Review ArticleOpen Access

Food Microbial Contamination by Toxigenic Molds-Threat for Human and Animal Health

Menkovska M1*, Tomovska J2, Vllasaku I3, Gjorgovska N1, and Levkov V1

1Institute of Animal Science, Ss Cyril and Methodius University, 1000 Skopje, Republic of Macedonia
2Faculty of Biotechnical Sciences, St. Kliment Ohridski University, 7000 Bitola, Republic of Macedonia
3Ministry of Agriculture, Forestry and Water Economy, Aminta Treti str.No.3, 1000 Skopje, Republic of Macedonia

*Corresponding Author: 
Menkovska M
  Institute of Animal Science
  Ss Cyril and Methodius University
  1000 Skopje, Republic of Macedonia
  Tel: +38975277623
  E-mail: [email protected]

Received: February 03, 2018; Published: October 24, 2018

Citation: Menkovska M, Tomovska J, Vllasaku I, Gjorgovska N, Levkov V (2018) Food Microbial Contamination by Toxigenic Molds-Threat for Human and Animal Health. J Nutr Diet Suppl 2(1): 101


The food is necessity for keeping in life humans and animals, but it can also be a threat for their health and wellbeing. Food can be contaminated by a range of microorganisms and their toxins causing foodborne illnesses. Among them the mycotoxigenic molds produce mycotoxins as metabolic products. Most of them are carcinogenic causing acute damage to human and animal organs. The most important genera in the spoilage of foods and animal feeds are Aspergillus and Penicillium species which produce a variety of aflatoxins having deleterious effects on human and animal health.

Keywords: Mycotoxins; Alfatoxins; Occurance; Detection; Control


Mycotoxins are chemical compounds, metabolic products of the mold group Michofite, so named mold secondary metabolites. Aspergillus species are one of the most important genera of toxigenic molds in the spoilage of foods and animal feeds that produce a variety of aflatoxins (AFTs), that cause severe health problems to humans and animals [1-3]. Among them, the aflatoxin B1 is the most potent liver carcinogen producing acute liver damage, liver cirrhosis, tumor induction, and terarogenesis. From the harmful impact of the aflatoxins especially are affected the third world countries. There is evidence that acute aflatoxicosis outbreaks in Asia and India caused simptoms such as vomiting, abdominal pain, pulmonary edema, and fatty infiltration and necrosis of the liver, as well as fatalities [4,5].

Many other mycotoxins produced by Aspergillus are of great significance from the point of view of human health in cancer induction and immunosuppresion. The immunosuppression caused by AFTs can increase susceptibility to infectious diseases, particularly in populations where AFT ingestion is chronic, and it can be developed by either alone or in combination with other mycotoxins. Aflatoxin B1 is an immunosuppressor [6].

Organs that are mainly attacked by aflatoxins resulting in acute toxicity and carcinogenicity are the liver and the lungs [4]. Human liver canser has a high incidence in central Africa and parts of Southest Asia, and studies in several African countries and Thailand have shown a correlation between aflatoxin intake and the occurance of primary liver canser. It was found very strong correlation between the daily dietary intake of AFB1 and the incidence of primary liver cancer in humans [7]. Suppression of phagocytosis by alveolar macrophages that persisted for 2 weeks was caused by exposure of lungs to aerosolic AFTs [8,9]. The main target organ of Ochratoxin A (OTA) is kidney. Animal studies showed that OTA is a potent renal carcinogen [10], also being carcinogenic to humans, as well as an immunosuppressive, teratogenic, and nephrotoxic compound [11]. High dosage of mycotoxins' contamination causes chronic mycotoxicosis, such as HCC, involving formation of DNA adducts, regulation of DNA methylation, and alteration of gene expression [12,13].

The purpose of this article is to draw attention to the danger of food contamination with mycotoxins, especially with Aspergillus species, as well as for the possible prevention and control of this food natural contamination threatening the health of humans and animals.

Varieties of Aflatoxins

Significant mycotoxins produced by Aspergillus species and their toxic effects are presented in Table 1.

