Aflatoxins Contamination of Human Food Commodities Collected from Jeddah Markets, Saudi Arabia

Mahmoud  El Tawila; Serdar Sadeq; Alrasheedi Amani Awad; Jamil Serdar; Mohamed Hussein Fahmy Madkour; Mohamed M. Deabes

doi:10.3889/oamjms.2020.4643

Authors

Mahmoud El Tawila Department of Environmental Science, Faculty of Meteorology, Environment and Arid land Agriculture, King Abdulaziz University, Jeddah, Saudi Arabia
Serdar Sadeq Ministry of Health Saudi Arabia, Public Health Ministry of Health, Health Programs and Chronic Disease, Saudi Arabia
Alrasheedi Amani Awad Department of Food Nutrition, Faculty of Home Economics, King Abdulaziz University, Jeddah, Saudi Arabia
Jamil Serdar Ministry of Health Saudi Arabia, Alzahir Primary Health Care Centre, Saudi Arabia
Mohamed Hussein Fahmy Madkour Faculty of Environment and Arid Land Agriculture, King Abdulaziz University, Jeddah, Saudi Arabia
Mohamed M. Deabes Department of Food Toxicology and Contaminants, National Research Centre, Dokki, Giza, Egypt

DOI:

https://doi.org/10.3889/oamjms.2020.4643

Keywords:

Human food commodities, Aflatoxins, HPLC, Nuts, Cereal

Abstract

BACKGROUND: Aflatoxins (AFs) are fungal secondary metabolites produced by Aspergillus flavus. They contaminate of dietary food with AFs is a worldwide problem that affects both food safety and agricultural economies.

AIM: The aim of this study was designed to investigate the AFs contents of human food commodities mostly consumed in Jeddah, Saudi Arabia.

METHODS: The study was designed in vitro, contents in six food categories. A total of 288 samples were collected from 78 different markets in Jeddah. AFs were determined by high-performance liquid chromatography with fluorescence detector using immunoaffinity column clean-up.

RESULTS: The results indicated that the incidence rate 27.3% of nut samples collected from Jeddah, were contaminated with AFB1, AFB2. The concentrations of AFs (AFB1, AFB2, AFG1, and AFG2) were ranged from 0.19–482.4, 0.09–3.34, 0.19–87.1, to 0.09–579 μg/kg in the nut samples.

CONCLUSION: The results demonstrate the importance of routine monitoring of AFs contamination in various dry foods for human consumed should be performed regularly and the nuts contained high levels of AFs. The legal regulations must be unauthorized for human consumption to control the health risks associated with AFs.

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References

Wilson DM, Mubatanhema W, Jurjevic Z. Biology and ecology of mycotoxigenic Aspergillus species as related to economic and health concerns. Adv Exp Med Biol. 2002;504:3-17. https://doi.org/10.1007/978-1-4615-0629-4_2 PMid:11922097

Bathnagar D, Garcia S. Aspergillus. In: Labbe RG, Garcıa S, editors. Guide to Foodborne Pathogens. New York: John Wiley and Sons; 2001. p. 35-49.

International Agency for Research on Cancer. Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Amines and Mycotoxins. IARC Monographs on Evaluation of Carcinogenic Risk to Humans. Lyon, France: International Agency for Research on Cancer; 1993. p. 56. https://doi.org/10.1016/0003-2670(94)80328-5

Theumer MG, Henneb Y, Khoury L, Snini SP, Tadrist S, Canlet C, et al. Genotoxicity of aflatoxins and their precursors in human cells. Toxicol Lett. 2018;287:100-7. https://doi.org/10.1016/j.toxlet.2018.02.007 PMid:29421331

IARC. Aflatoxins, IARC Monographs on the Evaluvation of Carcinogenic Risks on Humans. Mono100-23. Lyon, France: IARC; 2012. Available from:https://monographs.iarc.fr/ENG/Monographs/%E2%80%A6/mono100F-23.pdf.

Joint FAO/WHO Expert Committee on Food Additives. 49th Meeting of the Joint FAO/WHO Expert Committee on Food Additives. In: Safety Evaluation of Certain Food Additives and Contaminants: Aflatoxins WHO Food Additives Series No. 40. Geneva: World Health Organization; 1998. p. 359-469. https://doi.org/10.1191/096032799678839888

Thuvander A, Moller T, Barbieri HE, Jansson A, Salomonsson AC, Olsen M. Dietary intake of some important mycotoxins by the Swedish population. Food Addit Contam. 2001;18(8):696-706. https://doi.org/10.1080/02652030121353 PMid:11469326

Ministry of Agriculture and Rural Affairs, Republic of Turkey. Data on Aflatoxins in Hazelnuts, Pistachios, Walnuts and Almonds during 1998-2002. Beijing, China: Ministry of Agriculture and Rural Affairs; 2002.

