Mycotoxins in Ethiopia: A Review on Prevalence, Economic and Health Impacts
Abstract
:1. Introduction
2. Mycotoxigenic Fungi and Growth Conditions
3. Agro-Ecology, Climate, and Storage Conditions in Ethiopia
4. Occurrence of Mycotoxigenic Fungi and Their Toxins in Ethiopia
Commodity | Location | Year of Study | Number of Sample (n) | Major Fungi Identified (Incidence; % or CFU/g) | Mycotoxin | Range or Mean (µg/kg or μg/l) | Positive Samples (%) | Test | Detections Limit (µg/kg) or LOD/LOQ | Incidence beyond EU Maximum Limit (%), (µg/kg) | Authors |
---|---|---|---|---|---|---|---|---|---|---|---|
Maize | Dire Dawa, Adama, Ambo | 2004/2005 | 17 | Aspergillus (94%), Fusarium (76.5%), Penicillium (64%) | Total AFs | <5–27 | 88 | ELISA | 1.75 | 5.8 (10) | [23] |
Groundnut | Babile, Darolabu, Gursum | 2013 | 120 | - | Total AFs | 15–11,900 | 93 | ELISA | - | 93 (4) | [24] |
Maize | SNNP Region | 2016 | 150 | Aspergillus (75%), Fusarium (11%), Penicillium (8%), Trichoderma (6%) | Total AFs | 20–91.4 | 100 | TLC | - | 100 (10) | [53] |
Locally brewed beers | Addis Ababa | 2015/2016 | 18 | - | Total AFs | 1.23–12.47 | 92 | HPLC | - | 16.7 (4) | [54] |
Sorghum | Babile, Kersa. Haramaya | 2013 | 45 | Aspergillus (1–2.5 log cfu/g) Fusarium (0.5–1.3 log cfu/g) | AFB1 | ND-33.1 | 94 | ELISA | 0.01–0.03 | 13.3 (10) | [47] |
Total FUMs | 907–2041 | 71.1 | 0.01–0.03 | 2.22 (1000) | |||||||
Maize | Major growing areas | 2011/2012 | 200 | - | Total FUMs | 25–4500 | 77 | ELISA | 0.025 | 7 (1000) | [55] |
Sorghum | North Showa Zone of Amhara region state | 2016 | 30 | A.flavus (56.7%), A.niger (16.7%), A.parasiticus (23.3%) | Total AFs | 11.44–344.26 | HPLC | - | 100 (4) | [49] | |
AFB1 | 3.95–153.72 | 96.66 | |||||||||
AFB2 | 1.17–91.82 | 93.33 | |||||||||
AFG1 | 9.87–139.64 | 96.7 | |||||||||
AFG2 | 3.22–52.02 | 90 | |||||||||
Wheat | Wenberma, Merawi, Ofla, Hetosa, Gedeb, Lemo. | 2016 | 179 | - | Total AFs | 2.5–16.7 | 60. | LFIA | 2 | 50.8 (4) | [52] |
Total FUM | 330–710 | 16.2 | 250 | - | |||||||
OTA | 2.1–148.8 | 20.1 | 2 | 4.5 (4) | |||||||
Maize | West showa and east wallega zones | 2019 | 90 | Aspergillus (50.7%), Fussarium(26.4%), Penicillium(22.3%) Trichoderma(1.07%) | AFB1 | 3.9–381.6 | 34.4 | ELISA | - | 7.7 (5) | [45] |
Pre-milling ingredients | Amhara, Tigray, Oromia, SNNP | 2018 | 126 | - | Total AFs | 4.57–3.50 | 64.3 | ELISA | - | >2.3% (4) | [56] |
Complementary foods | 3.7–7.1 | ||||||||||
Maize | South and southwestern Ethiopia | 2015 | 100 | Penicillium (80%), Aspergillus (75%) Fusarium (60%) | AFB1 | 9.3 | 8 | LC-MS/MS | 0.3 | [33] | |
AFB2 | 34 | 3 | 0.4 | ||||||||
AFG1 | 64 | 6 | 0.3 | ||||||||
AFG2 | 21 | 2 | 0.4 | ||||||||
AFM1 | 18 | 2 | 0.3 | ||||||||
FB1 | 606 | 70 | 3.2 | - | |||||||
FB2 | 202 | 62 | 2.4 | - | |||||||
FB3 | 136 | 51 | 2.4 | - | |||||||
FB4 | 85 | 60 | 2.4 | - | |||||||
FA1 | 37 | 34 | 2.4 | - | |||||||
FA2 | 32 | 35 | 2.4 | - | |||||||
ZEN | 92 | 96 | 0.12 | 13.5 (100) | |||||||
DON | 221 | 42 | 1.2 | - | |||||||
NIV | 91 | 45 | 1.2 | - | |||||||
Teff flour | Addis Ababa city | 2017 | 60 | - | OTA | 2 | 20 | HPLC | 0.78 | 3.3 (3) | [57] |
Wheat flour | 7.3 | 50 | 0.58 | 26.7 (3) | |||||||
Coffee | Jima zone | 2014–2016 | 75 | Aspergillus (79%), Fusarium (8%), Penicillium (5%) | OTA | 0.03–22.9 | 64 | ELISA | 1.9/2 (µg/L) | 5.5 (5) | [58] |
Groundnut | Babile, Darolabu, Fedis, Gursum | 2013–2015 | 160 | Aspergillus (70–100%) A. flavus, A. parasiticus, A. caelatus, A. niger, A. tamari, A. ochraceus | AFB1 | ND-2526 | 32 | UPLC | 1 (B1, G1) 0.05 (B2, G2) | - | [25] |
AFB2 | ND-237 | ||||||||||
AFG1 | ND-736 | ||||||||||
AFG2 | ND-171 | ||||||||||
Maize | West Gojjam | 2015 | 30 | Aspergillus (53.3–80%), A. flavus, A. parasiticus, A. niger | AFB1 | 7.43 | 78.7 | HPLC | 0.03 | 50 (4) | [50] |
AFB2 | 4.19 | 0.3 | |||||||||
AFG1 | 14.1 | 0.014 | |||||||||
AFG2 | 6.17 | 0.15 | |||||||||
Total AFs | 30.9 |
5. Public Health Impacts of Mycotoxins in Ethiopia
6. Early Age Mycotoxins Exposure and Malnutrition in Ethiopia
7. Mycotoxins and Their Economic Impacts in Ethiopia
8. Mycotoxins and Their Impacts on Livestock Production in Ethiopia
9. Mycotoxins Regulation in Ethiopia
10. Analysis of Mycotoxins in Ethiopia
