The field of health economics has made great strides in the last several decades. Health economics strives to quantify health benefits or costs in such a way as to be comparable to monetary benefits or costs. Otherwise, it can be difficult to understand the extent to which a particular risk affects human society, especially if death is not a significant outcome; or, conversely, how much a public health intervention benefits human society, if there is not a direct market outcome. Putting monetary values on these health outcomes aids policymakers in understanding how important a risky agent or a disease is, how useful an intervention might be, and how to compare the relative importance of risks and the relative effectiveness of interventions.
Much of the literature in health economics focuses on medical treatments, with relatively fewer applications in food and agriculture. Examples of health economic assessments of food additives include a study of the potential cost-effectiveness of transgenic golden rice in reducing vitamin A deficiency (Stein et al. 2008
), and a study of the cost-effectiveness of biofortifying foods to reduce micronutrient deficiency (Meenakshi et al. 2007
). Havelaar (2007)
provides a notable example of estimating the health-related costs of food contaminants: foodborne zoonoses (e.g., caused by Campylobacter, Salmonella
, and Cryptosporidium
) in Europe.
It is also important to consider the economic impacts of other food contaminants, such as mycotoxins (toxins of fungal origin). In particular, aflatoxin, the most toxic and carcinogenic of the known mycotoxins, imposes an enormous socioeconomic cost to human society. In industrial nations, it is relatively straightforward to estimate the cost of aflatoxin, because the costs are primarily market-related (Wu 2004
; Wu et al. 2008
). Namely, commodities that contain aflatoxin levels exceeding regulatory guidelines for human food or animal feed are discarded, or sold at a lower price for a different use. It is possible to estimate the cost of aflatoxin to a particular commodity group by estimating how much of the commodity must be discarded or discounted due to aflatoxin contamination.
In less developed countries (LDCs), however, estimating the total socioeconomic cost of aflatoxin is more complex. Health-related costs are almost certainly much higher than market-related costs (Williams 2008
), and more difficult to valuate. One notable assessment of aflatoxin's social costs is that of Lubulwa and Davis (1994)
, in which both trade and health costs were estimated in Thailand, Indonesia, and the Philippines. Indeed, aflatoxin primarily affects food in tropic and subtropic regions of the world, and is especially a scourge in nations where agricultural systems are poorly equipped to handle food safety risks. Suboptimal field practices and poor storage conditions make the crops vulnerable to fungal infection and subsequent aflatoxin accumulation. Maize and groundnuts (peanuts), the two crops most conducive to aflatoxin contamination, are staples in the diets of many people worldwide, increasing aflatoxin exposure where dietary variety is difficult to achieve (Shephard 2008
). Though nations suffering these risks have nominally established maximum allowable aflatoxin standards in food, there is very little enforcement of these standards. Subsistence farmers and local food traders sometimes have the luxury of discarding obviously moldy maize and groundnuts. But in drought seasons, or situations of food insecurity, oftentimes people have no choice but to eat moldy food or starve. For example, more than 125 people died due to acute aflatoxicosis in Kenya when food insecurity, caused by a variety of climatic and social reasons, led to widespread consumption of maize contaminated with high levels of aflatoxins (Lewis et al. 2005
Thus, regulations do little to help reduce aflatoxin and its related health effects in less developed countries (Shephard 2008
, Williams 2008
). Rather, the focus should be on promoting the adoption of strategies that can control aflatoxin and its associated health risks, in the field, in postharvest conditions, or in the diet.
Health effects of aflatoxin
Aflatoxins are primarily produced by the fungi Aspergillus flavus
and A. parasiticus
, which colonize a wide variety of food commodities including maize, oilseeds, spices, groundnuts, tree nuts, milk, and dried fruit (Strosnider et al. 2006
). Aflatoxin B1
, the most toxic of the aflatoxins, is the most potent naturally occurring chemical liver carcinogen known. Cytochrome P450 enzymes in the liver can metabolize aflatoxin into an epoxide (aflatoxin-8,9-epoxide), which can bind to proteins and cause acute toxicity (aflatoxicosis), or to DNA and induce hepatocellular carcinoma (HCC), a form of liver cancer.
Acute aflatoxicosis, characterized by hemorrhage, acute liver damage, edema, and death, is associated with extremely high doses of aflatoxin. In recent years, hundreds of acute aflatoxicosis cases in Kenya have been associated with consumption of contaminated home-grown maize (Azziz-Baumgartner et al. 2005
HCC as a result of chronic aflatoxin exposure has been well documented, presenting most often in persons with chronic hepatitis B virus (HBV) infection (Qian et al. 1994
, Groopman et al. 2008
). For individuals chronically infected with HBV, aflatoxin consumption raises by up to thirty-fold the risk of liver cancer compared with either exposure alone (Groopman et al. 2005
). Unfortunately, these two risk factors – aflatoxin and HBV – are especially prevalent in poor nations worldwide.
