Abstract
In the present study, a total of 112 raw milk samples were collected between October and December of 2018 from dairy farming households in Malawi and analyzed for aflatoxin M1 (AFM1) using VICAM aflatest fluorometry procedure. These data together with the consumption data obtained through a milk consumption frequency questionnaire were used for the calculation of AFM1 exposure and its association with hepatocarcinoma (HCC) risk in dairy farming population. Average daily milk intake by children and adults were approximately 300 ± 0.07 and 541.7 ± 0.14 mL, respectively. All raw milk samples tested positive to AFM1 averaging 0.551 μg/L. Probable mean daily exposure to AFM1 for adults was 4.98 ± 7.25 ng/kg BW/day almost half that of children (8.28 ± 11.82 ng/kg BW/day). Estimated risk of AFM1-induced HCC associated with consumption of milk among children and adults were 0.038 and 0.023 cases per 100,000 individuals per year, respectively. Although the results of this investigation suggest a low risk of HCC, other negative health effects of AFM1 justify its continuous monitoring and update of the risk assessment. This work presents the first insight in the occurrence of AFM1 in cow milk in Malawi as well as associated AFM1 exposure in dairy farming population.
Similar content being viewed by others
Abbreviations
- HCC:
-
Hepatocellular carcinoma
- AFM1 :
-
Aflatoxin M1
- AFB1 :
-
Aflatoxin B1
- BW:
-
Body weight
- AEZ:
-
Agroecological zone
- HBV:
-
Hepatitis B virus
- FAO:
-
Food and Agriculture Organization
- WHO:
-
World Health Organization
- JECFA:
-
Joint FAO/WHO Expert Committee on Food Additives
- HBsAg+:
-
hepatitis B surface antigen–positive
- HBsAg:
-
hepatitis B surface antigen–negative
- ALARA:
-
as low as reasonably achievable levels
- USAID:
-
United State Agency for International Development
- BHEARD:
-
Borlaug Higher Education for Agricultural Research and Development
- EFSA:
-
European Food Safety Authority
- CEC:
-
Commission of the European Communities
- EC:
-
European Commission
- FDA:
-
US Food and Drug Administration
References
Ahlberg S, Grace D, Kiarie G, Kirino Y, Lindahl J (2018) A risk assessment of aflatoxin M1 exposure in low and mid-income dairy consumers in Kenya. Toxins 10(9):348. https://doi.org/10.3390/toxins10090348
Alonso VA, Monge MP, Larriestra A, Dalcero AM, Cavaglieri LR, Chiacchiera SM (2010) Naturally occurring aflatoxin M1 in raw bulk milk from farm cooling tanks in Argentina. Food Addit Contam: Part A 27:373–379
Awasthi V, Bahman S, Thakur LK, Singh SK, Dua A, Ganguly S (2012) Contaminants in milk and impact of heating: an assessment study. Indian J Public Health 56:96–99
Bilandzic N, Varenina I, Solomun B (2010) Aflatoxin M1 in raw milk in Croatia. Food Control 21:1279–1281
Cano-Sancho G, Marin S, Ramos AJ, Peris-Vicent J, Sanchis V (2010) Occurrence of aflatoxin M1 and exposure assessment in Catalonia (Spain). Rev Iberoam Micol 27:130–135
CEC - Commission of the European Communities (2010) EC Regulation 165/2010. 26.02.2010. Bruxelles: Official Journal of the EC L50/8–12. Available from: https://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2010:050:0008:0012:EN:PDF
Covic N, Hendriks SL (2016) Achieving a nutrition revolution for Africa: the road to healthier diets and optimal nutrition. International Food Policy Research Institute (IFPRI), Washington, DC. https://images.agri-profocus.nl/upload/170629_NamukoloCovic_A-nutrition-revolution-for-Africa1500555365.pdf. Accessed 30 June 2020
Cullen JM, Ruebner BH, Hsieh LS, Hyde DM, Hsieh DP (1987) Carcinogenicity of dietary aflatoxin M1 in male Fischer rats compared to aflatoxin B1. Cancer Res 47:1913–1917
Driehuis F, Spanjer MC, Scholten JM, te Giffel MC (2008) Occurrence of mycotoxins in feedstuffs of dairy cows and estimation of total dietary intakes. J Dairy Sci 91:4261–4271
Duarte SC, Almeida AM, Teixeira AS, Pereira AL, Falcão AC, Pena A, Lino CM (2013) Aflatoxin M1 in marketed milk in Portugal: assessment of human and animal exposure. Food Control 30:411–417
EC – 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 L 364:5–24 Last consolidated version available from: https://eurlex.europa.eu/legal-content/DE/AUTO/?uri=CELEX:02006R1881-20180319
EFSA - European Food Safety Authority (2004) Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to aflatoxin B1 as undesirable substance in animal feed. EFSA J 39:1–27. Available from: https://doi.org/10.2903/j.efsa.2004.39