Ito Y, Peterson SW, Wicklow DT, Goto T. Aspergillus pseudo-tamariia new aflatoxin producing species in Aspergillus section Flavi. Mycol Res. 2001;105:233-9. https://doi.org/10.1017/s0953756200003385

Peterson SW, Ito Y, Horn BW, Goto T. Aspergillus bombycis, a new aflatoxigenic species, A. nomius. Mycologia. 2001;93:689-703. https://doi.org/10.1080/00275514.2001.12063200

Ehrlich KC, Chang PK, Yu J, Cotty PJ. Aflatoxins biosynthesis cluster gene cypA is required for G aflatoxin formation. Appl Environ Microbiol. 2004;70:6518-24. https://doi.org/10.1128/aem.70.11.6518-6524.2004 PMid:15528514

Lanyasunya TP, Wamae LW, Musa HH, Olowofeso O, Lokwaleput IK. The risk of mycotoxins contamination of dairy feed and milk on smallholder dairy farms in Kenya. Pak J Nutr. 2005;4(3):162-9.

Rahimi E, Bonyadian M, Rafei M, Kazemeini HR. Occurrence of aflatoxin M1 in raw milk of five dairy species in Ahvaz, Iran. Food Chem Toxicol. 2010;48(1):129-31. https://doi.org/10.1016/j.fct.2009.09.028 PMid:19786054

El-Nezami HS, Nicoletti G, Neal GE, Donohue DC, Ahokas JT. Aflatoxin M1 in human breast milk samples from Victoria, Australia and Thailand. Food Chem Toxicol. 1995;33(3):173-9. https://doi.org/10.1016/0278-6915(94)00130-g PMid:7896226

Fung F, Clark RF. Health effects of mycotoxins: A toxicological overview. J Toxicol Clin Toxicol. 2004;42(2):217-34. PMid:15214629

Binder EM, Tan LM, Chin LJ, Handl J, Richard J. Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Anim Feed Sci Technol. 2007;137:265-82. https://doi.org/10.1016/j.anifeedsci.2007.06.005

Sherif SO, Salama EE, Abdel-Wahhab MA. Mycotoxins and child health: The need for health risk assessment. Int J Hyg Environ Health. 2009;212(4):347-68. https://doi.org/10.1016/j.ijheh.2008.08.002 PMid:18805056

Juan C, Ritieni A, Mañes J. Determination of trichothecenes and zearalenones in grain cereal, flour and bread by liquid chromatography tandem mass spectrometry. Food Chem. 2012;134(4):2389-97. https://doi.org/10.1016/j.foodchem.2012.04.051 PMid:23442700

European Commission. Commission Regulation (EC) No 1126/2007. of 28 September 2007 Amending Regulation (EC) no 1881/2006 Setting Maximum Levels for Certain Contaminants in Foodstuffs as Regards Fusarium toxins in maize and maize products. Off J Eur Union 2007;255:14-7. https://doi.org/10.5771/9783845266466-1032-1

Wu F. Mycotoxin reduction in Bt corn: Potential economic, health, and regulatory impacts. Transgenic Res. 2006;15:277-89. https://doi.org/10.1007/s11248-005-5237-1 PMid:16779644

Prietto L, Moraes PS, Kraus RB, Meneghetti V, Fagundes CA, Furlong EB. Post-harvest operations and aflatoxin levels in rice (Oryza sativa). Crop Protect 2015;78:172-7. https://doi.org/10.1016/j.cropro.2015.09.011

Saudi Food and Drug Authority. Contaminants and Toxins in Food and Feed; 2019. Available from: https://www.resources.selerant.com/food-regulatory-news/saudi-government-publishes-a-new-draft-standard-on-contaminants-and-toxins.

AOAC Official Methods of analysis of AOAC International. Published 19thedby AOAC International Suite 500 481 North Fredrick Avenue Gaithersburg, Maryland, USA. Ch. 49. Washington: Association of Official Analytical Chemists; 2012.