11. Raising Awareness and Adulteration Practices in Ethiopia
12. Mycotoxin Management Strategies
13. Conclusions and Recommendations
Funding
Acknowledgments
Conflicts of Interest
References
- Frisvad, J.C.; Thrane, U.; Samson, R.A.; Pitt, J.I. Important mycotoxins and the fungi which produce them. In Advances in Experimental Medicine and Biology; Hocking, A.D., Pitt, J.I., Samson, R.A., Thrane, U., Eds.; Springer Science and Business Media: New York, NY, USA, 2006; pp. 3–31. ISBN 9780387283852. [Google Scholar]
- Marta, T.; Kebede, B. Occurrence, Importance and Control of Mycotoxins: A review. Cogent Food Agric. 2016, 2, 1–26. [Google Scholar] [CrossRef]
- Hocking, A.; Pitt, J. Food, fungi and mycotoxins: An update. Mycology 2011, 32, 5–8. [Google Scholar]
- Milićević, D.R.; Škrinjar, M.; Baltić, T. Real and perceived risks for mycotoxin contamination in foods and feeds: Challenges for food safety control. Toxins (Basel) 2010, 2, 572–592. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- IARC (International Agency for Research on Cancer). Mycotoxin Control in Low- and Middle Income Countries; Wild, C.P., Miller, J.D., Groopman, J.D., Eds.; IARC Press: Lyon, France, 2015. [Google Scholar]
- Zain, M.E. Impact of mycotoxins on humans and animals. J. Saudi Chem. Soc. 2011, 15, 129–144. [Google Scholar] [CrossRef] [Green Version]
- Watson, S.; Moore, S.E.; Darboe, M.K.; Chen, G.; Tu, Y.; Huang, Y.; Eriksen, K.G.; Bernstein, R.M.; Prentice, A.M.; Wild, C.P.; et al. Impaired growth in rural Gambian infants exposed to aflatoxin: A prospective cohort study. BMC Public Health 2018, 18, 1–9. [Google Scholar] [CrossRef]
- Bhat, R.; Rai, R.V.; Karim, A.A. Mycotoxins in Food and Feed: Present Status and Future Concerns. Compr. Rev. Food Sci. Food Saf. 2010, 9, 57–81. [Google Scholar] [CrossRef]
- Udomkun, P.; Wiredu, A.N.; Nagle, M.; Bandyopadhyay, R.; Müller, J.; Vanlauwe, B. Mycotoxins in Sub-Saharan Africa: Present situation, socio-economic impact, awareness, and outlook. Food Control 2017, 72, 110–122. [Google Scholar] [CrossRef]
- CAST (Council for Agricultural Science and Technology). Mycotoxins: Risks in PLANT, Animal, and Human Systems; Bhatnagar, D., Bryden, W., de Koe, W., Gilbert, J., Pohland, A.E., Eds.; Council for Agricultural Science and Technology Press: Ames, IA, USA, 2003; Available online: www.cast-science.org (accessed on 15 June 2016).
- Neme, K.; Mohammed, A. Mycotoxin occurrence in grains and the role of postharvest management as a mitigation strategies: A review. Food Control 2017, 78, 412–425. [Google Scholar] [CrossRef]
- OECD/FAO. Agriculture in Sub-Saharan Africa: Prospects and challenges for the next decades. In OECD-FAO Agricultural Outlook 2016–2025; OECD Publishing: Paris, France, 2016; pp. 59–95. [Google Scholar]
- Darwish, W.S.; Ikenaka, Y.; Nakayama, S.M.M.; Ishizuka, M. An Overview on Mycotoxin Contamination of Foods in Africa. J. Vet. Med. Sci. 2014, 76, 789–797. [Google Scholar] [CrossRef] [Green Version]
- Kebede, H.; Liu, X. Current status of major mycotoxins contamination in food and feed in Africa. Food Control 2020, 110, 106975. [Google Scholar] [CrossRef]
- Liu, Y.; Wu, F. Global burden of Aflatoxin-induced hepatocellular carcinoma: A risk assessment. Environ. Health Perspect. 2010, 118, 818–824. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Paterson, R.R.M.; Lima, N. How will climate change affect mycotoxins in food? Food Res. Int. 2010, 43, 1902–1914. [Google Scholar] [CrossRef] [Green Version]
- Beyene, A.A.; Woldegiorgis, A.Z.; Adish, A.A.; De Saeger, S.; Tolossa, A.L. Assessment of mothers’ knowledge and practice towards aflatoxin contamination in complementary foods in Ethiopia: From pre-harvest to household. World Mycotoxin J. 2016, 9, 535–544. [Google Scholar] [CrossRef]
- Matouš, P.; Todo, Y.; Mojo, D. Roles of extension and ethno-religious networks in acceptance of resource-conserving agriculture among Ethiopian farmers. Int. J. Agric. Sustain. 2013, 11, 301–316. [Google Scholar] [CrossRef]
- World Bank. Integrated Surveys on Agriculture Ethiopia Socioeconomic Survey (ESS); World Bank: Washington, DC, USA, 2017; Available online: https://www.worldbank.org (accessed on 28 July 2018).
