Assessing the impact of aflatoxin consumption on animal health and productivity.
Malnutrition, including micronutrient deficiencies, is a major problem in East Africa. Animal source foods are essential sources of protein and micronutrients and could contribute to improving nutritional security. Indeed the livestock sector in East Africa is growing rapidly in response to increased demand . Production gains can be obtained most readily by intensifying short cycle species (poultry and pigs) and dairy and egg production. But as these livestock systems intensify, they rely more on nutrient dense feeds (concentrates). Commonly used livestock feeds are based on maize, groundnuts, soybean products, oil cake, fishmeal and brewers' grains, all of which are prone to contamination with aflatoxins .
Aflatoxins are produced by the fungi Aspergillus flavus, A. parasiticus and occasionally other Aspergillus species ; they are common contaminants of foods and feeds in tropical and sub-tropical regions. At least 20 types of aflatoxin naturally occur, but only four types are commonly found in plant based foods; these are called aflatoxin [B.sub.1], [B.sub.2], [G.sub.1] and [G.sub.2]. When animals consume aflatoxins [B.sub.1] and [B.sub.2], some is converted in the liver to the metabolites aflatoxin [M.sub.1] and [M.sub.2]; these are rapidly excreted in milk and urine . Aflatoxins may also be carried over from feed to poultry eggs and some remains in the body as residues in meat and organs [5, 6]. Aflatoxins can also be present in animal source foods as the result of accidental contamination of livestock products with Aspergillus fungi or deliberate introduction during mould fermenting of animal source foods .
Aflatoxin consumption causes liver cancer in people and has been associated with stunting and other health problems [8-14]. Consumption of very high levels of aflatoxins by animals also results in severe, sudden onset illness and death. Aflatoxicosis was first identified when more than 100,000 turkeys died in the United Kingdom and feed containing contaminated groundnuts imported from Brazil was implicated . Since then, field outbreaks causing morbidity and mortality have been well documented in turkeys, laying hens, pigs, cattle, rainbow trout and dogs . No exclusively livestock outbreaks have been reported from East Africa; however, in a major Kenyan outbreak, affected households reported the death of their pet dogs, probably due to aflatoxin ingestion . Adverse impacts are more severe where there is co-contamination with other mycotoxins [2, 18]. Consumption of lower levels of aflatoxins can cause liver damage, gastrointestinal dysfunction, immunosuppression, decreased appetite, decreased reproductive function, decreased growth and decreased production .
Toxicity is influenced by environmental factors, exposure level and duration of exposure in tandem with age, health and nutritional status . Foetuses are very susceptible to even low levels of aflatoxins and young and fast-growing animals are more affected than adults; some authors have reported that females are more affected than males . Aflatoxin [B.sub.1] ([AFB.sub.1]) is considered the most toxic and is produced by both A. flavus and A. parasiticus. [AFB.sub.1] is carcinogenic and teratogenic in both humans and animals. To date, [AFB.sub.1] is the only mycotoxin classified as a Group 1a human carcinogen by the International Agency for Research on Cancer .
Most aflatoxin research has focused on aflatoxins in grains and their impacts on human health. The objective of this review was to synthesize information on this important but neglected area by conducting a systematic literature review on the impact of aflatoxins on livestock health and productivity, with a special focus on East Africa.
A systematic literature review was undertaken following PRISMA  guidelines to capture information on aflatoxin impacts on livestock health and productivity, and the risks associated with aflatoxin contamination of animal feeds and animal source foods (dairy products, meat, eggs, fish, other aquatic foods and honey). Twenty-three (23) databases were searched using a combination of the MESH terms: Africa, sub-Saharan Africa, swine, pigs, poultry, chickens, layers, broilers, dairy, goats, sheep, shoats, cattle, cows, fish, animal feed, animal source foods, livestock, aflatoxin and mycotoxin. Abstracts of identified papers were read, and if relevant to the review objective, full papers were obtained. Information from the papers was captured using a Microsoft Excel template. Data were categorised by natural or experimental exposure and by species, breed and age.