Dragacci S, Grosso F, Gilbert J. Immunoaffinity column cleanup with liquid chromatography for determination of aflatoxin M1 in liquid milk: Collaborative study. J AOAC Int. 2001;84(2):437-43. https://doi.org/10.1093/jaoac/84.2.437 PMid:11324608

Deabes MM, Aboelsoud NH, Taha L. In vitro Inhibition of growth and aflatoxin B1 production of Aspergillus flavus strain (ATCC 16872) by various medicinal plant essential oils. Maced J Med Sci. 2011;4(4):345-50. https://doi.org/10.3889/mjms.1857-5773.2011.0190

Deabes MM, Darwish HR, Abdel-Aziz KB, Farag IM, Nada SA, Tewfik NS. Protective effects of Lactobacillus rhamnosus GG on aflatoxins-induced toxicities in male albino mice. J Environ Anal Toxicol. 2012;2:2-9. https://doi.org/10.4172/2161-0525.1000132

Eshak MG, Deabes MM, Farrag AH, Farag IM, Stino FK. Effect of ozone-treated aflatoxin contaminated diets on DNA damage, expression of androgen and androgen receptor genes, and histopathological changes in Japanese quail. Glob Vet. 2013;11(1):1-13.

Abou El-Soud NH, Deabes MM, Abou El-Kassem L, Khalil M. Chemical composition and antifungal activity of Ocimum basilicum L. essential oil. Maced J Med Sci. 2015;3(3):374-9. https://doi.org/10.3889/oamjms.2015.082 PMid:27275253

a. Deabes MM, Wagdy KB, Attallah AG, El-Desouky TA, Naguib K. Impact of silver nanoparticles on gene expression in Aspergillus flavus producer aflatoxin B1. Maced J Med Sci. 2018;6(4):600-5. https://doi.org/10.3889/oamjms.2018.117 PMid:297319

b. Deabes MM, Amra HA, El-Damaty EM, Rowayshed GH. Natural Co-occurrence of aflatoxins, cyclopiazonic acid, and their production by Aspergillusflavus isolates from corn grown in Egypt. Adv Clin Toxicol. 2018;3(3):1-10. https://doi.org/10.23880/act-16000136

International Conference on Harmonization. Harmonized tripartite guideline, validation of analytical procedures, text and methodology. Geneva, Switzerland: International Conference on Harmonization; 2006. p. 12e4. https://doi.org/10.1007/springerreference_83218

NATA Technical Note 17. Guidelines for the Validation and Verification of Quantitative and Qualitative Test Methods. Australia: National Association of Testing Authorities. 2013. p. 17-8.

IBM Corp. IBM SPSS Statistics for Windows, Version 22.0. Armonk, NY: IBM Corp; 2013.

Scott PM, Lawrence GA. Determination of aflatoxins in beer. J AOAC Int. 1997;80(6):1229-34. PMid:9419863

Stroka J, Anklam E. New strategies for the screening and determination of aflatoxins and the detection of aflatoxin-producing moulds in food and feed. Trends Anal Chem. 2002;21(2):90-5. https://doi.org/10.1016/s0165-9936(01)00133-9

Stoloff L. Aflatoxins an overview. In: Rodricks JV, Hesseltine CW, Mehlman MA, editors. Mycotoxins in Human and Animal Health. Park Forest South, Illinois: Pathotos Publishers; 1977. p. 7-28.

Shank RC, Gordon JE, Wogan GN, Nondasuta A, Subhamani B. Dietary aflatoxins and human liver cancer. III. Field survey of rural Thai families for ingested aflatoxins. Food Cosmet Toxicol 1972;10:71-84. https://doi.org/10.1016/s0015-6264(72)80048-8

Krishnamachari KA, Bhat RV, Nagarajan V, Tilak TB. Investigations into an outbreak of hepatitis in parts of Western India. Indian J Med Res. 1975;63(7):1036-48. PMid:1213790

Turner PC, Mendy M, White H, Fortuin M, Hall AJ, Wild CP. Hepatitis B infection and aflatoxin biomarker levels in Gambian children. Trop Med Int Health. 2000;5(12):837-41. https://doi.org/10.1046/j.1365-3156.2000.00664.x PMid:11169271

European Food Safety Authority. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to the potential increase of consumer health risk by a possible increase of the existing maximum levels for aflatoxins in almonds, hazelsnuts and pistachios and derived products. EFSA J. 2007;446:1-127. https://doi.org/10.2903/j.efsa.2007.446

Turner PC, Sylla A, Diallo MS, Castegnaro JJ, Hall AJ, Wild CP. The role of aflatoxins and hepatitis viruses in the etiopathogenesis of hepatocellular carcinoma: A basis for primary prevention in Guinea Conakry, West Africa. J Gastroent Hep. 2002;17:441-8. https://doi.org/10.1046/j.1440-1746.17.s4.7.x PMid:12534775

