A Comprehensive Review on Aflatoxin Contamination, Its Impact on Human Health and Management Strategies

Main Article Content

Hafiz Muhammad Sultan
Sidra Nosheen
Qurat-Ul-Ain
Fizza Hafeez
Usama Ahmed
Muhammad Zubair
Amina Bibi
Fatima Irfan

Abstract

Background: Aflatoxins are secondary metabolites produced by Aspergillus species, significantly impact global economic and health sectors, and contaminating key agricultural products such as maize, cotton, and groundnuts. The mycotoxins, particularly types B1 and B2, pose severe risks to animal and human health, leading to diseases like hepatic cellular carcinoma and liver cancer.


Objective: This review aims to analyze the prevalent impacts of AF contamination on human health and to evaluate current management strategies to mitigate this issue.


Methods: We utilize a comprehensive array of techniques to detect AF in agricultural products, including culturing, chromatography, immunochemical methods, and molecular assays. Our review also explores preventive measures during the pre-harvest and post-harvest phases of crop development, focusing on the efficacy of biopesticides in reducing contamination levels.


Results: AF contamination levels vary widely, with some regions recording levels as high as 35 ppb in crops, surpassing the maximum residue limits (5-20 ppb) set by many countries. The application of biopesticides has shown a reduction in toxigenic strain prevalence by up to 40%, demonstrating a significant decrease in AF levels in treated crops compared to untreated ones.


Conclusion: Effective management of AF contamination involves early detection and the strategic use of biopesticides to control fungal growth. Adopting these strategies can substantially reduce the health risks associated with AF exposure.

Article Details

How to Cite
Sultan, H. M., Sidra Nosheen, Qurat-Ul-Ain, Fizza Hafeez, Usama Ahmed, Muhammad Zubair, Amina Bibi, & Fatima Irfan. (2024). A Comprehensive Review on Aflatoxin Contamination, Its Impact on Human Health and Management Strategies . Journal of Health and Rehabilitation Research, 4(2), 1212–1220. https://doi.org/10.61919/jhrr.v4i2.1087
Section
Articles
Author Biographies

Hafiz Muhammad Sultan, National Agricultural Research Centre (NARC) - Islamabad - Pakistan.

Crop Diseases Research Institute (CDRI) - National Agricultural Research Centre (NARC) - Islamabad - Pakistan.

Sidra Nosheen, University of Agriculture - Faisalabad - Pakistan.

Institute of Microbiology - Faculty of Sciences - University of Agriculture - Faisalabad - Pakistan.

Qurat-Ul-Ain, University of Agriculture - Faisalabad - Pakistan.

Institute of Microbiology - Faculty of Sciences - University of Agriculture - Faisalabad - Pakistan.

Fizza Hafeez, Huazhong Agricultural University - Wuhan - China.

College of Life Sciences - Huazhong Agricultural University - Wuhan - China.

Usama Ahmed, District Headquarter Teaching Hospital - Sargodha - Pakistan.

Biosafety Level-III Laboratory - District Headquarter Teaching Hospital - Sargodha - Pakistan.

Muhammad Zubair, Khwaja Fareed University of Engineering and Information Technology - Rahim Yar Khan - Pakistan.

Institute of Biological Sciences - Khwaja Fareed University of Engineering and Information Technology - Rahim Yar Khan - Pakistan.

Amina Bibi, The Islamia University of Bahawalpur - Bahawalpur - Pakistan.

Department of Zoology - The Islamia University of Bahawalpur - Bahawalpur - Pakistan.

Fatima Irfan, Government College University - Lahore - Pakistan.

Sustainable Development Study Centre - Government College University - Lahore - Pakistan.

References

Kumar A, Pathak H, Bhadauria S, Sudan JJFP, Processing, Nutrition. Aflatoxin contamination in food crops: causes, detection, and management: a review. 2021;3:1-9.

Janik E, Niemcewicz M, Ceremuga M, Stela M, Saluk-Bijak J, Siadkowski A, et al. Molecular aspects of mycotoxins—A serious problem for human health. 2020;21(21):8187.

Eskola M, Kos G, Elliott CT, Hajšlová J, Mayar S, Krska RJCrifs, et al. Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’of 25%. 2020;60(16):2773-89.

Abo Nouh FA, Gezaf SA, Abdel-Azeem AMJAIFfSAVFAfCP. Aspergillus mycotoxins: Potential as biocontrol agents. 2020:217-37.

Pickova D, Ostry V, Malir FJT. A recent overview of producers and important dietary sources of aflatoxins. 2021;13(3):186.

