Skip to main content

Advertisement

SpringerLink
Log in

Aflatoxin-lysine adducts in blood serum of the Malawian rural population and aflatoxin contamination in foods (groundnuts, maize) in the corresponding areas

  • Original Article
  • Published:
Mycotoxin Research Aims and scope Submit manuscript

Abstract

Aflatoxin-lysine (AFB1-lys) adduct levels in blood samples collected from 230 individuals living in three districts of Malawi (Kasungu, Mchinji, and Nkhotakota) and aflatoxin B1 (AFB1) levels in groundnut and maize samples collected from their respective homesteads were determined using indirect competitive enzyme-linked immunosorbent assay (IC-ELISA) methods. AFB1-lys adducts were detected in 67% of blood samples, with a mean concentration of 20.5 ± 23.4 pg/mg of albumin. AFB1 was detected in 91% of groundnut samples and in 70% of maize samples, with mean AFB1 levels of 52.4 and 16.3 μg/kg, respectively. All participants of this study reported consuming maize on a daily basis and consuming groundnuts regularly (mean consumption frequency per week: 3.2 ± 1.7). According to regression analysis, a frequency of groundnut consumption of more than four times per week, being female, and being a farmer were significant (p < 0.05) contributors to elevated AFB1-lys adduct levels in the blood. This is the first report on AFB1-lys adducts in blood samples of residents in Malawi. The results reinforce the urgent need for interventions, aiming at a reduction of aflatoxin exposure of the population.

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

  • Abass HK, Shier WT, Horn BW, Weaver MA (2004) Cultural methods for aflatoxin detection. J Toxicol Toxin Rev 23:295–315

    Article  CAS  Google Scholar 

  • Anitha S, Waliyar F, Reddy AS, Rao R, Raghunadha-Rao D, Kumar PL (2011) The development of simple enzyme-linked immunosorbent assay for quantitative estimation of aflatoxin B1 adduct in humans. Curr Sci 101:844–846

    CAS  Google Scholar 

  • Chawanthayatham S, Thiantantwat A, Egner PA, Groopman JD, Wogan GN, Croy RG, Essigmann JM (2015) Prenatal exposure of mice to the human liver carcinogen aflatoxin B1 reveals a critical window of susceptibility to genetic changes. Int J Cancer 136:1254–1262

    Article  PubMed  CAS  Google Scholar 

  • Chen SY, Chen CJ, Chou SR, Hsieh LL, Wang LY, Tsai WY, Ahsan H, Santella RM (2001) Association of aflatoxin B1-albumin adduct levels with hepatitis B surface antigen status among adolescents in Taiwan. Cancer Epidemiol Biomark Prev 10:1223–1226

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Degen GH (2011) Tools for investigating workplace related risks from mycotoxin exposure. WMJ 4(3):315–327

    Google Scholar 

  • Do JH, Choi D (2007) Aflatoxins: detection, toxicology and biosynthesis. Biotechnol Bioprocess Eng 12:585–593

    Article  CAS  Google Scholar 

  • Eaton DL, Gallagher EP (1994) The mechanism of aflatoxin carcinogenesis. Annu Rev Pharmacol Toxicol 34:135–172

    Article  PubMed  CAS  Google Scholar 

  • Eaton DL, Groopman JD (1994) The toxicology of aflatoxins: human health, veterinary, and agricultural significance. Academic Press Inc., San Diego

    Google Scholar 

  • Ecker O, Qaim M (2011) Analyzing nutritional impacts of policies: an empirical study for Malawi. World Dev 39:412–428

    Article  Google Scholar 

  • Ediage EN, Diana Di Mavungu J, Song S, Wu A, Van Peteghem C, De Saeger S (2012) A direct assessment of mycotoxin biomarkers in human urine samples by liquid chromatography tandem mass spectrometry. Anal Chim Acta 741:58–69

    Article  PubMed  CAS  Google Scholar 

  • El-Nahla SM, Imam HM, Moussa EA, Ibrahim AM, Ghanam AR (2013) Teratogenic effects of aflatoxin in rabbits (Orycto-laguscuniculus). J Vet Anat 6:67–85

    Google Scholar 

  • Fitzgerald G (2015) The production of ready to use therapeutic food in Malawi: smallholder farmers’ experience with groundnut production: results from a four year livelihoods analysis in Malawi’s Central Region. University of College Cork, Cork http://www.validnutrition.org/wp-content/uploads/2015/03/The-Production-of-RUTF-in-Malawi-Part-1-Smallholder-famers-experience-with-groundnut-production-.pdf

    Google Scholar 

  • Gong YY, Egal S, Hounsa A, Turner PC, Hall AJ, Cardwell KF, Wild CP (2003) Determinants of aflatoxin exposure in young children from Benin and Togo, West Africa: the critical role of weaning. Int J Epidemiol 32:556–562. https://doi.org/10.1093/ije/dyg109.