Identified papers used different units for measuring aflatoxin levels. For consistency in this article, units were converted to parts per billion (ppb) which is equivalent to pg/kg; or parts per trillion (ppt), which is equivalent to ng/kg.
An initial 2700 papers were identified as part of a broader systematic literature review to capture information on aflatoxin prevalence, risk factors and control options and costs to support risk maps and evidence around costs and controls. After screening for relevance to animal health and productivity, 46 full papers, which were available and had information relevant to the review, were retained for data extraction and inclusion in this report, which emphasizes papers from East Africa.
Livestock sector in East Africa
The dairy cattle population of the East African Community (EAC) is estimated at 16.4 million, of which 5.5 million are improved breeds. The commercial poultry population is estimated at 8 million in Kenya, 6.5 million in Uganda, 1.7 million in Tanzania and 1.6 million in Rwanda; the sector is less developed in Burundi . The commercial pork sector is estimated at 150,000 pigs in Kenya and is under-developed in other EAC countries. Uganda is experiencing massive expansion of the pork sector . However, this growth is mainly in the smallholder sector, mostly managed by women and children in backyard activities .
Kenya produces about 500,000 tonnes of animal feed per year  and Tanzania 800,000 tonnes . In Uganda the annual production of compound feeds by the commercial feed millers is estimated at about 80,000 tonnes  with around half produced by small-scale mixers . Approximately 70% of the feeds produced in Kenya are poultry feeds  and this may also be the case in other East African countries, as their livestock sectors are broadly similar.
A study from 1982 reported a significant decrease in milk production when dairy cattle (n=10) were experimentally fed 13,000 ppb un-purified aflatoxin per day for seven days, compared to dairy cattle on an aflatoxin free diet; feeding the same amount of pure aflatoxin had no effect . A 1979 study showed that a dairy herd exposed to contaminated maize (120 ppb) for several months had severe health problems, including the birth of small and unhealthy calves, diarrhoea, acute mastitis, respiratory problems, rectal prolapse and hair loss. Milk production was decreased by 28% and breeding efficiency by 2% . A review by Gallo summarises four earlier studies, all showing decreased milk yield in cattle as a result of aflatoxin exposure .
Many aflatoxin exposure studies in dairy cattle have aimed to determine carryover rates to milk or to determine the presence and levels of aflatoxin [M.sub.1] ([AFM.sub.1]) in milk. The results show that the amount of [AFM.sub.1] excreted in milk is around 1-7% of the total amount of [AFB.sub.1] ingested [32, 33]. Higher levels were seen in high yielding cows. However, in EAC, average milk yields are low . The threshold for aflatoxin excretion in cows' milk is 15 ppb in their feed .
Overall, studies in chickens found that experimental feeding of aflatoxins reduced body weight, feed conversion efficiency, average daily gain and feed conversion ratios (Table 1). Broilers were more susceptible than layers [35, 36]. Productivity losses in commercial broiler operations can occur when aflatoxin concentrations are below those levels of concern established by research in laboratory situations . A case study in South Africa found that broiler houses with poor growth and ascites had consistently higher levels of aflatoxin in feed than samples from broiler houses without problems (18 ppb versus 9 ppb) . A meta-analysis of studies done on the effect of aflatoxins on growth performance found that, for every 1000 ppb increase of aflatoxin in the diet, the growth rate in broilers would be reduced by 5% . In laying hens, aflatoxin consumption is associated with reduction in egg production, egg weight and yolk weight as well as changes in yolk colour, shell weight and shell integrity .
In chickens, impaired immune response can occur at levels that have no effect on growth rate . Experimental studies found that exposure of chickens to 200 ppb aflatoxin in feed in conjunction with vaccination against Newcastle disease and two other commonly used vaccines resulted in lack of adequate protection against subsequent experimental exposure to disease . The interaction of infectious bursal disease (IBD) and aflatoxicosis led to an increased mortality of 35.6% when compared to 3-21% mortality with IBD alone and 0.03% mortality with aflatoxicosis alone .