Luo S, Du H, Kebede H, Liu Y, Xing FJFC. Contamination status of major mycotoxins in agricultural product and food stuff in Europe. 2021;127:108120.

Awuchi CG, Ondari EN, Ogbonna CU, Upadhyay AK, Baran K, Okpala COR, et al. Mycotoxins affecting animals, foods, humans, and plants: Types, occurrence, toxicities, action mechanisms, prevention, and detoxification strategies—A revisit. 2021;10(6):1279.

Kariyawasam RM, Dingle TC, Kula BE, Vandermeer B, Sligl WI, Schwartz ISJCM, et al. Defining COVID-19–associated pulmonary aspergillosis: systematic review and meta-analysis. 2022;28(7):920-7.

Hakamifard A, Hashemi M, Fakhim H, Aboutalebian S, Hajiahmadi S, Mohammadi RJJoMM. Fatal disseminated aspergillosis in an immunocompetent patient with COVID-19 due to Aspergillus ochraceus. 2021;31(2):101124.

Murokore BJ, Masawi AN, Wacoo AP, Wangalwa R, Ajayi COJJoFQ. Aflatoxin Susceptible Food Consumption Frequency, Prevalence, and Levels in Household Foodstuffs in Southwestern Uganda. 2023;2023.

Kaale L, Kimanya M, Macha I, Mlalila NJWMJ. Aflatoxin contamination and recommendations to improve its control: a review. 2021;14(1):27-40.

Shabeer S, Asad S, Jamal A, Ali AJT. Aflatoxin contamination, its impact and management strategies: an updated review. 2022;14(5):307.

Rocha AR, Cardoso MS, Júnior JAS, Júnior EAG, Maciel LF, Menezes-Filho JAJFC. Occurrence of aflatoxins B1, B2, G1, and G2 in beers produced in Brazil and their carcinogenic risk evaluation. 2023;145:109348.

Zeba N, Jabeen M, Raza A, Rajput MS, Tabassum S, Asif R, et al. Increased Severity due to Aflatoxin in Viral Cause of Hepatocellular Carcinoma: A Case Control Study. 2023;50(2).

Benkerroum NJIjoer, health p. Chronic and acute toxicities of aflatoxins: Mechanisms of action. 2020;17(2):423.

Ouadhene MA, Callicott KA, Ortega‐Beltran A, Mehl HL, Cotty PJ, Battilani PJEMR. Structure of Aspergillus flavus populations associated with maize in Greece, Spain, and Serbia: Implications for aflatoxin biocontrol on a regional scale. 2024;16(2):e13249.

Moore GGJCRiFS, Nutrition. Practical considerations will ensure the continued success of pre-harvest biocontrol using non-aflatoxigenic Aspergillus flavus strains. 2022;62(15):4208-25.

Klich MAJMpp. Aspergillus flavus: the major producer of aflatoxin. 2007;8(6):713-22.

Valencia-Quintana R, Milić M, Jakšić D, Šegvić Klarić M, Tenorio-Arvide MG, Pérez-Flores GA, et al. Environment changes, aflatoxins, and health issues, a review. 2020;17(21):7850.

Maina AW, Wagacha JM, Mwaura FB, Muthomi JW, Woloshuk CP. Postharvest practices of maize farmers in Kaiti District, Kenya and the impact of hermetic storage on populations of Aspergillus spp. and aflatoxin contamination. 2016.

Abdel-Hadi A, Schmidt-Heydt M, Parra R, Geisen R, Magan NJJotRSI. A systems approach to model the relationship between aflatoxin gene cluster expression, environmental factors, growth and toxin production by Aspergillus flavus. 2012;9(69):757-67.

Priesterjahn E-M, Geisen R, Schmidt-Heydt MJM. Influence of light and water activity on growth and mycotoxin formation of selected isolates of Aspergillus flavus and Aspergillus parasiticus. 2020;8(12):2000.

Dong T, Qiao S, Xu J, Shi J, Qiu J, Ma GJT. Effect of abiotic conditions on growth, mycotoxin production, and gene expression by Fusarium fujikuroi species complex strains from maize. 2023;15(4):260.

Caceres I, Al Khoury A, El Khoury R, Lorber S, P. Oswald I, El Khoury A, et al. Aflatoxin biosynthesis and genetic regulation: A review. 2020;12(3):150.

Liu X, Guan X, Xing F, Lv C, Dai X, Liu YJFC. Effect of water activity and temperature on the growth of Aspergillus flavus, the expression of aflatoxin biosynthetic genes and aflatoxin production in shelled peanuts. 2017;82:325-32.