    Article  PubMed  CAS  Google Scholar 

  • Gong YY, 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 113:1763–1767

    Google Scholar 

  • Groopman JD, Wild CP, Hasler J, Junshi C, Wogan GN, Kensler TW (1993) Molecular epidemiology of aflatoxin exposures: validation of aflatoxin-N7-guanine levels in urine as a biomarker in experimental rat models and humans. Environ Health Perspect 99:107–113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hayes AF, Cai L (2007) Using heteroskedasticity-consistent standard error estimators in OLS regression: an introduction and software implementation. Behav Res Methods 39:709–722

    Article  PubMed  Google Scholar 

  • IARC (2002) Working group on the evaluation of carcinogenic risks to humans. Some traditional herbal medicines, some mycotoxins, naphthalene and styrene. IARC Monogr Eval Carcinog Risk Chem Hum 82:1–556

    Google Scholar 

  • Imbens GW, Kolesár M (2016) Robust standard errors in small samples: some practical advice. Rev Econ Stat 98:701–712

    Article  Google Scholar 

  • International Agency for Research on Cancer (IARC) (1993) Some naturally occurring substances, food items and constituents, heterocyclic aromatic amines and mycotoxins. World health Organization, International Agency for Research in Cancer. IARC Monogrpahs on evaluation of carcinogenic risks to humans. Lyon, France 56:245–391

  • Jiang Y, Jolly PE, Preko P, Wang JS, Ellis WO, Phillips TD (2008) Aflatoxin related immune dysfunction in health and in human immunodeficiency virus disease. Clin Dev Immunol 2008:12 Article ID 790309. https://doi.org/10.1155/2008/790309.

  • Johnson WW, Harris TM, Guengerich FP (1996) Kinetics and mechanism of hydrolysis of aflatoxin B1 exo-8,9-oxide and rearrangement of the dihydrodiol. J Am Chem Soc 118:8213–8220

    Article  CAS  Google Scholar 

  • Jolly PE (2014) Aflatoxin: does it contribute to an increase in HIV viral load? Future Microbiol 9:121–124

    Article  PubMed  CAS  Google Scholar 

  • Jolly PE, Inusah S, Lu B, Ellis WO, Nyarko A, Phillips TD, Williams JH (2013) Association between high aflatoxin B1 levels and high viral load in HIV-positive people. WMJ 6:255–261

    CAS  Google Scholar 

  • Leong YH, Latiff AA, Ahmad NI, Rosma A (2012) Exposure measurement of aflatoxins and aflatoxin metabolites in human body fluids. Mycotoxin Res 28:79–87

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Chang CH, Marsh GM, Wu F (2012) Population attributable risk of aflatoxin-related liver cancer. Systematic review and meta-analysis. Eur J Cancer 48:2125–2136

    Article  PubMed  PubMed Central  Google Scholar 

  • Magoha H, Kimanya M, De Meulenaer B, Roberfroid D, Lachat C, Kolsteren P (2014) Association between aflatoxin M1 exposure through breast milk and growth impairment in infants from Northern Tanzania. WMJ 7:277–284

    CAS  Google Scholar 

  • Matumba L, Sulyo M, Monjerez M, Biswick T, Kruska R (2015a) Fungal metabolites diversity in maize and associated human dietary exposures relate to micro-climatic patterns in Malawi. WMJ 8:269–282

    CAS  Google Scholar 

  • Matumba L, Van Poucke C, Njumbe Ediage E, Jacobs B, De Saegar S (2015b) Effectiveness of hand sorting, flotation/washing, dehulling and combinations thereof on the decontamination of mycotoxin-contaminated white maize. Food Addit Contam 32:960–969

    Article  CAS  Google Scholar 

  • McDonald JF, Moffitt RA (1980) The review of economics and statistics: the uses of Tobit analysis. Rev Econ Stat 62:318–321

