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Aflatoxin
Photo: ICRISAT
Aflatoxin-contaminated groundnuts (below)
 
 

Aflatoxin-free grains are necessary to meet international market standards and ensure higher returns for farmers as well as to provide safer products for consumers.

25% - World's food crops significantly contaminated with mycotoxins (FAO 1999)

15 - Number of countries in Sub-Saharan Africa with regulations governing aflatoxins

4.5 billion - People in developing countries chronically exposed to aflatoxins in their diets (Source: Center for Disease Control)

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(a) Aflatoxins

Groundnut (Arachis hypogaea L.) is an important grain legume and oilseed crop grown in the tropical, subtropical and warm temperate regions of the world. Worldwide, groundnut occupies 24.71 million ha and the annual production totals approximately 41.19 million tons (Food and Agriculture Organization of the United Nations, 2014). Groundnuts provide a rich source of proteins and vitamins and are a major nutrient supplement in many households. Asia contributes 67.91%, Africa 24.45% and the Americas 7.87% to world groundnut production.

Aflatoxin contamination by Aspergillus section Flavi group of fungi contributes to sizeable losses in groundnut yield and trade. These aflatoxin-producing molds contaminate groundnuts in the field and during post-harvest stages. Pre-harvest infection occurs when pods are exposed to water and heat stress due to end-of-season drought; and by pod damage due to insects or nematodes. Post-harvest deterioration and aflatoxin contamination in groundnuts is due to conditions that favor molding during post-harvest operations and storage. These aflatoxins are an important cause of Hepato Cellular Carcinoma (HCC), the most common cancers in developing tropical countries. Out of 550,000 - 600,000 new HCC cases reported annually worldwide,  about 25,200 - 155,000 are attributed to aflatoxin exposure. Most of these are in sub-Saharan Africa, Southeast Asia, and China and are caused by uncontrolled aflatoxin exposure in food and hepatitis B virus (HBV) infection (Liu and Wu 2010).

Aflatoxins are the secondary metabolites produced by Aspergillus flavus and A. parasiticus that have carcinogenic, estrogenic, hepatotoxic, teratogenic and immuno-suppressive effects. These toxins are difuranocoumarin derivatives produced by a polyketide pathway. They were isolated and characterized after the death of >100,000 turkey birds (turkey X disease) due to consumption of mold-contaminated groundnut meal.

Major aflatoxins are categorized as B1, B2, G1 and G2 (AFB1 > AFG1 > AFB2 > AFG2 in terms of toxicity) based on their fluorescence under UV light and their relative chromatographic mobility during thin layer chromatography (TLC). AFB1 is the most prevalent and a group 1 carcinogen produced by almost all toxigenic strains of A. flavus group of fungi. Aflatoxins M1 and M2 are the metabolically biotransformed and hydroxylated form of B1 and B2 respectively in milk when cows consume aflatoxin-contaminated feed. It lowers the body's normal immune response to invasion by foreign substances.

Aflatoxin exposure  impairs growth in children, notably in Africa, and causes childhood cirrhosis in India. In poultry and livestock, it leads to feed refusal, weight loss, reduced egg production and contamination of milk.

Chemical and physical properties of aflatoxins.

Aflatoxins

Molecular formula

Molecular weight (g/mol)

Melting point (°C)

B1

C17 H12O6

312

268-269

B2

C17 H14O6

314

286-289

G1

C17 H12O7

328

244-246

G2

C17 H14O7

330

237-240

M1

C17 H12O7

328

299

M2

C17 H14O7

330

293

B2A

C17 H14O7

330

240

G2A

C17 H14O8

346

190


Structure of aflatoxins.
Crops affected

The Food and Agriculture Organization (FAO) declared that 25% of all crops in the world are affected by aflatoxins. They dominantly affect cereals and millets (maize, sorghum, pearl millet, rice, wheat); oilseeds (groundnut, soybean, rapeseed, sunflower, cotton); spices (chillies, black pepper, coriander, turmeric, ginger); tree nuts (almond, pistachio, walnut, cashewnut, hazelnut, Brazil nut, tiger nut, coconut); pulses (pigeonpea, horse gram, green gram, mung bean, lentil, cowpea, haricot bean); figs, meats, dairy products and fruit juices (apple and guava).