EFSA - European Food Safety Authority (2020) Panel on contaminants in the food chain (CONTAM), risk assessment of aflatoxins in food. EFSA J 18(3):e06040. https://doi.org/10.2903/j.efsa.2020.6040
Ezekiel CN, Sulyok M, Warth B, Odebode AC, Krska R (2012) Natural occurrence of mycotoxins in peanut cake from Nigeria. Food Control 27:338–342
FAO - Food and Agriculture Organization of the United Nations (2004) Worldwide regulations for mycotoxins in food and feed in 2003. Food nutrition, 81. FAO. Available from: http://www.fao.org/3/y5499e/y5499e00.htm
FDA – US Food and Drug Administration (2005) Compliance Policy Guides Sec. 527.400 Whole milk, low fat milk, skim milk-aflatoxin M (CPG 7106.10). Washington, DC: FDA Compliance Policy Guides, 219. Available from: https://www.fda.gov/regulatory-information/search-fda-guidance-documents/cpg-sec-527400-whole-milk-lowfat-milk-skim-milk-aflatoxin-m1
Flores-Flores ME, Lizarraga E, López de Cerain A, González-Peñas E (2015) Presence of mycotoxins in animal milk: a review. Food Control 53:163–176
Hussein HS, Brasel JM (2001) Toxicity, metabolism, and impact of mycotoxins on humans and animals. Toxicology 167:101–134
IARC - International Agency for Research on Cancer (2012) Aflatoxins. In: Chemical agents and related occupations, Vol. 100F: a review of human carcinogens, pp. 225–248. Available from: https://monographs.iarc.fr/ENG/Monographs/vol100F/mono100F.pdf
IFS - Integrated Farming Systems Project (2013) Baseline survey report. Department of Agriculture Research Services, Malawi
JECFA - Joint FAO/WHO Expert Committee on Food Additives (2001) Safety evaluation of certain mycotoxins in food (WHO food additives series no. 47), 56th meeting of the joint FAO/WHO expert committee on food additives (JECFA), Geneva, international Programme on chemical safety, World Health Organization Available from: http://www.fao.org/3/a-bc528e.pdf
JECFA - Joint FAO/WHO Expert Committee on Food Additives (1999) Evaluation of certain food additives and contaminants (forty-ninth report of the joint FAO/WHO expert committee on food additives). In FAO/WHO expert committee on food additives; FAO/WHO: Geneva, Switzerland. Available from: https://apps.who.int/iris/handle/10665/42142
JECFA - Joint FAO/WHO Expert Committee on Food Additives (2017) Evaluation of certain contaminants in food: eighty-third report of the joint FAO/WHO expert committee on food additives. World Health Organization Available from: https://apps.who.int/iris/handle/10665/254893
Kang’ethe EK, Lang’a KA (2009) Aflatoxin B1 and M1 contamination of animal feeds and milk from urban centers in Kenya. Afr Health Sci 9:218–226
Kirino Y, Makita K, Grace D, Lindahl J (2016) Survey of informal milk retailers in Nairobi, Kenya and prevalence of aflatoxin M1 in marketed milk. Afr J Food Agric Nutr Dev 16:11022–11038
Kuboka MM, Imungi JK, Njue L, Mutua F, Grace D, Lindahl JF (2019) Occurrence of aflatoxin M1 in raw milk traded in peri-urban Nairobi, and the effect of boiling and fermentation. Infect Ecol Epidemiol 9(1):1625703. https://doi.org/10.1080/20008686.2019.1625703
Li H, Xing L, Zhang M, Wang J, Zheng N (2018) The toxic effects of aflatoxin B1 and aflatoxin M1 on kidney through regulating L-Proline and downstream apoptosis. Hindawi BioMed Res 2018:1–11. https://doi.org/10.1155/2018/9074861
Lu PX, Wang JB, Zhang QN, Wu Y, Sun Y, Chen TY (2010) Longitudinal study of aflatoxin exposure in the development of primary liver cancer in patients with chronic hepatitis. Zhonghua Yi Xue Za Zhi 90:1665–1669
Maleta K, Virtanen S, Espo M, Kulmala T, Ashorn P (2003) Timing of growth faltering in rural Malawi. Arch Dis Child 88:574–578
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 10:1–19
Matumba L, Monjerezi M, Van Poucke C, Biswick T, Mwatseteza J, De Saeger S (2013) Evaluation of the bright greenish yellow fluorescence test as a screening technique for aflatoxin-contaminated maize in Malawi. World Mycotoxin J 6:367–373
Matumba L, Sulyok M, Monjerezi M, Biswick T, Krska R (2014) Fungal metabolites diversity in maize and associated human dietary exposures relate to micro-climatic patterns in Malawi. World Mycotoxin J 8:269–282
Matumba L, Kimanya M, Chunga-Sambo W, Munthali M, Ayalew A (2019) Probabilistic dietary based estimation of the burden of aflatoxin-induced hepatocellular carcinoma among adult Malawians. World Mycotoxin J 12:409–419