    Article  Google Scholar 

  • Monyo ES, Njoroge SMC, Coe R, Osiru M, Madinda F, Waliyar F, Thakur RP, Chilunjika T, Anitha S (2012) Occurance and distribution of aflatoxin contamination in groundnuts and population density of aflatoxigenic Aspergilli in Malawi. Crop Prot 42:149–155

    Article  CAS  Google Scholar 

  • National Statistical Office (NSO) [Malawi] and ICF (2017) Malawi Demographic and Health Survey 2015–2016. Zomba, Malawi and Rockvillie, Maryland, USA, NSO and ICF. Government of Malawi. pp 692. https://dhsprogram.com/pubs/pdf/FR319/FR319.pdf

  • Oswald IP, Martin DE, Bouhet S, Pinton P, Taranu I, Accensi F (2005) Immunotoxicological risk of mycotoxins for domestic animals. Food Addit Contam 22:354–360

    Article  PubMed  CAS  Google Scholar 

  • Park DL, Trucksess MW, Nesheim S, Stack M, Newell RF (1994) Solvent-efficient thin-layer chromatographic method for the determination of aflatoxins B1, B2, G1, and G2 in corn and peanut products: collaborative study. J AOAC Int 77(3):637–646

    PubMed  CAS  Google Scholar 

  • Ranjan PK, Phanindra G (2014) Determinants and constraints of modern varieties of paddy adoption by marginal and small farmers in Odisha: a Tobit analysis. Agric Econ Res Rev 27:189

    Google Scholar 

  • Reddy SV, Kiran Mayi D, Uma Reddy M, Thirumala-Devi, Reddy DVR (2001) Aflatoxin B1 in different grades of chillies (Capsicum annum L.) in India as determined by indirect competitive ELISA. Food Addit Contam 18:553–558

    Article  PubMed  CAS  Google Scholar 

  • Sabbioni G (1990) Chemical and physical properties of the major serum albuim adduct of aflatoxin B1 and their implications for the quantification in biological samples. Chem Biol Interact 75:1–15

    Article  PubMed  CAS  Google Scholar 

  • Sabbioni G, Ambs S, Wogan GN, Groopman JD (1990) The aflatoxin-lysine adduct quantified by high performance liquid chromatography from human serum albumin samples. Carcinogenesis 11:2063–2066

    Article  PubMed  CAS  Google Scholar 

  • Seetha A, Munthali W, Msere HW, Swai E, Muzanila Y, Sichone E, Tsusaka TW, Okori P (2017) Occurrence of aflatoxins and its management in diverse cropping system of central Tanzania. Mycotoxin Res 33:323–331. https://doi.org/10.1007/s12550-017-0286-x

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shirima CP, Kimanya ME, Kinabo JL, Rourledge MN, Srey C, Wild CP, Gong YY (2013) Dietary exposure to aflatoxin and fumonisin among Tanzania children as determined using biomarkers of exposure. Mol Nutr Food Res 57:1874–1881

  • Shirima CP, Kimanya ME, Routledge MN, Srey C, Kinabo JL, Humpf HU, Wild CP, Tu YK, Gong YY (2015) A prospective study of growth and biomarkers of exposure to aflatoxin and fumonisin during early childhood in Tanzania. Environ Health Perspect 123:173–178

    Article  PubMed  CAS  Google Scholar 

  • Sun CA, Wu DM, Wang LY, Chen CJ, You SL, Santella RM (2002) Determinants of formation of aflatoxin-albumin adducts; a seven township study in Taiwan. Br J Cancer 87:966–970

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tsusaka TW, Msere HW, Siambi M, Mazvimavi K, Okori P (2016) The evolution and impacts of groundnut research and development in Malawi: an ex-post analysis. Afr J Agric Res 11:139–158. https://doi.org/10.5897/AJAR2015.10167

    Article  Google Scholar 

  • Tsusaka TW, Singano C, Kumwenda N, Seetha A (2017) “On-farm assessment of post-harvest losses: the case of groundnut in Malawi” Socioeconomics Discussion Paper Series 43, Patancheru 502 324, Telangana: International Crops Research Institute for the Semi-Arid Tropics, 59pp. http://oar.icrisat.org/10049/1/T_Tsusaka_etal_ISEDPS_43.pdf

  • Turner PC (2013) The molecular epidemiology of chronic aflatoxin driven impaired child growth. Scientifica, Article ID 152879, 21 pages. https://doi.org/10.1155/2013/152879