Factors contributing to aflatoxin contamination in groundnut

   Pre-harvest factors

  • Presence of the A. flavus fungus in the soil and air causes infection at every stage from pre-harvest to storage, producing aflatoxin in the kernels.
  • Use of susceptible cultivars
  • More than 20 days of end-of-season moisture stress to the crop
  • Mean soil temperatures of 28-31°C in the pod zone
  • Growth cracks and mechanical injury to the pod
  • Insect damage to pods by termites or pod borers
  • Death caused by diseases (stem, root and pod rots) at pod maturity
  • Nematode damage to the pod.

   Post-harvest factors

Post-harvest operations include cleaning, grading, transportation, storage, processing, packaging and marketing (Kimatu et al. 2012). The optimal conditions for bulk storage of unshelled groundnuts by farmers for up to one year are 7.5% kernel moisture, a temperature of 100oC and a relative humidity (RH) of 65% (Pattee and Young 1982). Among the post-harvest operations responsible for aflatoxin contamination are:

  • Harvesting an overly mature crop, mechanical damage to the pod at harvest
  • Stacking the harvest when pod moisture is more than 10% or under high humidity conditions
  • Insect damage to the pod during storage
  • Storing haulms with immature or small pods
  • Presence of gleans in the soil after harvest
  • Rewetting stored pods due to factors like ground-moisture or roof         

b)   Health and regulations

The International Agency for Research on Cancer (IARC) of the World Health Organization (WHO) has classified aflatoxins as Group I (established carcinogens to  humans). Aflatoxins cause Aflatoxicosis. The higher prevalence of HCC in Africa is linked to the carcinogenic nature of aflatoxins. Hepatitis B and C carriers are at high risk of developing into hepatocellular cancer on exposure to aflatoxins.

Acute toxicity

Limited availability of food, environmental conditions favoring fungal development in crops and commodities, and lack of regulatory systems for aflatoxin monitoring and control contribute to acute aflatoxicosis in humans. Studies have shown that ducklings are most susceptible to acute poisoning by aflatoxins. Aflatoxins mainly target the liver. After toxins invade the liver, lipids infiltrate hepatocytes, leading to necrosis or liver cell death. This happens when aflatoxin metabolites react negatively with different cell proteins, inhibiting carbohydrate and lipid metabolism and protein synthesis. Decrease in liver function leads to derangement of the blood clotting mechanism, icterus (jaundice), and a decrease in essential serum proteins synthesized by the liver. Other general signs of aflatoxicosis are edema of the lower extremities, abdominal pain, and vomiting.

Chronic toxicity

HCC due to chronic aflatoxin exposure presents itself most often in those with chronic Hepatitis B virus (HBV) infection (Qian et al. 1994, Groopman et al. 2008), raising the risk of liver cancer up to thirty-fold, compared with exposure alone (Groopman et al. 2008). Both the risk factors are prevalent in poor nations worldwide (Liu and Wu 2010; Wu et al., 2011). Chronic exposure to aflatoxins in animals can inhibit growth and suppress immunity (Khlangwiset et al. 2011). Nursing animals may be affected, and aflatoxin M1 may be excreted in the milk of dairy cattle and other dairy animals. This in turn poses potential health risks to both animals and humans that consume that milk.

Effect on human health

Humans are exposed to aflatoxins by consuming foods contaminated with products of fungal growth. Even though heavily contaminated food supplies are not permitted in the market place in developed countries, concerns remain about the possible adverse effects of long-term exposure to low levels of aflatoxins. Evidence of acute aflatoxicosis in humans has been reported from many countries such as Taiwan, Ouganda, and India with symptoms that include vomiting, abdominal pain, pulmonary edema, convulsions, coma, and death with cerebral edema and fatty involvement of the liver, kidney, and heart.

Expression of aflatoxin-related diseases in humans may be influenced by age, sex, nutritional status, and/or concurrent exposure to other causative agents such as viral hepatitis (HBV) or parasitic infestation. Ingestion of aflatoxin, viral diseases, and hereditary factors have been suggested as possible aetiological agents of childhood cirrhosis. There is evidence that children, malnourished as well, exposed to aflatoxin breast milk, contaminated food and unrefined groundnut oil may develop cirrhosis. Though suggestions have been made that aflatoxin could be an aetiological agent of Reye's syndrome in children in Thailand, New Zealand, etc, there is no conclusive evidence of it. Epidemiological studies have shown the involvement of aflatoxins in Kwashiorkor in malnourished children.