Turkeys and ducks are highly susceptible to aflatoxins, more so than chickens. A review of several studies reported that the [AFB.sub.1] contamination level needed to impair production was 800 ppb in chickens, 700 ppb in geese and quail, 500 ppb in ducks and 400 ppb in turkeys . Turkey X disease (caused by aflatoxins in imported feed), appears to have led to salmonellosis and candidiasis outbreaks . Dietary aflatoxins caused liver damage in ducks while no damage was recorded in chickens . In Zimbabwe, 70 ostriches died after being fed aflatoxin-contaminated commercial pelleted feed. Samples found levels of 11, 55, 98 and 129 ppb, suggesting ostriches are more susceptible to aflatoxins than chickens . Quail appear more susceptible than chickens . In one experiment, laying quail were fed 25, 50 or 100 ppb of aflatoxin. Average weight and egg production were not affected but in groups receiving 50 ppb and above, egg weight was lower, while liver lesions were seen at 200 ppb .
Pigs are highly susceptible to aflatoxins. Clinical signs of acute aflatoxicosis include anorexia, nervous signs and sudden death . Acute and peri-acute signs were evident after pigs ingested peanut screenings contaminated with 22,000 ppb aflatoxin, while sub- acute aflatoxicosis due to ingestion of sorghum with levels of 4640 ppb led to death in weeks . Experimental intoxications have shown damaged white blood cells in piglets, indicating a loss of immune competence .
Studies on pigs show reduced weight gain and feed conversion ratios to different extent (Table 2). A meta-analysis of experimental studies in swine reviewed 85 articles published between 1968 and 2010 . Aflatoxin effects were greater in younger animals and at higher doses. For each additional 1000 ppb of aflatoxin in the feed, there was a reduction of 3.9% in pig weight gain. The authors also reported methionine and protein were protective, improving the feed intake and the weight gain in challenged animals. Another meta-analysis of studies done on the effect of aflatoxins on growth performance in pigs found that for every 1000 ppb increase of aflatoxin in the diet, the growth rate in pigs would be reduced by 16% . Additionally, in this study, dietary concentrations that would cause a 5% reduction in growth rate were estimated at 300 ppb for pigs. Aflatoxin [B.sub.1], [AFG.sub.1] and [AFM.sub.1] can be present in the sow's milk and different levels are possible depending on the initial contamination of the feed .
Lewis et al.  showed that feeding sheep 1750 ppb aflatoxins for 3.5 years led to nasal and liver tumours in three out of eight sheep. A study in Nigeria exposed West African dwarf goats to 0, 50, 100 and 150 ppb of aflatoxins and found dose dependent decreases in weight gain, concentrate intake, feed conversion ratios and mortality .
Fish vary in susceptibility to aflatoxins but toxic signs such as feed refusal, jaundice, weight loss, feed efficiency reduction, liver dysfunction and cellular damage are commonly observed . Nile tilapia is widely farmed in tropical and subtropical regions. There have been several studies on the impact of aflatoxin consumption and growth rates, with variable results. A diet with 100 ppb for ten weeks significantly reduced growth , yet a diet with 250 ppb led to no adverse effects . More recent, larger and longer term trials show no difference in weight gain at 85 ppb but significantly less weight gain at 245 ppb and above .
Honeybees are relatively resistant to aflatoxins. One study found 1000 ppb and 2500 ppb diet of [AFB.sub.1] did not have any apparent toxic effects on bees. A higher dose of 5000 ppb caused less than 50% mortality after 72 hours. Doses of [AFB.sub.1] above 10,000 ppb caused over 90% mortality in 72 hours . Fresh honey collected in Palestine was contaminated with aflatoxins at levels ranging from 0.5-22 ppb . The origin of contamination was not determined, but the research showed that honeybees can be naturally affected by aflatoxins.