MBS - Malawi Bureau of Standards (2008) Contaminants and toxins in foods – General standards. MS 302, ICS 67.020. Blantyre, Malawi
Meucci V, Razzuoli E, Soldani G, Massart F (2010) Mycotoxin detection in infant formula milks in Italy. Food Addit Contam 27:64–71
Neal GE, Eaton DL, Judah DJ, Verma A (1998) Metabolism and toxicity of aflatoxins M1 and B1 in human-derived in vitro systems. Toxicol Appl Pharmacol 151:152–158
Neuveut C, Wei Y, Buendia MA (2010) Mechanisms of HBV-related hepatocarcinogenesis. J Hepatol 52:594–604
Njombwa CA (2019) Occurrence of aflatoxin and zearalenone in concentrate feeds and milk contamination with aflatoxin M1 and bacterial pathogens in Malawi. Louisiana State University, Dissertation
Nkosi MM, Andy SC, Mtegha C (2019) Prevalence and contamination levels of aflatoxins in dairy cattle feeds from five milk bulking groups in Malawi. Afr J Rural Dev 3:883–894
NSO - National Statistical Office [Malawi] and ICF (2017) Malawi demographic and health survey 2015–16. Zomba, Malawi, and Rockville, Maryland, USA: NSO and ICF https://dhsprogram.com/pubs/pdf/FR319/FR319.pdf. Accessed 25 June 2020
Peng K, Chen C (2009) Prevalence of aflatoxin M1 in Milk and its potential liver cancer risk in Taiwan. J Food Prot 72:1025–1029
Reddy KR, Salleh B, Saad B, Abbas HK, Abel CA, Shier WT (2010) An overview of mycotoxin contamination in foods and its implications for human health. Toxin Rev 29:3–26
Sadler K, Catley A (2009) Milk matters: improving health and nutritional status of children in pastoralist communities. https://www.ennonline.net/page/renderforpdf/4001. Accessed 26 September 2020
Schweitzer A, Horn J, Mikolajczyk RT, Krause G, Ott JJ (2015) Estimations of worldwide prevalence of chronic hepatitis B virus infection: a systematic review of data published between 1965 and 2013. Lancet 386:1546–1555
Sherif OS, Salama EE, Abdel-Wahhab MA (2009) Mycotoxins and child health: the need for health risk assessment. Int J Hyg Environ Health 212:347–368
Streit E, Schwab C, Sulyok M, Naehrer K, Krska R, Schatzmayr G (2013) Multi-mycotoxin screening reveals the occurrence of 139 different secondary metabolites in feed and feed ingredients. Toxins 5:504–523
Sun Z, Lu P, Gail MH, Pee D, Zhang Q, Ming L, Wang J, Wu Y, Liu G (1999) Increased risk of hepatocellular carcinoma in male hepatitis B surface antigen carriers with chronic hepatitis who have detectable urinary aflatoxin metabolite M1. Hepatology 30:379–383
Tebug SF, Chikagwa-Malunga S, Wiedemann S (2012) On-farm evaluation of dairy farming innovations uptake in northern Malawi. Livest Res Rural Dev 24:1–9
Udovicki B, Djekic I, Kalogianni EP, Rajkovic A (2019) Exposure assessment and risk characterization of aflatoxin M1 intake through consumption of milk and yoghurt by student population in Serbia and Greece. Toxins 11(4):205. https://doi.org/10.3390/toxins11040205
VICAM (2014) AflaTest, AflaM1, ZearalaTest and DONtest Instruction manuals. Available from: http://vicam.com. Accessed 10 January 2020
Walpole SC, Prieto-Merino D, Edwards P, Cleland J, Stevens G, Roberts I (2012) The weight of nations: an estimation of adult human biomass. BMC Public Health 12:439. https://doi.org/10.1186/1471-2458-12-439
Xiang X, Qin HG, You XM, Wang YY, Qi LN, Ma L, Xiang BD, Zhong JH, Li LQ (2017) Expression of P62 in hepatocellular carcinoma involving hepatitis B virus infection and aflatoxin B1 exposure. Cancer Med 6:2357–2369. https://doi.org/10.1002/cam4.1176
Acknowledgments
We acknowledge the support rendered by Chitedze Laboratory technicians in Malawi during AFM1 analysis in milk samples.
Funding
This work has been done with funds from USAID through Borlaug Higher Education for Agricultural Research and Development (BHEARD) under the Master Research Agreement #RC102095 and LSU#42900-2.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical standard
The study was conducted in full compliance with the current laws of Malawi.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(XLS 47 kb)
Rights and permissions
About this article
Cite this article
Njombwa, C.A., Moreira, V., Williams, C. et al. Aflatoxin M1 in raw cow milk and associated hepatocellular carcinoma risk among dairy farming households in Malawi. Mycotoxin Res 37, 89–96 (2021). https://doi.org/10.1007/s12550-020-00417-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12550-020-00417-5