- FAO. Small Family Farms Country Factsheet: Ethiopia; FAO: Rome, Italy, 2018; Available online: www.fao.org/ (accessed on 14 May 2018).
- FAO. The Economic Lives of Smallholder Farmers; An Analysis Based on Household Data from Nine Countries; FAO: Rome, Italy, 2015; Available online: www.fao.org/publications (accessed on 17 May 2018).
- Besrat, A.; Gebre, P. A preliminary study on the aflatoxin content of selected Ethiopian foods. Ethiop. Med. J. 1981, 19, 47–52. [Google Scholar]
- Ayalew, A. Mycotoxins and Surface and Internal Fungi of Maize From Ethiopia. Afr. J. Food Agric. Nutr. Dev. 2010, 10, 76–99. [Google Scholar] [CrossRef]
- Chala, A.; Mohammed, A.; Ayalew, A.; Skinnes, H. Natural occurrence of aflatoxins in groundnut (Arachis hypogaea L.) from eastern Ethiopia. Food Control 2013, 30, 602–605. [Google Scholar] [CrossRef]
- Mohammed, A.; Chala, A.; Dejene, M.; Fininsa, C.; Hoisington, D.A.; Sobolev, V.S.; Arias, R.S. Aspergillus and aflatoxin in groundnut (Arachis hypogaea L.) and groundnut cake in Eastern Ethiopia. Food Addit. Contam. Part B Surveill. 2016, 9, 290–298. [Google Scholar] [CrossRef] [Green Version]
- Ayelign, A.; De Saeger, S. Mycotoxins in Ethiopia: Current status, implications to food safety and mitigation strategies. Food Control 2020, 113, 107163. [Google Scholar] [CrossRef]
- Pitt, J.I.; Hocking, A.D. Fungi and Food Spoilage, 3rd ed.; Springer Science and Business Media: New York, NY, USA, 2009; ISBN 9780387922065. [Google Scholar]
- Greeff-laubscher, M.R.; Beukes, I.; Marais, G.J. Mycotoxin production by three different toxigenic fungi genera on formulated abalone feed and the effect of an aquatic environment on fumonisins. Mycology 2020, 11, 105–117. [Google Scholar] [CrossRef] [Green Version]
- Aldars-garcía, L.; Berman, M.; Ortiz, J.; Ramos, A.J.; Marín, S. Probability models for growth and a flatoxin B1 production as affected by intraspecies variability in Aspergillus flavus. Food Microbiol. J. 2018, 72, 166–175. [Google Scholar] [CrossRef] [Green Version]
- Pettersson, O.V.; Leong, S.L. Fungal Xerophiles (Osmophiles). In Encyclopedia of Life Science, eLS (Microbiology); John Wiley & Sons, Ltd.: Chichester, UK, 2011; pp. 1–9. [Google Scholar] [CrossRef]
- Agriopoulou, S.; Stamatelopoulou, E.; Varzakas, T. Advances in Occurrence, Importance, and Mycotoxin Control Strategies: Prevention and Detoxification in Foods. Foods 2020, 137, 137. [Google Scholar] [CrossRef] [PubMed]
- Benkerroum, N. Aflatoxins: Producing-Molds, Structure, Health Issues and Incidence in Southeast Asian and Sub-Saharan African Countries. Int. J. Environ. Res. Public Health 2020, 17, 1215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Getachew, A.; Chala, A.; Hofgaard, I.S.; Brurberg, M.B.; Sulyok, M.; Tronsmo, A.M. Multimycotoxin and fungal analysis of maize grains from south and southwestern Ethiopia. Food Addit. Contam. Part B Surveill. 2018, 11, 64–74. [Google Scholar] [CrossRef] [PubMed]
- Frisvad, J.C.; Hubka, V.; Ezekiel, C.N.; Nov, A.; Chen, A.J.; Arzanlou, M.; Larsen, T.O.; Sklen, F.; Mahakarnchanakul, W.; Samson, R.A.; et al. Taxonomy of Aspergillus section Flavi and their production of aflatoxins, ochratoxins and other mycotoxins. Stud. Mycol. 2019, 63, 1–63. [Google Scholar] [CrossRef]
- Malir, F.; Ostry, V.; Pfohl-leszkowicz, A.; Malir, J.; Toman, J. Ochratoxin A: 50 Years of Research. Toxins (Basel) 2016, 8, 191. [Google Scholar] [CrossRef] [Green Version]
- Belizán, M.; Gomez, A.; Baptista Terán, Z.; Jimenez, C.; Sánchez Matías, M.; Catalán, C.; Sampietro, D. Influence of water activity and temperature on growth and production of trichothecenes by Fusarium graminearum sensu stricto and related species in maize grains. Int. J. Food Microbiol. 2019, 305, 108242. [Google Scholar] [CrossRef]
- Perincherry, L.; Lalak-Kańczugowska, J.; Stępień, Ł. Fusarium-Produced Mycotoxins in Plant-Pathogen Interactions. Toxins (Basel) 2019, 11, 664. [Google Scholar] [CrossRef] [Green Version]
- Mamo, B.E.; Steffenson, B.J. Genome-wide Association Mapping of Fusarium Head Blight Resistance and Agromorphological Traits in Barley Landraces from Ethiopia and Eritrea. Crop Sci. 2015, 55, 1494–1512. [Google Scholar] [CrossRef]
- Mitiku, M.; Eshete, Y. Assessment of Wheat Diseases in South Omo Zone of Ethiopia. Sci. Res. 2016, 4, 183–186. [Google Scholar] [CrossRef]
- MOE (Ministry of Agriculture). Agro-Ecological Zones of Ethiopia; MOE: Addis Ababa, Ethiopia, 1998. Available online: http://www.moa.gov.et/web/guest/resources (accessed on 2 March 2018).
