mazariegos, M., Contreras, H. et al. Aflatoxin Exposure Among Mothers and Their Infants from the Western Highlands of Guatemala. Matern Child Health J 25, 1316–1325 (2021). https://doi.org/10.1007/s10995-021-03151-1
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DOI: https://doi.org/10.1007/s10995-021-03151-1