Research Articles

Fusarium spp. and levels of fumonisins in maize produced by subsistence farmers in South Africa

Edson Ncube, Bradley C. Flett, Cees Waalwijk, Altus Viljoen
South African Journal of Science | Vol 107, No 1/2 | a367 | DOI: https://doi.org/10.4102/sajs.v107i1/2.367 | © 2011 Edson Ncube, Bradley C. Flett, Cees Waalwijk, Altus Viljoen | This work is licensed under CC Attribution 4.0
Submitted: 21 July 2010 | Published: 28 January 2011

About the author(s)

Edson Ncube, Agricultural Research Council-Grain Crops Institute, Potchefstroom, South Africa
Bradley C. Flett, Agricultural Research Council-Grain Crops Institute, Potchefstroom, South Africa
Cees Waalwijk, Plant Research International BV, Wageningen, Netherlands
Altus Viljoen, Department of Plant Pathology, University of Stellenbosch, South Africa

Abstract

Fusarium spp. produce fumonisins – mycotoxins that are of importance to maize production in South Africa. Fumonisins have been associated with human oesophageal cancer and cause various diseases in animals that are of concern to the animal feed industry. Maize samples, collected from subsistence farm fields in the Eastern Cape, KwaZulu-Natal, Limpopo and Mpumalanga provinces of South Africa during the 2006 and 2007 growing seasons, were analysed for Fusarium spp. and contamination with fumonisins. Fusarium verticillioides was the most common Fusarium species in maize followed by F. subglutinans and F. proliferatum. Levels of contamination with fumonisins ranged from 0 μg/g to 21.8 μg/g, depending on the region where samples were collected. Levels of fumonisins were highest in northern KwaZulu-Natal (Zululand) where 52% and 17% of samples collected in 2006 and 2007, respectively, exceeded 2 μg/g. Regression analyses showed a positive correlation between fumonisin-producing Fusarium spp. determined by real-time polymerase chain reaction and concentration of fumonisins (r = 0.93). Many samples from Zululand, and some from Mokopane (Limpopo) and Lusikisiki (Eastern Cape), contained fumonisins at levels well above the maximum levels of 2 μg/g set by the Food and Drug administration (USA) and therefore also the limit of 1 μg/g set by the European Union for food intended for direct human consumption. Regulations governing contamination of grain with fumonisins are not yet implemented in South Africa. The high incidence of fumonisins in subsistence farming systems indicates the need for awareness programmes and further research.

Keywords

mycotoxins; fumonisins; Fusarium species

Metrics

Total abstract views: 2874
Total article views: 4096

References


Crop Estimates Committee. Calculated area and crop production figures of maize and sorghum: 2006/07 production season [document on the Internet]. c2007 [cited 2009 Dec 14]. Available from: http://www.nda.agric.za/doaDev/cropestimates/Calculated%20final%20crop%20of%20summer%20crops%20Nov%202007.doc

Northern Cape Department of Agriculture and Land Reform. Maize industry: Situation analyses, market indicators and outlook for 2008 season [document on the Internet]. c2007 [cited 2009 Dec 14]. Available from: http://www.agrinc.gov.za/docs/Maize%20Outlook%202008.pdf

Bankole SA, Adebanjo A. Mycotoxins in food in West Africa: Current situation and possibilities of controlling it. Afr J Biotech. 2003;2:254–263.

Ncube E. Mycotoxin levels in subsistence farming systems in South Africa [MSc dissertation]. Stellenbosch: University of Stellenbosch; 2008.