Mycotoxin (s) Toxicity Species
Aflatoxin B1 and B2 Acute liver damage, cirrhosis, carcinogenic (liver), teratogenic, and immunosuppressive A. flavus, A. Parasiticus,
Aflatoxin G1 and G2 Effects similar to those of B aflatoxins, G1 toxicity less than that of B1 but greater than that of B2 A. Parasiticus, A. nomius
Cyklopiazonic acid Degeneration and necrosis of various organs, tremorgenic, low oral toxicity A. flavus, A. tamarii
Ochratoxin A Kidney necrosis (especially in pigs), terato-genic, immunosuppressive, probably carcinogenic A. ochraceus, and related species, A. carbonarius, A. niger (occasional)
Sterigmatocystin spp Acute liver and kidney damage, A. versicolor, Emericella
Fumitremorgens carcinogenic (liver) Tremorgenic (rats and mice) A. fumigatus
Territrems Tremorgenic (rats and mice) Tremorgenic A. terreus
A. clavatus
Cytochalasins Cytotoxic A.clavatus
Echinulins Feed refusals (pigs) Tryptoquivalines

aAdapted from Table 24.1 in Food Mycrobiology, 24.Toxigenic Aspergillus species, pp.539
Table 1: Mycotoxins with their toxic effects produced by Aspergillus speciesa

The letters B and G refer to the fluorescent colors (blue and green, respectively) observed under long-wave UV light, and the subscripts 1 and 2 refer to the toxins’s separation patterns on thin-layer-chromatography plates.

Occurrence of AFs

The first data for Aspergillus associated with food date back to 300 years ago. They commonly occure in stored food such as grains, nuts, and spices and more frequently in tropical and subtropical climates [14,15]. A. flavus is one of the most commonly occurring Aspergillus molds in nuts and oilseeds, soybeans, mung beans and sorghum. A.Nomius was detected most often in peanuts and corn. The most important crops invaded by these molds are corn, peanuts and cottonseed [15]. Cereals and spices are also common crops invided for A. flavus, as a result of poor drying, handling, or storage [16]. The invasion of AFTs in these commodities can takes place before harvest while still in the ground, during the storage and processing. Food contaminated with AFTs is the most important risk factor in South East Africa and South East Asia [17]. AFTs are also frequent at high levels in airborne, respirable grain dust particles duing cerel processing and in indoor air, because of what they represent potentinal threat for the environment [18-20]. There is evidence for a significant increasing in fatality from cancer and respiratory cancer in peanut-processing workers exposed to AFT-contaminated dust. There are data for co-occurence on various mycotoxins such as AFTs with ochratoxin A in spices and processed cereal-based foods [21,22].

Chemical Structure of Aflatoxins

AFTs are difuranocoumarin derivatives (Figure 1) and they are synthesized through the polyketide pathway The B-type ATFs are characterized by a cyclopentane E-ring. These compounds have a blue fluorescence under long-wavelength UV light, while the G-type AFTs have a xanthone ring in place of the cyclopentane and fluoresce green under UV light. AFTs of the B2 and G2 type have a saturated bis-furanyl ring. In Figure 1 only the bis-furan is shown. AFTs of the Bla and Gia type have a hydrated bis-furanyl structure.

Biochemical Activation and Molecular Mechanism of Aflatoxin Action

AFTs are converted into acutely toxic and carcinogenic reactive species by undergoing the process of oxidative metabolism. Their toxicity and carcinogenicity are exerted by covalent binding of reactive AFT metabolites to cellular macromolecules proteins, DNA and RNA. Carcinogenicity and mutagenicity by transformation with DNA modified by the carcinogen-mutagen, aflatoxin B1. of AFTs are associated with their DNA binding properties [7].

Factors Affecting Aflatoxin’s Growth and Toxin Production

Environmental factors have an influence on the production of mycotoxins [23]. AFTs are produced at optimum temperature and water activity (aw). The temperature ranges from 12 to 40 oC. The optimum temperatures for A. flavus and A. paraziticus are from 30 to 33 oC. The optimum water activity for growth is near 0.996. The optimum water activity for growth of AFTs is of 0.80 to 0.83, but they are produced in greater quantity at higher aw (0.98 to 0.99). pH is another important factor for growth of AFTs, with a range from obove 2.0 up to 10.5 [17]. The final mycotoxin concentrations observed in food may be due to complex interactions between species and the environmental factors of the samples analyzed [24].

Control and Inactivation of Aflatoxins

Prevention of the plants from becoming infected with aflatoxigenic molds is the primary method of control of AFTs in agricultural commodities. Controls are carried out with screening techniques which are based on separation of affected grains, nuts or seeds. Screening for AFTs in corn, cottonseed and figs usually is performed by examination under UV light. Infected commodities with AFTs are segregated by electronic color-sorting machines which detect discolored kernels.

Management practices were also applied for reduction of pre-harvest [25,26] and post-harvest [27] contamination of agricultural commodities with AFTs. Sensitive and accurate analitical methods were developed for separate and simultaneous determination of the frequent mycotoxins, including aflatoxin B1 [28-31].