- Deressa, T.T. Measuring the Economic Impact of Climate Change on Ethiopian Agriculture: Ricardian Approach; World Bank: Washington, DC, USA, 2007; Available online: https://documents.worldbank.org/en/publication/documentsreports/documentdetail/143291468035673156/ (accessed on 1 July 2020).
- CSA. Area and Production of Major Crops in Ethiopia (2017/18); CSA: Addis ababa, Ethiopia, 2018; Volume I. Available online: www.csa.gov.et (accessed on 17 June 2018).
- Kuyu, C.G. Review on contribution of indigenous food preparation and preservation techniques to attainment of food security in Ethiopian. Food Sci. Nutr. 2020, 8, 3–15. [Google Scholar] [CrossRef] [PubMed]
- Tesfaye, W.; Tirivayi, N. The impacts of postharvest storage innovations on food security and welfare in Ethiopia. Food Policy 2018, 75, 52–67. [Google Scholar] [CrossRef]
- Yilma, S.; Sadessa, K.; Kebede, D. Fungal Infections and Aflatoxin Contamination in Maize Grains Collected from West Showa and East Wallega. Int. J. Curr. Res. Rev. 2019, 11, 16–22. [Google Scholar] [CrossRef]
- EC. European Commission, amending Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in foodstuffs as regards aflatoxins. Off. J. Eur. Union 2010, 165, 8–12. [Google Scholar]
- Taye, W.; Ayalew, A.; Chala, A.; Dejene, M. Aflatoxin B1 and total fumonisin contamination and their producing fungi in fresh and stored sorghum grain in East Hararghe, Ethiopia. Food Addit. Contam. Part B Surveill. 2016, 9, 237–245. [Google Scholar] [CrossRef]
- EC. 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, 1126, 14–17. [Google Scholar]
- Geremew, W.; Bekele, T.; Zewdu, A.; Fekadu, H. Study on Aspergillus Species and Aflatoxin Levels in Sorghum (Sorghum bicolor L.) Stored for Different Period and Storage System in Kewet Districts, Northern Shewa, Ethiopia. J. Food Sci. Nutr. 2016, 2, 1–8. [Google Scholar] [CrossRef]
- Assaye, M.A.; Gemeda, N.; Weledesemayat, G.T. Aspergillus species and Aflatoxin Contamination of Pre and Post-Harvest Maize Grain in West Gojam, Ethiopia. J. Food Sci. Nutr. 2016, 2, 1–7. [Google Scholar] [CrossRef]
- Mohammed, A.; Chala, A. Incidence of Aspergillus contamination of groundnut (Arachis hypogaea L.) in Eastern Ethiopia. Afr. J. Microbiol. Res. 2014, 8, 759–765. [Google Scholar] [CrossRef]
- Worku, A.; Merkuz, A.; Kalsa, K.; Tenagashaw, M.; Habtu, N. Occurrence of Mycotoxins in farm-Stored Wheat in Ethiopia. Afr. J. Agric. Nutr. Dev. 2019, 19, 14829–14847. [Google Scholar] [CrossRef]
- Chauhan, N.M.; Washe, A.P.; Minota, T. Fungal infection and aflatoxin contamination in maize collected from Gedeo zone, Ethiopia. Springerplus 2016, 5, 753. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nigussie, A.; Bekele, T.; Fekadu Gemede, H.; Zewdu Woldegiorgis, A. Level of aflatoxins in industrially brewed local and imported beers collected from Ethiopia market. Cogent Food Agric. 2018, 4, 1–13. [Google Scholar] [CrossRef]
- Tsehaye, H.; Brurberg, M.B. Natural occurrence of Fusarium species and fumonisin on maize grains in Ethiopia. Eur. J. Plant Pathol. 2016, 147, 141–155. [Google Scholar] [CrossRef]
- Ayelign, A.; Woldegiorgis, A.Z.; Adish, A.; De Saeger, S. Total aflatoxins in complementary foods produced at community levels using locally available ingredients in Ethiopia. Food Addit. Contam. Part B Surveill. 2018, 11, 111–118. [Google Scholar] [CrossRef]
- Geremew, T.; Haesaert, G.; Abate, D.; Audenaert, K. An HPLC-FLD method to measure ochratoxin A in teff (Eragrostis tef) and wheat (Triticum spp.) destined for the local Ethiopian market. World Mycotoxin J. 2017, 11, 359–368. [Google Scholar] [CrossRef]
- Geremew, T.; Abate, D.; Landschoot, S.; Haesaert, G.; Audenaert, K. Occurrence of toxigenic fungi and ochratoxin A in Ethiopian coffee for local consumption. Food Control 2016, 69, 65–73. [Google Scholar] [CrossRef]
- Chala, A.; Taye, W.; Ayalew, A.; Krska, R.; Sulyok, M.; Logrieco, A. Multimycotoxin analysis of sorghum (Sorghum bicolor L. Moench) and finger millet (Eleusine coracana L. Garten) from Ethiopia. Food Control 2014, 45, 29–35. [Google Scholar] [CrossRef]