Watkinson E, Makgetla N. South Africa’s food security crisis [document on the Internet]. c2002 [cited 2007 Apr 19]. Available from: http://www.sarpn.org.za/documents/0000077/P93_safscrisis.pdf

Shephard GS, Marasas WFO, Burger H-M, et al. Exposure assessment for fumonisins in the former Transkei region of South Africa. Food Add Contam. 2007;24:621–629. doi:10.1080/02652030601101136

Wilke AL, Bronson CR, Tomas A, Munkvold GP. Seed transmission of Fusarium verticillioides in maize plants grown under three different temperature regimes. Plant Dis. 2007;91:1109–1115. doi:10.1094/PDIS-91-9-1109

Meissle M, Mouron P, Musa T, et al. Pests, pesticide use and alternative options in European maize production: Current status and future prospects. J Appl Entomol. 2010;134:357–375. doi:10.1111/j.1439-0418.2009.01491.x

Munkvold GP, Desjardins AE. Fumonisins in maize. Can we reduce their occurrence? Plant Dis. 1997;81:556–565. doi:10.1094/PDIS.1997.81.6.556

Marasas WFO. Fumonisins: History, world-wide occurrence and impact. Adv Exp Med Biol. 1996;392:1–17. PMid:8850601

Leslie JF. Diversity in toxigenic Fusarium species in Africa. Paper presented at: Myco-Globe 2005. Proceedings of the Conference on Reducing Impact of Mycotoxins in Tropical Agriculture with Emphasis on Health and Trade in Africa; 2005 Sept 13–26; Accra, Ghana. [homepage on the Internet]. c2005 [cited 2010 Oct 18]. Available from: http://www.ispa.cnr.it/mycoglobe/Research Article http://www.sajs.co.za S Afr J Sci 2011; 107(1/2) index.php?page=result&id=18

Gelderblom WCA, Jaskiewicz K, Marasas WFO, et al. Fumonisins –novel mycotoxins with cancer promoting activity produced by Fusarium moniliforme. Appl Environ Microbiol. 1988;54:1806–1811. PMid:2901247, PMCid:202749

Shephard GS. Mycotoxins in the context of food risks and nutrition issues. In: Barug A, Bhatnagar D, van Egmond HP, van der Kamp JW, van Osenbruggen WA, Visconti A, editors. The mycotoxin factbook. Wageningen: Wageningen Academic Publishers, 2006; p. 21–36.

Summerell BA, Salleh B, Leslie JF. A utilitarian approach to Fusarium identification. Plant Dis. 2003;87:117–128. doi:10.1094/PDIS.2003.87.2.117

Thiel PG, Meyer CJ, Marasas WFO. Natural occurrence of moniliformin together with deoxynivalenol and zearalenone in Transkeian corn. J Agric Food Chem. 1982;30:308–317. doi:10.1021/jf00110a023

Chu FS, Li GY. Simultaneous occurrence of fumonisin B1 and other mycotoxins in mouldy corn collected from the People’s Republic of China in regions with high incidences of oesophageal cancer. Appl Environ Microbiol. 1994;60:847–852. PMid:8161178, PMCid:201401

Rheeder JP, Marasas WFO, Thiel PG, Sydenham EW, Shephard GS, Van Schalkwyk DJ. Fusarium moniliforme and fumonisins in corn in relation to human oesophageal cancer in Transkei. Phytopathology. 1992;82:353–357. doi:10.1094/Phyto-82-353

Missmer SA, Suarez L, Felkner M, et al. Exposure to fumonisins and the occurrence of neural tube defects along the Texas-Mexico border. Environ Health Persp. 2006;114:237–241. doi:10.1289/ehp.8221, PMid:16451860, PMCid:1367837

Glenn AE. Mycotoxigenic Fusarium species in animal feed. Anim Feed Sci Technol. 2007;137:213–240. doi:10.1016/j.anifeedsci.2007.06.003

Kellerman TS, Marasas WFO, Thiel PG, Gelderblom WCA, Cawood ME, Coetzer JA. Leukoencephalomalacia in two horses induced by oral dosing of fumonisin B1 . Onderst J Vet Res. 1990;57:269–275.

Haschek WM, Gumprecht LA, Smith G, Tumbleson ME, Constable PD. Fumonisin toxicosis in swine: An overview of porcine pulmonary edema and current perspectives. Environ Health Persp Suppl. 2001;109:251–257. doi:10.2307/3435016, PMid:11359693, PMCid:1240673

Van Wyk PS, Scholtz DJ, Los O. A selective medium for the isolation of Fusarium spp. from soil debris. Phytophylactica. 1986;18:67–69.