Various treatments can be used for destroying AFTs in various agricultural products [32,33]. So, ozone and hydrogen peroxide have been demonstrated to remove AFTs from contaminated peanut meals. Anhydrous ammonia gas that was used at elevated temperatures and pressures was effective with a 95 to 98% reduction in total AFTs in peanut meal. With these techniques detoxification of animal feeds in several countries (Senegal, France and the USA) was applied. The surfaces of baked products may be contaminated with airborne mold spores during the relatively long product cooling period between baking and packaging. The baking of dough products reduces the microflora and moisture content, so enabling the mycotoxins that could cause spoilage to be reduced. Reduction of available oxygen by modified-atmosphere packaging of foods in barrier film or with oxygen scavengers can inhibit AFTs formation by A. flavus and A. paraziticus.


Aspergillus is one of the most important genera in the spoilage of foods and animal feeds, containing a number of highly mycotoxigenic molds. The aflatoxigenic and ochratoxigenic species are the most important for human health. Other mycotoxins produced by many other mycotoxigenic molds are also of great importance for animal health than those products by Aspergillus species.

Because food mycotoxin contamination may occure at any stage of the food chain from the primary production, processing and storage to distribution and consumtion, it is necessary to introduce a proper control as a prevention, a preventive quality systems according to the accepted standards for safety food, as well as application of the quality managing.