Effects on animals

Aflatoxin lowers resistance to diseases and interferes with vaccine-induced immunity in livestock (Diekman and Green 1992). Suppression of immunity by aflatoxin B1 has been demonstrated in turkeys, chickens, pigs, mice, guinea pigs, and rabbits (Sharma 1993). Swine, ducks, and rainbow trout are very susceptible to it. Broiler chickens are more susceptible to aflatoxin than layer-type chickens. Pale, friable, fatty livers may be evident in acute aflatoxicosis in poultry. Symptoms of acute aflatoxicosis in mammals include inappetance, lethargy, ataxia, rough hair coat, and pale, and enlarged fatty livers. Symptoms of chronic aflatoxin exposure include reduced feed efficiency and milk production, icterus, and decreased appetite (Nibbelink 1986). The mechanism by which aflatoxins reduce growth rate is probably related to disturbances in protein, carbohydrate and lipid metabolism (Cheeke and Shull 1985). Depending on interactions with other factors, aflatoxin concentrations as low as 100 ppb may be toxic to beef cattle, however the toxic level is generally considered to be between 300 to 700 ppb. Garrett et al. (1968) showed an effect on weight gain and intake with diets containing 700 ppb aflatoxin, but not with 300 ppb. Trends in the data suggest that toxicity may occur at the lower concentrations of aflatoxin.

Cellular affects

Aflatoxins are inhibitors of nucleic acid synthesis due to their high affinity for nucleic acids and polynucleotides. They decrease protein synthesis, lipid metabolism, and mitochondrial respiration, leading to accumulation of lipids in the liver causing fatty liver. Carcinogenesis has been observed in rats, ducks, mice, trout (most susceptible), and subhuman primates, but rarely seen in poultry or ruminants There is a correlation between aflatoxin presence and increased liver cancer in individuals who are Hepatitis B carriers.

Total maximum aflatoxin levels fixed by different countries for groundnuts/all food products (Codex Alimentarius Commission, 2013). 

Country

Product

Aflatoxin

Maximum level (µg/kg)

China, Japan, Thailand, Egypt, Turkey

Groundnuts

Total

10

Indonesia, Malaysia, Taiwan province of China, Australia

Groundnuts

Total

15

EU

Groundnuts

Total

4*/15**

Kenya

Groundnuts

Total

20

Russia

Groundnuts

B1

5

Canada

Nuts and nut products

Total

15

India

All food products

Total

30

Philippines

Nuts and products

Total

20

Singapore

Nuts

Total

5

USA

All foods except milk

Total

20

Vietnam

Food stuffs

Total

10

*Standard for groundnut meant for direct human consumption.

**Standard for groundnut meant for further processing. 

C) Losses

About 25% of the world's food crops are significantly contaminated with mycotoxins (FAO 1999).  According to a World Bank study, the European Union regulation on aflatoxins costs Africa $ 670 million each year in exports of cereals, dried fruit and nuts. Wu 2004 calculates that there would be approximately $450 million annual loss to all food exporters if all nations harmonized to EU aflatoxin standards. Only 15 countries in Sub-Saharan Africa have regulations governing aflatoxins, thus making the trade challenging.

The Center for Disease Control has estimated that more than 4.5 billion people in developing countries are chronically exposed to aflatoxins in their diets. These have       

significant negative impacts on health, food and nutritional security and incomes at the household, community and national levels (Coulibaly et al., 2008). Health risks decrease labor productivity, while increasing health costs and overall income losses due to opportunity costs linked to lost days of work (Lubulwa and Davis 1994). 

Dr Njoroge during a field visit to the aflatoxin mitigation trials in Zambia.
Photo: E Musukwa
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People gather to watch a short video animation on mould and how it infects groundnuts.
Photo: S Sridharan, ICRISAT


Kit to detect aflatoxin contamination
ICRISAT


An ICRISAT scientific Officer trains farmers on integrated aflatoxin management in Kouyou village, Mali.
ICRISAT


Aflatoxin contamination levels are high during end-of-season drought.
ICRISAT


Participants in the aflatoxin resistance screening field at ICRISAT headquarters.
Photo: L Vidyasagar, ICRISAT


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