Leslie JF, Summerell BA. The Fusarium laboratory manual. Ames: Blackwell

Waalwijk C, Koch S, Ncube E, et al. Quantitative detection of fumonisin-producing Fusarium spp. and its correlation with fumonisin content in maize from South African subsistence farmers. World Mycotoxin J. 2008;1:39–47. doi:10.3920/WMJ2008.x005

Neogen Corporation [DVD]. Veratox® Software for Windows. Log/Logit and Single Test Format. Version 3.0.1 EU. Lansing, MI, USA. 2008.

Manugistics Incorporated. Statgraphics® 5 Plus. Rockville, MD, USA. 2000.

Food and Drug Administration (FDA). Guidelines for industry: Fumonisin levels in human foods and animal feeds. Rockville: FDA; 2001.

European Commission (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;L255:14–17.

Marasas WFO, Kriek NPJ, Wiggins VM, Steyn PS, Towers DK, Hastie TJ. Incidence, geographic distribution, and toxicigenicity of Fusarium species in South Africa. Phytopathology. 1979;69:1181–1185. doi:10.1094/Phyto-69-1181

McFarlane SA, Govender P, Rutherford RS. Interactions between Fusarium species from sugarcane and the stalk borer Eldana saccharina (Lepidoptera: Pyralidae). Ann Appl Biol. 2009;155:349–359. doi:10.1111/j.1744-7348.2009.00345.x

Waalwijk C, Van der Heide R, De Vries PM, et al. Quantitative detection of Fusarium species in wheat using TaqMan. Eur J Plant Path. 2004;110:481–494. doi:10.1023/B:EJPP.0000032387.52385.13



Reader Comments

Before posting a comment, read our privacy policy.

Post a comment (login required)

 

Crossref Citations

1. Potential of Novel Sequence Type of Burkholderia cenocepacia for Biological Control of Root Rot of Maize (Zea mays L.) Caused by Fusarium temperatum
Setu Bazie Tagele, Sang Woo Kim, Hyun Gu Lee, Youn Su Lee
International Journal of Molecular Sciences  vol: 20  issue: 5  first page: 1005  year: 2019  
doi: 10.3390/ijms20051005

2. Rural Subsistence Maize Farming in South Africa: Risk Assessment and Intervention models for Reduction of Exposure to Fumonisin Mycotoxins
Johanna Alberts, John Rheeder, Wentzel Gelderblom, Gordon Shephard, Hester-Mari Burger
Toxins  vol: 11  issue: 6  first page: 334  year: 2019  
doi: 10.3390/toxins11060334

3. Mycotoxin patterns in ear rot infected maize: A comprehensive case study in Nigeria
Isaac Maikasuwa Ogara, Afiniki Bawa Zarafi, Olufunmilola Alabi, Olalekan Banwo, Chibundu N. Ezekiel, Benedikt Warth, Michael Sulyok, Rudolf Krska
Food Control  vol: 73  first page: 1159  year: 2017  
doi: 10.1016/j.foodcont.2016.10.034

4. Resistance in Maize Inbred Lines to Fusarium verticillioides and Fumonisin Accumulation in South Africa
I. M. Small, B. C. Flett, W. F. O. Marasas, A. McLeod, M. A. Stander, A. Viljoen
Plant Disease  vol: 96  issue: 6  first page: 881  year: 2012  
doi: 10.1094/PDIS-08-11-0695

5. Mycotoxin contamination of foods in Southern Africa: A 10-year review (2007–2016)
J. M. Misihairabgwi, C. N. Ezekiel, M. Sulyok, G. S. Shephard, R. Krska
Critical Reviews in Food Science and Nutrition  vol: 59  issue: 1  first page: 43  year: 2019  
doi: 10.1080/10408398.2017.1357003