  1. 1. Monson MS, Settlage RE, Mendoza KM, Rawal S, El-Nezami HS, et al. (2015) Modulation of the spleen transcriptome in domestic turkey (Meleagris gallopavo) in response to aflatoxin B1 and probiotics. Immunogenetics 67: 163-78.
  2. 2. Capcarova M, Zbynovska K, Kalafova A, Bulla J, Bielik P (2016) Environment contamination by mycotoxins and their occurrence in food and feed: Physiological aspects and economical approach. J Environ Sci Health B. 51:236-44.
  3. 3. Yang X, Liu L, Chen J, Xiao A (2017) Response of Intestinal Bacterial Flora to the Long-term Feeding of Aflatoxin B1 (AFB1) in Mice Toxins 9: 317.
  4. 4. Reed KM, Mendoza KM, Abrahante JE, Coulombe RA (2018) Comparative Response of the Hepatic Transcriptomes of Domesticated and Wild Turkey to Aflatoxin B1. Toxins 10: 42.
  5. 5. Muhammad I, Sun X, Wang H, Li W, Wang X, et al. (2017) Curcumin successfully inhibited the computationally identified CYP2A6 enzyme-mediated bioactivation of aflatoxin B1 in arbor acres broiler. Front Pharmacol 8:143.
  6. 6. Pierron A, Alassane-Kpembi I, Oswald IP (2016) Impact of mycotoxin on immune response and consequences for pig health. Animal Nutr 2 :63-8.
  7. 7. Wilson CL (2008) Microbial Food Contamination. Taylor & Francis Group, LLC, CRC Press, USA.
  8. 8. Damp Indoor Spaces and Health (2004) Institute of Medicine (US) Committee on Damp Indoor Spaces and Health. National Academies Press, Washington (DC), USA.
  9. 9. Bbosa GS, Kitya D, Lubega A, Ogwal-Okeng J, Anokbonggo WW, et al. (2013) Review of the Biological and Health Effects of Aflatoxins on Body Organs and Body Systems. Aflatoxins Mehdi Razzaghi-Abyaneh, IntechOpen.
  10. 10. Russo P, Capozzi V, Spano G, Corbo MR, Sinigaglia M, et al. (2016) Metabolites of microbial origin with an impact on health: ochratoxin A and biogenic amines. Front Microbiol 7: 482.
  11. 11. Ladeira C, Frazzoli C, Orisakwe OE (2017) Engaging one health for non-communicable diseases in Africa: perspective for mycotoxins. Front Public Health 5: 266.
  12. 12. Dai Y, Huang K, Zhang B, Zhu L, Xu W (2017) Aflatoxin B1-induced epigenetic alterations: an overview. Food Chem Toxicol 109: 683-9.
  13. 13. Zhu L, Zhang B, Dai Y, Li H, and Xu W (2017) A review: epigenetic mechanism in ochratoxin a toxicity studies. Toxins 9: 113.
  14. 14. Pandya JP, Arade PC (2016) Mycotoxin: a devil of human, animal and crop health. Adv Life Sci 5: 3937-41.
  15. 15. Alshannaq A, Jae-Hyuk Y (2017) Occurrence, Toxicity, and Analysis of Major Mycotoxins in Food. Int J Environ Res Public Health 14: 632.
  16. 16. Thathana MG, Murage H, Abia ALK, Pillay M (2017) Morphological Characterization and Determination of Aflatoxin-Production Potentials of Aspergillus flavus Isolated from Maize and Soil in Kenya. Agriculture 7: 80.
  17. 17. Doyle MP, Beuchat LR (2007) Food Mycrobiology:Fundamentals and Frontiers, (4th Edn.) American Society for Microbiology, ASM Press, USA.
  18. 18. Schaarschmidt S, Fauhl-Hassek C (2018) The Fate of Mycotoxins During the Processing of Wheat for Human Consumption. Compr Rev Food Sci Food Safet 556-93.
  19. 19. Viegas S, Paula LV, Almeida FA, Caroletino E, Viegas C (2015) Assessment of Workers’ Exposure to Aflatoxin B1 in a Portuguese Waste Industry. Ann Occupa Hyg 59: 173-81.
  20. 20. Aleksic B, Draghi M, Ritoux S, Bailly S, Lacroix M, et al. (2017) Aerosolization of Mycotoxins after Growth of Toxinogenic Fungi on Wallpaper. App Environ Microbiol 83: PMC5541226.
  21. 21. Ozbey F, Kabak B (2012) Natural Co-Occurrence of Aflatoxins and Ochratoxin A in Spices. Food Control 28: 354-361.
  22. 22. Assunção R, Martins C, Dupont D and Alvito P (2016) Patulin and ochratoxin a co-occurrence and their bioaccessibility in processed cereal-based foods: a contribution for Portuguese children risk assessment. Food Chem Toxicol 96: 205-14.
  23. 23. Kalinina SA, Jagels A, Cramer B, Geisen R, Humpf-HU (2017) Influence of Environmental Factors on the Production of Penitrems A-F by Penicillium crustosum. Toxins 9: 210.
  24. 24. Magan N, Aldred D, Hope R, Mitchell D (2010) Environmental Factors and Interactions with Mycobiota of Grain and Grapes: Effects on Growth, Deoxynivalenol and Ochratoxin Production by Fusarium culmorum and Aspergillus carbonarius. Toxins 2: 353-66.
  25. 25. Critical Reviews in Food Science and Nutrition (2013) Aflatoxins: Biosynthesis, Occurrence, Toxicity, and Remedies. 53: 862-74.
  26. 26. Gebreselassie R, Dereje A, Solomon H (2014) On Farm Pre Harvest Agronomic Management Practices of Aspergillus Infection on Groundnut in Abergelle, Tigray. J Plant PatholMicrobiol 5:228.
  27. 27. Abdu Selim Hamid, Isaias Goitom Tesfamariam, Yucheng Zhang, Zhen Gui Zhang (2013) Aflatoxin B1-induced hepatocellular carcinoma in developing countries: Geographical distribution, mechanism of action and prevention (Review). Oncol Lett 5: 1087-92.
  28. 28. Laganà A (2017) Introduction to the Toxins Special Issue on LC-MS/MS Methods for Mycotoxin Analysis. Toxins 9: 325.
  29. 29. Li H, Yang D, Li P, Zhang Q, Zhang W, et al. (2017) Palladium Nanoparticles-Based Fluorescence Resonance Energy Transfer Aptasensor for Highly Sensitive Detection of Aflatoxin M1 in Milk. Toxins 9: 318.
  30. 30. Ren G, Hu Y, Zhang J, Zou L, Zhao G (2018) Determination of Multi-Class Mycotoxins in Tartary Buckwheat by Ultra-Fast Liquid Chromatography Coupled with Triple Quadrupole Mass Spectrometry. Toxins 1: 28.
  31. 31. Levasseur-Garcia C (2018) Updated Overview of Infrared Spectroscopy Methods for Detecting Mycotoxins on Cereals (Corn, Wheat, and Barley). Toxins 10: 38.
  32. 32. Karlovsky P, Suman M, Berthiller F, Meester JD, Eisenbrand G, et al. (2016) Impact of food processing and detoxification treatments on mycotoxin contamination. Mycotoxin Res 32: 179-205.
  33. 33. Mauro A, Garcia-Cela E, Pietri A, Cotty PJ, Battilani P (2018) Biological Control Products for Aflatoxin Prevention in Italy: Commercial Field Evaluation of Atoxigenic Aspergillus flavus Active Ingredients. Toxins 10: 30.

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