Only a small number of studies were identified from East Africa. Studies from Kenya found that feed samples were contaminated with aflatoxin ranging from 5.13-1123 ppb [59, 60]. One three-year study found only 5% of samples were below the regulatory limit of 10 ppb and 35% of feed samples had more than 100 ppb . A survey in Tanzania found broiler feed samples had on average 36 ppb aflatoxins and layer feed 15 ppb . A recent study from Ethiopia sampled cattle feed from peri-urban Addis Ababa. Out of a total of 156 feed samples collected, only 16 (10%) contained [AFB.sub.1] at a level less than or equal to 10 ppb, while 26% exceeded 100 ppb .
In East Africa, as elsewhere, maize is an important component of poultry feed. Dairy feed sources appear to be more diverse and, at least in Ethiopia, maize is used less often . There are several reports on aflatoxin contamination of maize in East Africa but presence in maize is not a good indicator of presence in feed because (a) some farmers are known to channel worst quality maize to animal feed and (b) some feed manufacturers may test for aflatoxin.
Animal source foods
A limited number of surveys in East Africa have assessed aflatoxin levels in milk. Across five papers reviewed, aflatoxin was detected in 45-100% of milk samples and in all surveys some samples had levels exceeding 0.05 ppb [59-61, 63, 64], the European Union standard for acceptable aflatoxin levels in milk. No studies were found that assessed the aflatoxin levels in eggs or meat in East Africa.
This wide-ranging review allows some broad conclusions to be drawn, which can inform strategies to address the problems of livestock production in sub-Saharan Africa. Consumption of aflatoxins by livestock and fish seriously reduces their productivity. Chronic aflatoxicosis probably has greater economic impacts than acute disease, as acute disease has never been reported but livestock are exposed to un-controlled aflatoxin through feed. Typically, animals show a worsening in feed conversion ratio, a decrease in average daily gain and decrease in body weight for animals experimentally fed aflatoxins; this has been reported by other reviews .
Different species differ widely in their susceptibility to aflatoxins. The age of the animals also plays an important role. Therefore, management should be differentiated by species, age and other relevant factors. Generalising across the papers we identified, dietary levels of aflatoxin (in ppb) generally tolerated are [less than or equal to] 50 in young poultry, [less than or equal to]100 in adult poultry, [less than or equal to] 50 in weaned pigs, [less than or equal to] 200 in finishing pigs, <100 in calves, <300 in cattle and <100 in Nile tilapia. However, ill effects may be observed at lower levels, especially if animals are exposed to other stressors. Conversely, in other studies reviewed, no ill effects were evident at considerably higher levels. As mentioned, mycotoxins may interact and therefore health effects can be difficult to predict based only on studies of aflatoxins. Papers reviewed also suggested that the decrease in body weight due to aflatoxin exposure can be partially improved by exercise, increased dietary protein, increased dietary methionine and good environmental conditions.
This literature review also shows some inconsistencies between studies. Some studies show impacts in commercial herds/flocks at levels below those shown to cause impacts in laboratory trials. Some studies show impacts at low levels of aflatoxins while others do not show impacts even at high levels. In the first case, this could be because animals are exposed to multiple stressors in real life and could also be ingesting a mixture of mycotoxins. Confounding factors may include food quality, exercise, breed and age of animals or the trials being too short or having too few animals to detect any clinical effects.
Nearly 18 million poultry and over five million dairy cattle in East Africa are dependent on livestock feed. Yet few studies have examined aflatoxin contamination of feeds in East Africa. The limited information suggests a substantial proportion of this feed is contaminated at levels likely to reduce milk, egg and poultry meat production. Aflatoxin levels in milk are also of concern especially because milk consumption is often higher among infants and children, who are likely to be more vulnerable.
THE WAY FORWARD
As livestock systems intensify, problems with aflatoxins are likely to worsen. This could be compounded if the larger regulatory framework to address aflatoxin in the human food supply is strengthened, possibly resulting in an increased flow of rejected and highly contaminated grains entering the commercial and informal feed supply chains. In East Africa, livestock are often subject to other stressors such as disease and malnutrition, making them more vulnerable to disease and enhancing the effects of aflatoxins.