  • Turner PC, Dingley KH, Coxhead J, Russell S, Garner CR (1998) Detectable levels of serum aflatoxin B1 exposure in the United Kingdom. Cancer Epidemiol Biomarker Prev 7:441–447

    CAS  Google Scholar 

  • Turner PC, Sylla A, Gong YY, Diallo MS, Sutcliffe AE, Hall AJ, Wild CP (2005) Reduction in exposure to carcinogenic aflatoxins by postharvest intervention measures in West Africa: a community-based intervention study. Lancet 365:1950–1956

    Article  PubMed  CAS  Google Scholar 

  • Verma RJ (2004) Aflatoxin causes DNA damage. Int J Hum Genet 4:231–236

    Article  CAS  Google Scholar 

  • Waliyar F, Reddy SV, Kumar PL (2009) Review of immunological methods for the quantification of aflatoxins in peanut and other foods. Peanut Sci 36:54–59

    Article  Google Scholar 

  • Warth B, Braun D, Ezekiel CN, Turner PC, Degan GH, Marko D (2016) Bio-monitoring of mycotoxins in human breast milk: current state and future perspectives. Chem Res Toxicol 29:1087–1097. https://doi.org/10.1021/acs.cherestox.6b00125.

    Article  PubMed  CAS  Google Scholar 

  • Wild CP, Turner PC (2002) The toxicology of aflatoxins as a basis for public health decisions. Mutagenesis 17(6):471–481

    Article  PubMed  CAS  Google Scholar 

  • Wild CP, Garner RC, Montesano R, Tursi F (1986) Aflatoxin B1 binding to plasma albumin and liver DNA upon chronic administration to rats. Carcinogenesis 7(6):853–858

    Article  PubMed  CAS  Google Scholar 

  • Wild CP, Jiang YZ, Sabbioni G, Chapot B, Montesano R (1990) Evaluation of methods for quantitation of aflatoxin-albumin adducts and their application to human exposure assessment. Cancer Res 50(2):245-251

  • Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D (2004) Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr 80:1106–1122

    Article  PubMed  CAS  Google Scholar 

  • Wong JJ, Hsieh DP (1976) Mutagenicity of aflatoxins related to their metabolism and carcinogenic potential. Proc Natl Acas Sci USA 73:2241–2244

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank the National Health Science Research Committee (NHSRC), Malawi, for permitting the implementation of this study.

Funding

This study was financially supported by the McKnight Foundation (USA) and the CGIAR Research Program on Agriculture for Nutrition and Health (CRP A4NH).

Author information

Authors and Affiliations

  1. International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), PO Box 1096, Lilongwe, Malawi

    Anitha Seetha, Takuji W. Tsusaka, Harry W. Msere & Dickson Mbughi

  2. International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Patancheru, Hyderabad, Telangana, India

    Emmanuel S. Monyo

  3. Arusha Lutheran Medical Center, Arusha, Tanzania

    Frank Madinda

  4. Kamuzu Central Hospital, Lilongwe, Malawi

    Tiyamika Chilunjika

  5. Food and Agricultural Organization (FAO), Lilongwe, Malawi

    Ethel Sichone

  6. Community Health Sciences Unit (CHSU), P/Bag 65, Lilongwe, Malawi

    Benson Chilima

  7. Food Technology and Nutrition Group, Lilongwe University of Agriculture and Natural Resources, NRC Campus, PO Box 143, Lilongwe, Malawi

    Limbikani Matumba

Authors
  1. Anitha Seetha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emmanuel S. Monyo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takuji W. Tsusaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Harry W. Msere
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Frank Madinda
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tiyamika Chilunjika
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ethel Sichone
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dickson Mbughi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Benson Chilima
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Limbikani Matumba
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anitha Seetha.

Ethics declarations

The study with human volunteers was approved by National Health Sciences Research Committee (NHSRC) of Malawi. All objectives of the study were clearly explained to the participants by medical professionals, and consent was obtained from each volunteer before collecting 10 ml of blood. In cases of minors, written consent was obtained from parents and guardians.

Conflict of interest

The authors declare that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seetha, A., Monyo, E.S., Tsusaka, T.W. et al. Aflatoxin-lysine adducts in blood serum of the Malawian rural population and aflatoxin contamination in foods (groundnuts, maize) in the corresponding areas. Mycotoxin Res 34, 195–204 (2018). https://doi.org/10.1007/s12550-018-0314-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12550-018-0314-5

Keywords

Search

Navigation