Hellany H, Assaf JC, El-Badan D, Khalil MJP. Quantification, Prevalence, and Pretreatment Methods of Mycotoxins in Groundnuts and Tree Nuts: An Update. 2023;11(12):3428.

Ma NL, Peng W, Soon CF, Hassim MFN, Misbah S, Rahmat Z, et al. Covid-19 pandemic in the lens of food safety and security. 2021;193:110405.

Mahato DK, Lee KE, Kamle M, Devi S, Dewangan KN, Kumar P, et al. Aflatoxins in food and feed: An overview on prevalence, detection and control strategies. 2019;10:483502.

Jallow A, Xie H, Tang X, Qi Z, Li PJCrifs, safety f. Worldwide aflatoxin contamination of agricultural products and foods: From occurrence to control. 2021;20(3):2332-81.

Battilani P, Toscano P, Van der Fels-Klerx H, Moretti A, Camardo Leggieri M, Brera C, et al. Aflatoxin B1 contamination in maize in Europe increases due to climate change. 2016;6(1):24328.

Tahir NI, Hussain S, Javed M, Rehman H, Shahzady TG, Parveen B, et al. Nature of aflatoxins: Their extraction, analysis, and control. 2018;38(6):e12561.

Kenei F, Mezene Woyessa AM, Lema K, Gemmeda MJJLR. Review on Occurrence and Public Health Significance of Aflatoxin in Dairy Products and Feed. 2023;13:1-13.

Dhanasekaran D, Shanmugapriya S, Thajuddin N, Panneerselvam AJA-B, Biology M. Aflatoxins and aflatoxicosis in human and animals. 2011;10(22717):221-54.

Chandra P. Aflatoxins: Food safety, human health hazards and their prevention. Aflatoxins-Occurrence, Detoxification, Determination and Health Risks: IntechOpen; 2021.

Mohamed SI, Shehata SA, Bassiony SM, Mahgoub SA, Abd El-Hack MEJP, Proteins A. Does the use of different types of probiotics possess detoxification properties against aflatoxins contamination in rabbit diets? 2023;15(5):1382-92.

Benkerroum NJIjoer, health p. Aflatoxins: Producing-molds, structure, health issues and incidence in Southeast Asian and Sub-Saharan African countries. 2020;17(4):1215.

Chain EPoCitF, Schrenk D, Bignami M, Bodin L, Chipman JK, del Mazo J, et al. Risk assessment of aflatoxins in food. 2020;18(3):e06040.

Yousaf A, Tasneem N, Mustafa A, Fatima R, Nabia N, Khan RA, et al. Gastric cancer associated risk factors and prevalence in Pakistan. 2021;1(2):73-8.

Riaz M, Zubair M, Iqbal MK, Bukhari SMA, Sultan HMJJoCO, Sciences M. Exploring the platelet and cancer cell interaction in metastasis targeting: Platelets and cancer cell interaction. 2024.

Liu Y, Wu FJEhp. Global burden of aflatoxin-induced hepatocellular carcinoma: a risk assessment. 2010;118(6):818-24.

Wu HC, Santella RJHm. The role of aflatoxins in hepatocellular carcinoma. 2012;12(10 HCC).

Ma J, Liu Y, Guo Y, Ma Q, Ji C, Zhao LJT. Transcriptional profiling of aflatoxin B1-induced oxidative stress and inflammatory response in macrophages. 2021;13(6):401.

Monson MS, Coulombe RA, Reed KMJA. Aflatoxicosis: Lessons from toxicity and responses to aflatoxin B1 in poultry. 2015;5(3):742-77.

Kosmidis C, Denning DWJT. The clinical spectrum of pulmonary aspergillosis. 2015;70(3):270-7.

Arastehfar A, Carvalho A, Houbraken J, Lombardi L, Garcia-Rubio R, Jenks J, et al. Aspergillus fumigatus and aspergillosis: From basics to clinics. 2021;100(1):100115-.

Maryam S, Rasheed M, Javed I, Amjad M, Sultan HJAJoM, Sciences A. Synthesis and Function of Multi-modality Probe for Early Tumor Diagnosis in Mouse. 2021:152-62.

Chuang WY, Hsieh YC, Lee T-TJA. The effects of fungal feed additives in animals: A review. 2020;10(5):805.

Janssens I, Lambrecht BN, Van Braeckel E, editors. Aspergillus and the Lung. Seminars in Respiratory and Critical Care Medicine; 2024: Thieme Medical Publishers, Inc.

Lee M-R, Huang H-L, Chen L-C, Yang H-C, Ko J-C, Cheng M-H, et al. Seroprevalence of Aspergillus IgG and disease prevalence of chronic pulmonary aspergillosis in a country with intermediate burden of tuberculosis: A prospective observational study. 2020;26(8):1091. e1-. e7.