- Yabe, K.; Chihaya, N.; Hatabayashi, H.; Kito, M.; Hoshino, S.; Zeng, H.; Cai, J.; Nakajima, H. Production of M-/GM-group aflatoxins catalyzed by the OrdA enzyme in aflatoxin biosynthesis. Fungal Genet. Biol. 2012, 49, 744–754. [Google Scholar] [CrossRef]
- Abdallah, M.F.; Girgin, G.; Baydar, T. Occurrence of multiple mycotoxins and other fungal metabolites in animal feed and maize samples from Egypt using LC-MS/MS. Sci. Food Agric. 2017, 97, 4419–4428. [Google Scholar] [CrossRef]
- Sulyok, M.; Beed, F.; Boni, S.; Abass, A.; Mukunzi, A.; Krska, R. Quantitation of multiple mycotoxins and cyanogenic glucosides in cassava samples from Tanzania and Rwanda by an LC-MS/MS-based multi-toxin method. Food Addit. Contam. Part A 2014, 32, 37–41. [Google Scholar] [CrossRef]
- Fufa, H.; Urga, K. Screening of aflatoxins in Shiro and ground red pepper in Addis Ababa. Ethiop. J. Heal. Sci. 1996, 34, 243–249. [Google Scholar]
- Ayalew, A.; Fehrmann, H.; Lepschy, J.; Beck, R.; Abate, D. Natural occurrence of mycotoxins in staple cereals from Ethiopia. Mycopathologia 2006, 162, 57–63. [Google Scholar] [CrossRef] [PubMed]
- Bui-klimke, T.R.; Wu, F. Ochratoxin A and human health risk: A review of the evidence. Crit. Rev. Food Sci. Nutr. 2016, 55, 1860–1869. [Google Scholar] [CrossRef] [Green Version]
- IARC (International Agency for Research on Cancer). Evaluation of Carcinogenic Risks to Humans; Some Traditional Herbal Medicines, Some Mycotoxins, Naphthalene and Styrene; IARC Press: Lyon, France, 2002. [Google Scholar]
- Biru, T.G.; Tassew, D.A. Association of Coffee Bean Defects with Ochratoxin A Contamination in the Samples. Ethiop. J. Sci. Sustain. Dev. 2019, 6, 68–78. [Google Scholar]
- Behnke, R.; Metaferia, F. The Contribution of Livestock to the Ethiopian Economy—Part II; Working Paper No. 02–11; Inter-Governmental Authority on Development: Nairobi, Kenya, 2013. [Google Scholar]
- Petit, N. Ethiopia’s Coffee Sector: A Bitter or Better Future? J. Agrar. Chang. 2007, 7, 225–263. [Google Scholar] [CrossRef]
- Tefera, A. Ethiopia Coffee Annual Report; GAIN Report Number: ET1514; Global Agricultural Information Network: Addis Ababa, Ethiopia, 2015. [Google Scholar]
- Palumbo, R.; Crisci, A.; Ven, A.; Abrahantes, C.; Dorne, J.; Battilani, P.; Toscano, P. Occurrence and Co-Occurrence of Mycotoxins in Cereal-Based Feed and Food. Microorganisms 2020, 8, 74. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- CDC. Outbreak of Aflatoxin Poisoning Eastern and Central Provinces, Kenya, January–July 2004; CDC: Atlanta, GA, USA, 2004; Volume 53. [Google Scholar]
- Probst, C.; Njapau, H.; Cotty, P.J. Outbreak of an acute aflatoxicosis in Kenya in 2004: Identification of the causal agent. Appl. Environ. Microbiol. 2007, 73, 2762–2764. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mupunga, I.; Mngqawa, P.; Katerere, D.R. Peanuts, aflatoxins and undernutrition in children in Sub-Saharan Africa. Nutrients 2017, 9, 1287. [Google Scholar] [CrossRef] [Green Version]
- Okoth, S. Improving the Evidence Base on Aflatoxin Contamination and Exposure in Africa; The Technical Centre for Agricultural and Rural Cooperation, CTA: Wageningen, The Netherlands, 2016. [Google Scholar]
- Aydın, M.; Aydın, S.; Bacanlı, M.; Basaran, N. Aflatoxin levels in chronic hepatitis B patients with cirrhosis or hepatocellular carcinoma in Balıkesir, Turkey. J. Viral Hepat. 2015, 22, 926–935. [Google Scholar] [CrossRef]
- Chu, Y.; Yang, H.; Wu, H.; Liu, J.; Wang, L.; Lu, S.; Lee, M.; Jen, C.; You, S.; Santella, R.M.; et al. Aflatoxin B1 exposure increases the risk of cirrhosis and hepatocellular carcinoma in chronic hepatitis B virus carriers. Int. J. Cancer 2017, 141, 711–720. [Google Scholar] [CrossRef] [Green Version]