6. Occurrence of filamentous fungi in maize destined for human consumption in South Africa
Theodora I. Ekwomadu, Ramokone E. Gopane, Mulunda Mwanza
Food Science & Nutrition  vol: 6  issue: 4  first page: 884  year: 2018  
doi: 10.1002/fsn3.561

7. Pathogenicity and toxigenicity of Fusarium verticillioides isolates collected from maize roots, stems and ears in South Africa
A. Schoeman, B. C. Flett, B. Janse van Rensburg, E. Ncube, A. Viljoen
European Journal of Plant Pathology  vol: 152  issue: 3  first page: 677  year: 2018  
doi: 10.1007/s10658-018-1510-z

8. Inheritance and genotype by environment analyses of resistance to Fusarium verticillioides and fumonisin contamination in maize F1 hybrids
N. E. I. Netshifhefhe, B. C. Flett, A. Viljoen, L. J. Rose
Euphytica  vol: 214  issue: 12  year: 2018  
doi: 10.1007/s10681-018-2310-4

9. Progress in stacking aflatoxin and fumonisin contamination resistance genes in maize hybrids
N. Chiuraise, J. Derera, K. S. Yobo, C. Magorokosho, A. Nunkumar, N. F. P. Qwabe
Euphytica  vol: 207  issue: 1  first page: 49  year: 2016  
doi: 10.1007/s10681-015-1529-6

10. High occurrence of Aspergillus section Aspergillus in corn kernels for feed production
Mauro César Piotto de Lima, Dâmaris Cristine Landgraf, Sara Mataroli de Godoy, Daniele Cassiano Feliciano, Claudete de Fátima Ruas, Marina Venturini Copetti, Daniele Sartori
Brazilian Journal of Microbiology  vol: 56  issue: 4  first page: 2495  year: 2025  
doi: 10.1007/s42770-025-01778-8

11. Assessment of aflatoxin and fumonisin contamination levels in maize and mycotoxins awareness and risk factors in Rwanda
Marguerite Niyibituronsa, M Usabyembabazi, E Nkundanyirazo
African Journal of Food, Agriculture, Nutrition and Development  vol: 20  issue: 05  first page: 16420  year: 2020  
doi: 10.18697/ajfand.93.19460

12. Field evaluation of resistance to aflatoxin accumulation in maize inbred lines in Kenya and South Africa
Sheila Okoth, Lindy Joy Rose, Abigael Ouko, Ilze Beukes, Henry Sila, Marili Mouton, Bradley Charles Flett, Dan Makumbi, Altus Viljoen
Journal of Crop Improvement  vol: 31  issue: 6  first page: 862  year: 2017  
doi: 10.1080/15427528.2017.1391915

13. Nixtamalization of Maize to Reduce Mycotoxin Exposure: A Human Biomonitoring Intervention Study in Soweto, South Africa
Elias Maris, Palesa Ndlangamandla, Oluwasola A. Adelusi, Oluwakamisi F. Akinmoladun, Julianah O. Odukoya, Richard T. Fagbohun, Samson A. Oyeyinka, Palesa Sekhejane, Roger Pero-Gascon, Marthe De Boevre, Siska Croubels, Patrick B. Njobeh, Sarah De Saeger
Toxins  vol: 17  issue: 11  first page: 527  year: 2025  
doi: 10.3390/toxins17110527

14. Factors Determining the Adoption of Strategies Used by Smallholder Farmers to Cope with Climate Variability in the Eastern Free State, South Africa
Lindumusa Myeni, Mokhele Edmond Moeletsi
Agriculture  vol: 10  issue: 9  first page: 410  year: 2020  
doi: 10.3390/agriculture10090410

15. A sub-Saharan African perspective on mycotoxins in beer - a review
Tshikala Eddie Lulamba, Robert A. Stafford, Patrick Berka Njobeh
Journal of the Institute of Brewing  vol: 125  issue: 2  first page: 184  year: 2019  
doi: 10.1002/jib.558