Marr KA, Platt A, Tornheim JA, Zhang SX, Datta K, Cardozo C, et al. Aspergillosis complicating severe coronavirus disease. 2021;27(1):18.

Khambati A, Wright III RE, Das S, Pasula S, Sepulveda A, Hernandez F, et al. Aspergillus endophthalmitis: Epidemiology, pathobiology, and current treatments. 2022;8(7):656.

Sipos P, Peles F, Brassó DL, Béri B, Pusztahelyi T, Pócsi I, et al. Physical and chemical methods for reduction in aflatoxin content of feed and food. 2021;13(3):204.

Maguey-González JA, Nava-Ramírez MdJ, Gómez-Rosales S, Ángeles MdL, Solís-Cruz B, Hernández-Patlán D, et al. Humic acids preparation, characterization, and their potential adsorption capacity for aflatoxin B1 in an in vitro poultry digestive model. 2023;15(2):83.

Alameri MM, Kong AS-Y, Aljaafari MN, Ali HA, Eid K, Sallagi MA, et al. Aflatoxin contamination: An overview on health issues, detection and management strategies. 2023;15(4):246.

Babaee R, Karami-Osboo R, Mirabolfathy MJJoFC, Analysis. Evaluation of the use of Ozone, UV-C and Citric acid in reducing aflatoxins in pistachio nut. 2022;106:104276.

Afsah‐Hejri L, Hajeb P, Ehsani RJJCRiFS, Safety F. Application of ozone for degradation of mycotoxins in food: A review. 2020;19(4):1777-808.

Sultan HJAJoM, Sciences A. Protein and Polysaccharide Base Biomaterial for The Formation of Composite Bone Scaffold. 2021:80-8.

Marshall H, Meneely JP, Quinn B, Zhao Y, Bourke P, Gilmore BF, et al. Novel decontamination approaches and their potential application for post-harvest aflatoxin control. 2020;106:489-96.

Gibellato S, Dalsóquio L, Do Nascimento I, Alvarez TJWMJ. Current and promising strategies to prevent and reduce aflatoxin contamination in grains and food matrices. 2021;14(3):293-304.

Somda MK, Dabire Y, Mogmenga I, Ouattara A, Nikiema M, Mihin HB, et al. Assessment of maize contamination by aflatoxin in Burkina Faso: A review of methods of control. 2023;14(2):135-47.

Sirohi R, Tarafdar A, Gaur VK, Singh S, Sindhu R, Rajasekharan R, et al. Technologies for disinfection of food grains: Advances and way forward. 2021;145:110396.

Kutasi K, Recek N, Zaplotnik R, Mozetič M, Krajnc M, Gselman P, et al. Approaches to inactivating aflatoxins—a review and challenges. 2021;22(24):13322.

Tatar Y, Fadavi A, Koohsari HJJoCP. Mitigation of Aspergillus flavus and its aflatoxins in wheat grains by gamma irradiation and calcium oxide. 2021;10(2):261-70.

Guo Y, Zhao L, Ma Q, Ji CJFRI. Novel strategies for degradation of aflatoxins in food and feed: A review. 2021;140:109878.

Nazhand A, Durazzo A, Lucarini M, Souto EB, Santini AJF. Characteristics, occurrence, detection and detoxification of aflatoxins in foods and feeds. 2020;9(5):644.

Khan R, Ghazali FM, Mahyudin NA, Samsudin NIPJJoF. Biocontrol of aflatoxins using non-aflatoxigenic Aspergillus flavus: A literature review. 2021;7(5):381.

Ren X, Zhang Q, Zhang W, Mao J, Li PJT. Control of aflatoxigenic molds by antagonistic microorganisms: Inhibitory behaviors, bioactive compounds, related mechanisms, and influencing factors. 2020;12(1):24.

Cotty PJ, Probst C, Jaime-Garcia RJMdm, management, public health, trade a. Etiology and management of aflatoxin contamination. 2008:287-99.

Cotty P, Bayman PJP. Competitive exclusion of a toxigenic strain of Aspergillus flavus by an atoxigenic strain. 1993;83(12):1283-7.

Cotty PJJPD. Development of Aspergillus flavus AF36. 2005.

Dorner J, Lamb MJMR. Development and commercial use of afla-Guard®, an aflatoxin biocontrol agent. 2006;22:33-8.

Mauro A, Garcia-Cela E, Pietri A, Cotty PJ, Battilani PJT. Biological control products for aflatoxin prevention in Italy: Commercial field evaluation of atoxigenic Aspergillus flavus active ingredients. 2018;10(1):30.