- Shimelis, T.; Torben, W.; Medhin, G.; Tebeje, M.; Andualm, A.; Demessie, F.; Mulu, A.; Tegbaru, B. Hepatitis B virus infection among people attending the voluntary counselling and testing centre and anti-retroviral therapy clinic of St Paul’s General Specialised Hospital, Addis Ababa, Ethiopia. Epidemiology 2008, 84, 37–41. [Google Scholar] [CrossRef] [PubMed]
- Magnus, S.; Orlien, S.; Ismael, N.Y.; Ahmed, T.A.; Berhe, N.; Lauritzen, T.; Roald, B.; Goldin, R.D.; Stene-johansen, K.; Dyrhol-riise, A.M. Unexplained chronic liver disease in Ethiopia: A cross-sectional study. BMC Gastroenterol. 2018, 18, 27. [Google Scholar]
- Serag, H.B.E.L.; Rudolph, K.L. Reviews in basic and clinical gastroenterology. Gastroenterology 2007, 132, 2557–2576. [Google Scholar] [CrossRef] [PubMed]
- Come, J.; Cambaza, E.; Ferreira, R.; da Costa, J.M.C.; Carrilho, C.; Santos, L.L. Esophageal cancer in Mozambique: Should mycotoxins be a concern? Pan Afr. Med. J. 2019, 8688, 1–6. [Google Scholar] [CrossRef]
- Braun, M.S.; Michael, W. Exposure, Occurrence, and Chemistry of Fumonisins and their Cryptic Derivatives. Compr. Rev. Food Sci. Food Saf. 2018, 17, 769–791. [Google Scholar] [CrossRef] [Green Version]
- Bulcha, G.G.; Leon, M.E.; Gwen, M.; Abnet, C.C.; Sime, A.; Pritchett, N.R.; Dawsey, S.M. Epidemiology of Esophageal Cancer (EC) in Oromia Region, Ethiopia 2016: A 4-Year Medical Record Review. J. Glob. Oncol. 2018, 4, 1–14. [Google Scholar] [CrossRef]
- Shewaye, A.B.; Seme, A. Risk Factors Associated with Oesophageal Malignancy among Ethiopian Patients: A Case Control Study. East Cent. Afr. J. Surg. 2016, 21, 33–39. [Google Scholar] [CrossRef]
- Ishikawa, A.T.; Takabayashi-Yamashita, C.R.; Ono, E.Y.S.; Bagatin, A.K.; Rigobello, F.F.; Kawamura, O.; Hirooka, E.Y.; Itano, E.N. Exposure Assessment of Infants to Aflatoxin M1 through Consumption of Breast Milk and Infant. Toxins (Basel) 2016, 8, 246. [Google Scholar] [CrossRef] [Green Version]
- Lombard, M.J. Mycotoxin exposure and infant and young child growth in Africa: What do we know? Ann. Nutr. Metab. 2014, 64, 42–52. [Google Scholar] [CrossRef]
- Lauer, J.M.; Natamba, B.K.; Ghosh, S.; Webb, P.; Wang, J.; Griffiths, J.K. Aflatoxin exposure in pregnant women of mixed status of human immunodeficiency virus infection and rate of gestational weight gain: A Ugandan cohort study. Trop. Med. Int. Health 2020, 25, 1145–1154. [Google Scholar] [CrossRef]
- Khlangwisetl, P.; Shephard, G.S.; Wui, F. Aflatoxins and growth impairment: A review. Informa 2011, 41, 740–755. [Google Scholar] [CrossRef]
- Ayelign, A.; Woldegiorgis, A.; Adish, A.; De Boevre, M.; Heyndrickx, E.; De Saeger, S. Assessment of aflatoxin exposure among young children in Ethiopia using urinary biomarkers. Food Addit. Contam.Part A Chem. Anal. Control. Expo. Risk Assess. 2017, 34, 1606–1616. [Google Scholar] [CrossRef] [PubMed]
- Central Statistical Agency (CSA); ICF. Ethiopia Demographic and Health Survey 2016; CSA: Addis Ababa, Ethiopia; ICF: Rockville, MD, USA, 2016; Available online: https://microdata.worldbank.org/ (accessed on 17 April 2018).
- Rapid Alert System for Food and Feed (RASFF). EU Rapid Alert System for Food and Feed. Available online: https://webgate.ec.europa.eu/rasff-window/porta (accessed on 20 August 2020).
- Ethiopian Capital News Letter Ethiopia to Use Aflasafe Technology to Reduce Aflatoxin in Red Pepper. Available online: https://www.capitalethiopia.com/capital/ethiopia-use-aflasafe-technology-reduce-aflatoxin-red-pepper (accessed on 16 July 2018).
- ENTAG. Reopening the European Spice Market for Ethiopian Exporters; ENTAG: Addis Ababa, Ethiopia, 2018; Available online: http://entag.org/ (accessed on 20 July 2019).
- Worku, A.; Fentahun, T. Aflatoxin Related Challenges and Mitigation Strategies of Ethiopia in Spices, Herbs and Pulses, Domestic and International Markets; Ethio- Netherland Trade for Agricultural Growth: Addis Ababa, Ethiopia, 2018; Available online: http://entag.org/ (accessed on 20 July 2019).
- The Reporter News Spice Exporters Fear Losing EU Markets. Available online: https://www.thereporterethiopia.com/content/spice-exporters-fear-losing-eu-markets (accessed on 12 August 2017).