Even though there are relatively few studies on feed and animal source foods in East Africa, evidence suggests that aflatoxins are a problem in the livestock sector. However, to characterize the extent of the problem and its trends, further information is needed. This could be obtained through prevalence surveys to assess the extent of feed contamination, epidemiological studies to measure the impact on animal health and productivity, risk assessments to estimate the danger posed to human health by aflatoxin residues in milk and other animal source foods, and spatial mapping of aflatoxin prevalence and risk factors.
In parallel with these studies, better evidence is needed on the most appropriate management of aflatoxins in the livestock and aquaculture sectors. There are several technical options including biological control, testing feedstuffs, aflatoxin binders, anti-fungal agents, blending down and directing contaminated feed to least susceptible animals . Longer-term options include breeding for resistance in animals and breeding for lower susceptibility in crops . Other institutional approaches focus on policy change, regulation implementation, improved testing or market-based approaches . However, there is little evidence on the efficacy, sustainability, costs and benefits of proposed interventions under conditions unique to sub-Saharan Africa. Furthermore, the policy environment is not enabling within many countries. Operational research into these and other management options can be done in parallel with studies to better characterize the problem and initiatives to create a more enabling policy environment.
Also of importance is a better understanding of the role of livestock and aquaculture to supply essential macronutrients and micronutrients for public health, especially among vulnerable groups, whose nutritional status and food security can either be enhanced or eroded under various new regimes to address aflatoxin contaminated feeds and animal by-products.
Globally, aflatoxins are considered the most important contaminant of animal feed. Evidence is emerging that they are also a problem in East Africa. Understanding the risks associated with aflatoxins and the best ways to mitigate them will be important to the development of East Africa's burgeoning livestock sector.
The CGIAR Research Program on Agriculture for Nutrition and Health, led by the International Food Policy Research Institute, and the International Institute of Tropical Agriculture.
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Atherstone C (1) *, Grace D (2), Lindahl JF (2, 3), Kang'ethe EK (4) and F Nelson (5)
Corresponding author email: email@example.com
(1) International Livestock Research Institute, P.O. Box 24384, Kampala, Uganda
(2) International Livestock Research Institute, P.O. Box 30709-00100, Nairobi, Kenya
(3) Swedish University of Agricultural Sciences, P.O. Box 7054, SE-750 07 Uppsala, Sweden
(4) University of Nairobi, P.O. Box 29053-00625, Nairobi, Kenya
(5) International Institute of Tropical Agriculture, P.O. Box 34441, Dar es Salaam, Tanzania
Table 1: Published studies on the impact of aflatoxins in chickens on feed conversion ratio (FCR) and average daily weight gain (ADG) Animal Aflatoxin dose and Results Study duration of experiment Chickens 0 (A), 300 (B), 1250 Decrease in body  (n=900) (C) 2000 (D) ppb for weight and food 28 days intake. Increase in FCR (p<0.001) Broiler 0 (A), 5000 ppb feed Decrease in body chicks (B), exercise only weight in (n=40- (C), 5000 ppb feed + aflatoxin-treated  48) exercise (D) for 24 group which can be days partially improved by exercise (p<0.01 between birds fed aflatoxins and control). Increase in FCR in aflatoxin treated group. Layer 0 (A), 5000 ppb feed Decrease in body chicks (B), exercise