Senghor A, Ortega-Beltran A, Atehnkeng J, Jarju P, Cotty P, Bandyopadhyay RJPD. Aflasafe SN01 is the first biocontrol product approved for aflatoxin mitigation in two nations, Senegal and The Gambia. 2021;105(05):1461-73.

Agbetiameh D, Ortega-Beltran A, Awuah RT, Atehnkeng J, Elzein A, Cotty PJ, et al. Field efficacy of two atoxigenic biocontrol products for mitigation of aflatoxin contamination in maize and groundnut in Ghana. 2020;150:104351.

Bandyopadhyay R, Ortega-Beltran A, Akande A, Mutegi C, Atehnkeng J, Kaptoge L, et al. Biological control of aflatoxins in Africa: current status and potential challenges in the face of climate change. 2016;9(5):771-89.

Konlambigue M, Ortega-Beltran A, Bandyopadhyay R, Shanks T, Landreth E, Jacob O. Lessons learned on scaling Aflasafe® through commercialization in Sub-Saharan Africa: Intl Food Policy Res Inst; 2020.

Mahuku GS. AR-NAFAKA Project Aflatoxin Management: 2016-2017 Progress. 2017.

Atehnkeng J, Ojiambo P, Ikotun T, Sikora R, Cotty P, Bandyopadhyay RJFa, et al. Evaluation of atoxigenic isolates of Aspergillus flavus as potential biocontrol agents for aflatoxin in maize. 2008;25(10):1264-71.

Ehrlich KCJFim. Non-aflatoxigenic Aspergillus flavus to prevent aflatoxin contamination in crops: advantages and limitations. 2014;5:79174.

Donner M. Distribution and molecular characterization of aflatoxin-producing and nonproducing isolates of Aspergillus section Flavi for biological control of aflatoxin contamination in maize in Nigeria: Universitäts-und Landesbibliothek Bonn; 2009.

Ouadhene MA. New insights on Aspergillus flavus population in maize crops to boost the application of biocontrol with atoxigenic strains in Europe. 2023.

Lagogianni CS, Tsitsigiannis DIJFiM. Effective biopesticides and biostimulants to reduce aflatoxins in maize fields. 2019;10:490364.

Ortega‐Beltran A, Grubisha L, Callicott K, Cotty PJJoam. The vegetative compatibility group to which the US biocontrol agent Aspergillus flavus AF36 belongs is also endemic to Mexico. 2016;120(4):986-98.

Okun DO, Khamis FM, Muluvi GM, Ngeranwa JJ, Ombura FO, Yongo MO, et al. Distribution of indigenous strains of atoxigenic and toxigenic Aspergillus flavus and Aspergillus parasiticus in maize and peanuts agro-ecological zones of Kenya. 2015;4:1-10.

Yan L, Song W, Chen Y, Kang Y, Lei Y, Huai D, et al. Effect of non-aflatoxigenic strains of Aspergillus flavus on aflatoxin contamination of pre-harvest peanuts in fields in China. 2021;6(2):81-6.

Sood M, Kapoor D, Kumar V, Sheteiwy MS, Ramakrishnan M, Landi M, et al. Trichoderma: The “secrets” of a multitalented biocontrol agent. 2020;9(6):762.

Modrzewska M, Błaszczyk L, Stępień Ł, Urbaniak M, Waśkiewicz A, Yoshinari T, et al. Trichoderma versus Fusarium—inhibition of pathogen growth and mycotoxin biosynthesis. 2022;27(23):8146.

Ren X, Branà MT, Haidukowski M, Gallo A, Zhang Q, Logrieco AF, et al. Potential of Trichoderma spp. for biocontrol of aflatoxin-producing Aspergillus flavus. 2022;14(2):86.

Gandía M, Kakar A, Giner-Llorca M, Holzknecht J, Martínez-Culebras P, Galgóczy L, et al. Potential of antifungal proteins (AFPs) to control Penicillium postharvest fruit decay. 2021;7(6):449.

Visagie CM, Magistà D, Ferrara M, Balocchi F, Duong TA, Eichmeier A, et al. IMA genome-F18: The re-identification of Penicillium genomes available in NCBI and draft genomes for Penicillium species from dry cured meat, Penicillium biforme, P. brevicompactum, P. solitum, and P. cvjetkovicii, Pewenomyces kutranfy, Pew. lalenivora, Pew. tapulicola, Pew. kalosus, Teratosphaeria carnegiei, and Trichoderma atroviride SC1. 2023;14(1):21.