16. A Scoping Review of Mycotoxin Contamination of Maize and Other Grains in South Africa
Felix Fon Fru, Clarence Suh Yah, Lebogang Charity Motaung, Palesa Rose Sekhejane, Patrick Berka Njobeh
Shiraz E-Medical Journal  vol: 22  issue: 11  year: 2021  
doi: 10.5812/semj.113558

17. Bacterial Diversity and Mycotoxin Reduction During Maize Fermentation (Steeping) for Ogi Production
Chiamaka A. Okeke, Chibundu N. Ezekiel, Cyril C. Nwangburuka, Michael Sulyok, Cajethan O. Ezeamagu, Rasheed A. Adeleke, Stanley K. Dike, Rudolf Krska
Frontiers in Microbiology  vol: 6  year: 2015  
doi: 10.3389/fmicb.2015.01402

18. Spatial and temporal variations in contamination of mycotoxins in sub-humid, semi-arid areas of Eastern Central Tanzania
Kija Steven Magembe, Maulid Walad Mwatawala, Delphina Peter Mamiro
Archives of Phytopathology and Plant Protection  vol: 49  issue: 17-18  first page: 445  year: 2016  
doi: 10.1080/03235408.2016.1230961

19. Evaluation of maize cultivars for their susceptibility towards mycotoxigenic fungi under storage conditions
P. Dawlal, E. Barros, G.J. Marais
Journal of Stored Products Research  vol: 48  first page: 114  year: 2012  
doi: 10.1016/j.jspr.2011.10.006

20. Diversity and toxigenicity of fungi and description of Fusarium madaense sp. nov. from cereals, legumes and soils in north-central Nigeria
Chibundu N. Ezekiel, Bart Kraak, Marcelo Sandoval-Denis, Michael Sulyok, Oluwawapelumi A. Oyedele, Kolawole I. Ayeni, Oluwadamilola M. Makinde, Oluwatosin M. Akinyemi, Rudolf Krska, Pedro W. Crous, Jos Houbraken
MycoKeys  vol: 67  first page: 95  year: 2020  
doi: 10.3897/mycokeys.67.52716

21. Natural occurrence of Fusarium species and fumonisin on maize grains in Ethiopia
Hadush Tsehaye, May Bente Brurberg, Leif Sundheim, Dereje Assefa, Arne Tronsmo, Anne Marte Tronsmo
European Journal of Plant Pathology  vol: 147  issue: 1  first page: 141  year: 2017  
doi: 10.1007/s10658-016-0987-6

22. Tolerance to Fusarium verticillioides infection and fumonisin accumulation in maize F1 hybrids and subsequent F2 populations
Abigael Ouko, Sheila Okoth, Nakisani E. l. Netshifhefhe, Altus Viljoen, Lindy Joy Rose
Agronomy Journal  vol: 112  issue: 4  first page: 2432  year: 2020  
doi: 10.1002/agj2.20145

23. Fumonisins in African Countries
Tapani Yli-Mattila, Leif Sundheim
Toxins  vol: 14  issue: 6  first page: 419  year: 2022  
doi: 10.3390/toxins14060419

24. Underreported Human Exposure to Mycotoxins: The Case of South Africa
Queenta Ngum Nji, Olubukola Oluranti Babalola, Nancy Nleya, Mulunda Mwanza
Foods  vol: 11  issue: 17  first page: 2714  year: 2022  
doi: 10.3390/foods11172714

25. Determining resistance to Fusarium verticillioides and fumonisin accumulation in African maize inbred lines resistant to Aspergillus flavus and aflatoxins
Lindy Joy Rose, Sheila Okoth, Ilze Beukes, Abigael Ouko, Marili Mouton, Bradley Charles Flett, Dan Makumbi, Altus Viljoen
Euphytica  vol: 213  issue: 4  year: 2017  
doi: 10.1007/s10681-017-1883-7