Turner PC, Moore SE, Hall AJ, Prentice AM, Wild CP. Modification of immune function through exposure to dietary aflatoxin in Gambian children. Environ Health Pers. 2003;111:217-20. https://doi.org/10.1289/ehp.5753

Luttfullah G, Hussain A. Studies on contamination level of aflatoxins in some dried fruits and nuts of Pakistan. Food Control. 2011;22:426-9. https://doi.org/10.1016/j.foodcont.2010.09.015

Mojtahedi H, Rabie CJ, Lubben A, Steyn M, Danesh D. Toxic aspergilli from pistachio nuts. Mycopathol. 1979;67(2):123-7. PMid:481560

Pittet A. Natural occurrence of mycotoxins in foods and feeds-an updated review. Rev Med Vet. 1998;149:479-92.

Abdel-Hafez, A 2nd, Saber SM. Mycoflora and mycotoxin of hazelnut (Corylus avellana L.) and walnut (Juglans regia L.) seeds in Egypt. Zentralblatt Mikrobiol. 1993;148:137-47. https://doi.org/10.1016/s0232-4393(11)80117-4

Singh PK, Shukla AN. Survey of mycoflora counts, aflatoxin production and induced biochemical changes in walnut kernels. J Stored Prod Res. 2008;44:169-72. https://doi.org/10.1016/j.jspr.2007.10.001

Denning DW. Aflatoxin and human diseases. In: Davies DM, deGlanville H, editors. Adverse Drug Reactions and Acute Poisoning Reviews. Vol. 4. Oxford, UK: Oxford University Press; 1987. p. 175-209.

Payne GA, Hagler WM, Adkins CR. Aflatoxin accumulation in inoculated ears of field-grown maize. Plant Dis. 1998;72:422-4. https://doi.org/10.1094/pd-72-0422

Payne GA. Aflatoxin in maize. Crit Rev Plant Sci. 1992;10(5):423-40.

Rachaputi NR, Wright GC, Kroschi S. Management practices to minimise pre-harvest aflatoxin contamination in Australian groundnuts. Austr J Exp Agric. 2002;42:595-605. https://doi.org/10.1071/ea01139

Temba MC, Njobeh PB, Kayitesi E. Storage stability of maize groundnut composite flours and an assessment of aflatoxin B1 and ochratoxin a contamination in flours and porridges. Food Control. 2017;71:178-86. https://doi.org/10.1016/j.foodcont.2016.06.033

Martinez-Miranda MM, Rosero-Moreano M, Taborda-Ocampo G. Occurrence, dietary exposure and risk assessment of aflatoxins in arepa, bread and rice. Food Control. 2019;98:359-66. https://doi.org/10.1016/j.foodcont.2018.11.046

Andrade PD, Caldas ED. Aflatoxins in cereals: Worldwide occurrence and dietary risk assessment. World Mycotoxin J. 2015;8:415-31. https://doi.org/10.3920/wmj2014.1847

Tanaka K, Sago Y, Zheng Y, Nakagawa H, Kushiro M. Mycotoxinsin rice. Int J Food Microbiol. 2007;119(1-2):59-66. PMid:17913273.

Palumbo R, Crisci A, Venâncio A, Abrahantes JC, Dorne JL, Battilani P, et al. Occurrence and co-occurrence of mycotoxins in cereal-based feed and food microorganisms. Microorganisms. 2020;8:741-17. https://doi.org/10.3390/microorganisms8010074 PMid:31947721

Atanda SA, Pessu PO, Agoda S, Isong IU, Adekalu OA, Echendu MA. Fungi and mycotoxins in stored foods. Afr J Microbiol Res. 2011;5(25):4373-82. https://doi.org/10.5897/ajmr11.487

Smith LE, Stasiewicz M, Hestrin R, Morales L, Mutiga S, Nelson RJ. Examining environmental drivers of spatial variability in aflatoxin accumulation in Kenyan maize: Potential utility in risk prediction models. Afr J Food Agric Nutr Dev. 2016;16(3):11086-5. https://doi.org/10.18697/ajfand.75.ilri09

Reiter E, Vouk F, Bohm J, Razzazi-Fazeli E. Aflatoxins in rice a limited survey of products marketed in Austria. Food Control. 2010;21:988-91. https://doi.org/10.1016/j.foodcont.2009.12.014

Sarker M, Ibrahim M, Aziz N, Punan M. Application of simulation in determining suitable operating parameters for industrial scale fluidized bed dryer during drying of high impurity moist paddy. J Stored Prod Res. 2015;61:76-84. https://doi.org/10.1016/j.jspr.2014.12.004