- Lloyd, J.; Teshome, B. Foreign Exchange Allocation and Access for Businesses in Ethiopia; UK Aid: Addis Ababa, Ethiopia, 2018. Available online: https://www.gov.uk/dfid-research-outputs/ (accessed on 20 July 2019).
- Leta, S.; Mesele, F. Spatial analysis of cattle and shoat population in Ethiopia: Growth trend, distribution and market access. Research 2014, 3, 1–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shapiro, B.I.; Gebru, G.; Desta, S.; Negassa, A.; Nigussie, K.; Aboset, G.; Mechale, H. Ethiopia Livestock Sector Analysis; ILRI Project Report; International Livestock Research Institute (ILRI): Nairobi, Kenya, 2017. [Google Scholar]
- Gizachew, D.; Szonyi, B.; Tegegne, A.; Hanson, J.; Grace, D.; Gizachew, D.; Tegegne, A.; Hanson, J.; Grace, D.; Szonyi, B.; et al. Aflatoxin contamination of milk and dairy feeds in the Greater Addis Ababa milk shed, Ethiopia. Food Control 2016, 59, 773–779. [Google Scholar] [CrossRef]
- Pinotti, L.; Ottoboni, M.; Giromini, C.; Orto, V.D.; Cheli, F. Mycotoxin Contamination in the EU Feed Supply Chain: A Focus on Cereal Byproducts. Toxins (Basel) 2016, 8, 45. [Google Scholar] [CrossRef]
- Addis Standards Magazine December 2017. Available online: https://twitter.com/addisstandard/status/943838250820669441 (accessed on 15 December 2017).
- FAO (Food and Agriculture Organization). Worldwide Regulations for mycotoxins in food and feed 2003. FAO Food Nutr. Pap. 2003, 81, 1–165. [Google Scholar]
- Van Egmond, H.P.; Schothorst, R.C.; Jonker, M.A. Regulations relating to mycotoxins in food: Perspectives in a global and European context. Anal. Bioanal. Chem. 2007, 389, 147–157. [Google Scholar] [CrossRef] [Green Version]
- Cigić, I.K.; Prosen, H. An overview of conventional and emerging analytical methods for the determination of mycotoxins. Int. J. Mol. Sci. 2009, 10, 62–115. [Google Scholar] [CrossRef]
- Chawla, G.; Ranjan, C. Principle, Instrumentation, and Applications of UPLC: A Novel Technique of Liquid Chromatography. Open Chem. J. 2016, 3, 1–16. [Google Scholar] [CrossRef]
- Anfossi, L.; Baggiani, C.; Giovannoli, C.; Arco, G.D. Lateral-flow immunoassays for mycotoxins and phycotoxins: A review. Anal. Bioanal. Chem. 2013, 405, 467–480. [Google Scholar] [CrossRef]
- Guchi, E. Stakeholders’ awareness and knowledge about aflatoxin contamination of groundnut (Arachis hypogaea L.) andassociated factors in Eastern Ethiopia. Asian Pac. J. Trop. Biomed. 2014, 4, 931–937. [Google Scholar]
- EMI (Ethiopian Ministry of Industry). Spice Industry Strategic Plan (2015–2025); EMI: Addis Ababa, Ethiopia, 2015. [Google Scholar]
- EBT (Ethiopian Biotechnology Institute). Aflatoxin Project Progress Report and Personal Communication; EBT: Addis Ababa, Ethiopia, 2019. [Google Scholar]
- Udomkun, P.; Nimo, A.; Nagle, M.; Müller, J.; Vanlauwe, B.; Bandyopadhyay, R. Innovative technologies to manage aflatoxins in foods and feeds and the profitability of application—A review. Food Control 2017, 76, 127–138. [Google Scholar] [CrossRef] [PubMed]
- Baholet, D.; Kolackova, I.; Kalhotka, L.; Skladanka, J.; Haninec, P. Effect of Species, Fertilization and Harvest Date on Microbial Composition and Mycotoxin Content in Forage. Agriculture 2019, 9, 102. [Google Scholar] [CrossRef] [Green Version]
- Tucker, J.R.; Badea, A.; Blagden, R.; Pleskach, K.; Tittlemier, S.A.; Fernando, W.G.D. Deoxynivalenol-3-Glucoside Content Is Highly Associated with Deoxynivalenol Levels in Two-Row Barley Genotypes of Importance to Canadian Barley Breeding Programs. Toxins (Basel) 2019, 11, 319. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nimal, J.; Zhao, Y.; Sangare, L.; Xing, F.; Zhou, L.; Wang, Y.; Xue, X.; Li, Y.; Liu, Y. Limited survey of deoxynivalenol in wheat from different crop rotation fi elds in Yangtze-Huaihe river basin region of China. Food Control 2015, 53, 151–155. [Google Scholar] [CrossRef]
- Senghor, L.A.; Atehnkeng, J.; Callicott, K.A.; Cotty, P.J.; Bandyopadhyay, R. The Atoxigenic Biocontrol Product Aflasafe SN01 Is a Valuable Tool to Mitigate Aflatoxin Contamination of Both Maize and Groundnut Cultivated in Senegal. Plant Dis. 2020, 104, 510–520. [Google Scholar] [CrossRef] [PubMed]
- Alaniz Zanon, M.S.; Barros, G.G.; Chulze, S.N. Non-aflatoxigenic Aspergillus flavus as potential biocontrol agents to reduce aflatoxin contamination in peanuts harvested in Northern Argentina. Int. J. Food Microbiol. 2016, 231, 63–68. [Google Scholar] [CrossRef]
- Stepman, F. Scaling-Up the Impact of Aflatoxin Research in Africa. The Role of Social Sciences Francois. Toxin Rev. 2018, 10, 136. [Google Scholar] [CrossRef] [Green Version]
- The Reporter News Institute Finds High-Level of Aflatoxins Perilous to Health, Economy. Available online: https://www.thereporterethiopia.com/article/institute-finds-high-level-aflatoxins-perilous-health-economy (accessed on 25 August 2018).