26. Mycotoxigenic fungi and mycotoxins associated with stored maize from different regions of Lesotho
Sejakhosi Mohale, Angel Medina, Alicia Rodríguez, Michael Sulyok, Naresh Magan
Mycotoxin Research  vol: 29  issue: 4  first page: 209  year: 2013  
doi: 10.1007/s12550-013-0176-9

27. Fungal Species and Mycotoxins Associated with Maize Ear Rots Collected from the Eastern Cape in South Africa
Jenna-Lee Price, Cobus Meyer Visagie, Hannalien Meyer, Neriman Yilmaz
Toxins  vol: 16  issue: 2  first page: 95  year: 2024  
doi: 10.3390/toxins16020095

28. Proteomics and plant disease: Advances in combating a major threat to the global food supply
Christof Rampitsch, Natalia V. Bykova
PROTEOMICS  vol: 12  issue: 4-5  first page: 673  year: 2012  
doi: 10.1002/pmic.201100359

29. Fumonisin producing Fusarium spp. and fumonisin contamination in commercial South African maize
B. Janse van Rensburg, N. W. McLaren, B. C. Flett, A. Schoeman
European Journal of Plant Pathology  vol: 141  issue: 3  first page: 491  year: 2015  
doi: 10.1007/s10658-014-0558-7

30. Barriers Affecting Sustainable Agricultural Productivity of Smallholder Farmers in the Eastern Free State of South Africa
Lindumusa Myeni, Mokhele Moeletsi, Mulalo Thavhana, Mulalo Randela, Lebohang Mokoena
Sustainability  vol: 11  issue: 11  first page: 3003  year: 2019  
doi: 10.3390/su11113003

31. Fungal Mycoflora Associated with Busseola fusca Frass in Maize Plants
E. Ncube, M. Truter, B.C. Flett, J. Van den Berg, A. Erasmus, A. Viljoen
African Entomology  vol: 28  issue: 2  year: 2020  
doi: 10.4001/003.028.0394

32. Quantification of multi-mycotoxin in cereals (maize, maize porridge, sorghum and wheat) from Limpopo province of South Africa
Shandry Mmasetshaba Tebele, Sefater Gbashi, Oluwafemi Adebo, Rumbidzai Changwa, Kayleen Naidu, Patrick Berka Njobeh
Food Additives & Contaminants: Part A  vol: 37  issue: 11  first page: 1922  year: 2020  
doi: 10.1080/19440049.2020.1808715

33. Mycotoxin contamination of home-grown maize in rural northern South Africa (Limpopo and Mpumalanga Provinces)
P. Mngqawa, G.S. Shephard, I.R. Green, S.H. Ngobeni, T.C. de Rijk, D.R. Katerere
Food Additives & Contaminants: Part B  vol: 9  issue: 1  first page: 38  year: 2016  
doi: 10.1080/19393210.2015.1121928

34. A decade of plant proteomics and mass spectrometry: Translation of technical advancements to food security and safety issues
Ganesh Kumar Agrawal, Abhijit Sarkar, Pier Giorgio Righetti, Romina Pedreschi, Sebastien Carpentier, Tai Wang, Bronwyn J. Barkla, Ajay Kohli, Bongani Kaiser Ndimba, Natalia V. Bykova, Christof Rampitsch, Lello Zolla, Mohamed Suhail Rafudeen, Rainer Cramer, Laurence Veronique Bindschedler, Nikolaos Tsakirpaloglou, Roya Janeen Ndimba, Jill M. Farrant, Jenny Renaut, Dominique Job, Shoshi Kikuchi, Randeep Rakwal
Mass Spectrometry Reviews  vol: 32  issue: 5  first page: 335  year: 2013  
doi: 10.1002/mas.21365

35. Multi-environment Evaluation of Maize Inbred Lines for Resistance to Fusarium Ear Rot and Fumonisins
L. J. Rose, M. Mouton, I. Beukes, B. C. Flett, C. van der Vyver, A. Viljoen
Plant Disease  vol: 100  issue: 10  first page: 2134  year: 2016  
doi: 10.1094/PDIS-11-15-1360-RE