only weight in  (n=40- (C), 5000 ppb feed + aflatoxin-treated 48) exercise (D) for 33 group, which can be days partially improved by exercise (p<0.01 between birds fed aflatoxins and control). Increase in FCR in aflatoxin treated group. Broiler 0 (A), 5000 ppb feed Decrease in body chicks (B), exercise only weight in  (n=40- (C), 5000 ppb feed + aflatoxin-treated 48) exercise (D) for 39 group, which can be days partially improved by exercise. No difference in FCR. Broiler 0 (A), 75 ppb (B), 225 Decrease in body  chickens ppb (C) and 675 ppb weight in all (n=75) (D) feed for seven aflatoxin-treated weeks groups (p<0.05) Broiler 0 (A), 300 (B), 900 Decrease in body chickens (C) and 2700 (D) ppb weight in only 2700  (n=75) feed for seven weeks ppb feed group (p<0.05) One-day-old 0 (A), 625 (B), 1250 Aflatoxin broilers (C), 2500 (D), 5000 dose-dependent  (n=70) (E) and 10,000 (F) ppb decrease in body feed for three weeks weight at the dose 1250 ppb and higher (p<0.05) Day-old 0 (A), 2500 (B), 5000 Aflatoxin  chicks (C), and 10,100 (D) dose-dependent (n=120) ppb feed for four decrease in body weeks weight (p>0.05) One-day- 0 (A), 1000 (B) and Aflatoxin old broiler 4000 (C) ppb feed for dose-dependent  and layer four weeks decrease in body chicks weight (p>0.05) (n=40 each) Table 2: Published studies on the impact of aflatoxins in pigs on feed conversion rate (FCR), average daily weight gain (ADG) and average daily feed intake (ADFI) Animal Aflatoxin dose and Results Study duration of experiment Pigs 0 (A), 200 (B), 700 (C), No significant  (n=50) 1100 (D) ppb feed for difference in body 16 weeks weight between groups. Dose related increase in FCR (p<.05) Pigs 0 (A), 1000 (B), 2000 Dose related increase  (n=60) (C), 4000 (D) ppb feed in FCR (p<.001) for 13 weeks Pigs, <2 (A), <8 (B), 51 (C), No significant effect  weanlings 105 (D), 233 (E) ppb on weight gain or feed (n=110) feed for 120 days conversion Pigs, <6 (A), 45 (B), 615 Decrease in ADG at the  weanlings (C), 810 (D) ppb feed dose of 615 and 810 ppb (n=110) for 120 days feed (p<.05) Pigs 20 (A), 385 (B), 750 Dose related decrease  (n=32) (C), 1480 (D) ppb in in ADG and ADFI (p<.05) feed (control: 20 ppb Increase in FCR in the group) 1480 ppb group (p<.05) Pigs, 5-6 0 (A), 300 (B) and 500 Decrease in weight gain  week old (C) ppb feed for 10 and feed consumption in (n=30) weeks high-dose group compared with controls (p<.01) Pigs, 0 (A), 420 (B), 840 (C) Decrease in ADG and  weanlings ppb feed for 49 days increase in FCR (p (n=90) <.01) Pigs, 0 (A) and 800 (B) ppb Decrease in ADG  weanlings feed for 42 days (n=63) Pigs, 0 (A) and 992 (B) ppb Decrease in ADG (p<.01)  weanlings feed for 6 weeks (n=96) Pigs, 0 (A) and 880 (B) ppb Decrease in ADG and  weaned feed for 4 weeks ADFI (p<.05) Increase (n=54) in FCR (p<.05) Pigs, 0 (A) and 500 (B) ppb Decrease in ADG and  weaned feed for 5 weeks ADFI (p<.05) (n=81) Pigs, 0 (A) and 800 (B) ppb Decrease in ADG (p<.05)  weaned feed for 4 weeks and ADFI (p<.01) (n=63) Pigs, 0 (A) and 3000 (B) ppb Decrease in weight gain  growing feed for 28 days (p<.05) barrow (n=40) Pigs 0 (A), 2500 ppb feed Decrease in bodyweight  (n=27) (B), 2500 ppb feed + feed consumption 2400 IU tocopherol (C) (p<.05) for 32 days Pigs 0 (A), 2500 ppb feed Decrease in bodyweight,  (n=18) (B), 2500 ppb feed + weight gain and feed 100mg fumonisin B1/kg consumption feed (C) for 35 days Pigs, 4 0 (A), 240 (B), 480 (C) Decrease in ADG (p<.05)  week old ppb feed for 30 days weaned (n=36)
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|Author:||Atherstone, C.; Grace, D.; Lindahl, J.F.; Kangethe, E.K.; Nelson, F.|
|Publication:||African Journal of Food, Agriculture, Nutrition and Development|
|Date:||Jul 1, 2016|
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