- Vila-donat, P.; Marín, S.; Sanchis, V.; Ramos, A.J. Tri-octahedral bentonites as potential technological feed additive for Fusarium mycotoxin reduction. Food Addit. Contam. Part A 2020, 37, 1374–1387. [Google Scholar] [CrossRef]
- Chemicals, M.I.; Sciences, B. Adsorption of Zearalenone on Clay and Treated Clay Materials in Aqueous Solutions. Clay Sci. 2020, 24, 23–30. [Google Scholar] [CrossRef]
- Jaynes, W.F.; Zartman, R.E. Aflatoxin toxicity reduction in feed by enhanced binding to surface-modified clay additives. Toxins (Basel) 2011, 3, 551–565. [Google Scholar] [CrossRef] [PubMed]
- Fowler, J.; Li, W.; Bailey, C. Effects of a calcium bentonite clay in diets containing aflatoxin when measuring liver residues of aflatoxin B1in starter broiler chicks. Toxins (Basel) 2015, 7, 3455–3464. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiong, J.L.; Wang, Y.M.; Nennich, T.D.; Li, Y.; Liu, J.X. Transfer of dietary aflatoxin B1 to milk aflatoxin M1 and effect of inclusion of adsorbent in the diet of dairy cows. J. Dairy Sci. 2015, 98, 2545–2554. [Google Scholar] [CrossRef] [PubMed]
- Carraro, A.; De Giacomo, A.; Giannossi, M.L.; Medici, L.; Muscarella, M.; Palazzo, L.; Quaranta, V.; Summa, V.; Tateo, F. Clay minerals as adsorbents of aflatoxin M1from contaminated milk and effects on milk quality. Appl. Clay Sci. 2014, 88–89, 92–99. [Google Scholar] [CrossRef]
- Diaz, D.E.; Winston, M.H.; Blackwelder, J.T.; Eve, J.A.; Hopkins, B.A.; Anderson, K.L.; Jones, F.T.; Whitlow, L.W. Aflatoxin Binders II: Reduction of aflatoxin M1 in milk by sequestering agents of cows consuming aflatoxin in feed. Mycopathologia 2014, 157, 233–241. [Google Scholar] [CrossRef]
- FDA (Food and Drug Administration). 21CFR184.1155, Code of Federal Regulations, Title 21, Volume 3, Revised 1 April 2017. Available online: http://www.fda.gov/MedicalDevices/DeviceRegulationandGuidance/Databases/ucm135680.htm (accessed on 23 March 2019).
- Tessema, M. Occurrence of Bentonite in Ethiopia; Bentonite Promotion Document; Geological Survey of Ethiopia: Addis ababa, Ethiopia, 2012. Available online: http://www.gse.gov.et/ (accessed on 12 December 2017).
- Taffesse, A.S.; Dorosh, P.; Asrat, S. Crop Production in Ethiopia: Regional Patterns and Trends; ESSP II Working Paper 16 Crop; International Food Policy Research Institute: Washington, DC, USA; Addis ababa, Ethiopia, 2011; Available online: https://www.ifpri.org/ (accessed on 20 September 2016).
Commodities | Aflatoxins | Fumonisins (FUMs) | ||
---|---|---|---|---|
AFB1 | Total AFs | AFM1 | ||
Peanut kernels | 5 | 10 | - | |
Peanut butter | 4 | 10 | - | |
Maize | 5 | 10 | - | |
Wheat | - | 4 | - | |
Sorghum | 5 | 10 | - | |
Barley | 5 | 10 | - | |
Teff flour | - | 4 | - | |
Injera | 5 | 10 | 2000 | |
Raw cow milk | - | - | 0.05 | - |
Lentil | 5 | 10 | - | |
Chickpea | 5 | 10 | 2000 | |
Whole peas | 5 | 10 | 2000 | |
Split peas | 5 | 10 | 2000 | |
Dry beans | 5 | 10 | 2000 | |
Dry faba beans | 5 | 10 | 2000 | |
Kolo (roasted grain, ready-to-eat food) | - | - | 2000 | |
Beer | 5 | 10 | - |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Mamo, F.T.; Abate, B.A.; Tesfaye, K.; Nie, C.; Wang, G.; Liu, Y. Mycotoxins in Ethiopia: A Review on Prevalence, Economic and Health Impacts. Toxins 2020, 12, 648. https://doi.org/10.3390/toxins12100648
Mamo FT, Abate BA, Tesfaye K, Nie C, Wang G, Liu Y. Mycotoxins in Ethiopia: A Review on Prevalence, Economic and Health Impacts. Toxins. 2020; 12(10):648. https://doi.org/10.3390/toxins12100648
Chicago/Turabian StyleMamo, Firew Tafesse, Birhan Addisie Abate, Kassahun Tesfaye, Chengrong Nie, Gang Wang, and Yang Liu. 2020. "Mycotoxins in Ethiopia: A Review on Prevalence, Economic and Health Impacts" Toxins 12, no. 10: 648. https://doi.org/10.3390/toxins12100648