Aflatoxin exposure is also associated with immune system disorders and diminished weight and height in children. Over three decades of animal studies have found that aflatoxin may have immunosuppressive impacts (Jolly et al. 2008
). Aflatoxin and immunosuppression in humans has been relatively less well-characterized, but could in fact have enormous significance from a global health perspective (Williams et al. 2004
). Several recent human studies have shown evidence of immunomodulation (Turner et al. 2003
, Jiang et al. 2005
, Jiang et al. 2008
), though the actual outcomes of such immunomodulation have yet to be characterized in humans. Indeed, aflatoxin's immunotoxicity may be one explanation for the stunted growth in children that appears to follow a dose-response relationship with aflatoxin exposure (Gong et al. 2002
, Turner et al. 2003
). Another explanation may be altered intestinal integrity (Gong et al. 2008
Aflatoxin control strategies
Multiple public health interventions exist by which to control aflatoxin or its burden in the human body, to prevent HCC (Strosnider et al. 2006
). Several of these are listed in .
A sampling of interventions to reduce aflatoxin risk in field, dietary, and clinical settings.
Interventions to reduce aflatoxin-induced illness can be roughly grouped into three categories: agricultural, dietary, and clinical. Agricultural interventions are methods or technologies that can be applied either in the field (“preharvest”) or in drying, storage and transportation (“postharvest”) to reduce aflatoxin levels in food. Agricultural interventions can thus be considered “primary” interventions, because they directly reduce aflatoxin in food. Dietary and clinical interventions can be considered “secondary” interventions. They cannot reduce actual aflatoxin levels in food, but they can reduce aflatoxin-related illness; either by reducing aflatoxin's bioavailability in the body (e.g., through enterosorption) or by ameliorating aflatoxin-induced damage (e.g., through induction of Phase II enzymes that detoxify the aflatoxin-8,9-epoxide).
Our case studies focus on the health economics and cost-effectiveness of two interventions to reduce aflatoxin: biocontrol in preharvest conditions, and a postharvest intervention package to reduce aflatoxin in storage.
Biocontrol through atoxigenic Aspergillus strains
Biocontrol broadly refers to the use of organisms to reduce the incidence of pests, diseases, or toxins (Pitt and Hocking 2006
). The biocontrol strategy analyzed in this study refers to field application of atoxigenic strains of Aspergillus flavus
that can competitively exclude toxigenic strains from colonizing crops and thereby reduce aflatoxin concentration (Cotty et al. 2007
Biocontrol methods for aflatoxin reduction in corn, groundnuts, and pistachios have been demonstrated under field conditions; and are being used commercially in some parts of the United States, in select commodities. Cotty and Bhatnagar (1994)
found multiple strains of atoxigenic A. flavus
that could inhibit aflatoxin production of toxigenic strains in vitro
, but one in particular, AF36, that also lowers aflatoxin concentration in cottonseed in the field, by out-competing the toxigenic strains. AF36 has a defective polyketide synthase gene (Ehrlich and Cotty 2004
), which is required for aflatoxin biosynthesis. Dorner et al. (1999)
achieved successful aflatoxin reduction in maize through use of atoxigenic A. flavus
strains in preharvest field conditions. Inoculating corn with atoxigenic strains of A. flavus
has been shown to reduce aflatoxin contamination (Abbas et al. 2006
In AF36 applications, wheat seeds are coated with conidia of the AF36 atoxigenic strain, and these seeds are applied to cotton fields at a strategic time so that the atoxigenic strains competitively exclude toxigenic strains. Significant reductions in aflatoxin contamination in cottonseed have been achieved where AF36 has been approved for application to cotton (Arizona, Texas, and California) (Cotty et al. 2007
). Afla-Guard™, another commercially available product for aflatoxin biocontrol in the US, is applied primarily to groundnut fields. Pearl barley grains are coated with conidia of an atoxigenic strain of A. flavus
, and these grains are applied to groundnut fields to provide competitive exclusion of toxigenic strains. Similar to AF36, Afla-Guard™ achieved high levels of protection against aflatoxin contamination in peanuts.
Wu et al. (2008)
evaluated the cost-effectiveness of AF36 in US cottonseed and Afla-Guard™ in US groundnuts, through an assessment of market benefits from commodities with reduced aflatoxin contamination compared with the cost of the products. Both of these aflatoxin biocontrol methods were shown to be cost-effective in most years under most conditions in the US (Wu et al. 2008
), with AF36 having the greater margin of benefit because of the lower cost of product. However, these results are not directly generalizable to nations where aflatoxin losses are more related to health rather than to market deductions.
Importantly, atoxigenic A. flavus
strains have been found in sub-Saharan Africa, which show promise for controlling aflatoxin in African crops (Bandyopadhyay et al. 2005
, Atehnkeng et al. 2008
). In field trials involving inoculation of maize with toxigenic vs. atoxigenic isolates of A. flavus
, naturally occurring atoxigenic isolates found in Nigerian soils showed a 70.1% to 99.9% reduction in aflatoxin levels, compared with the toxigenic isolates (Atehnkeng et al. 2008
Selecting appropriate atoxigenic Aspergillus
strains for application is a complex task (Bandyopadhyay et al. 2005
, Pitt and Hocking 2006
). Pitt and Hocking (2006)
describe five criteria for the choice of strains: 1) they should be unable to produce toxins; 2) they should be unlikely to revert or incapable of reverting to toxicity; i.e., they should be genetically stable; 3) they must be competitive with naturally occurring toxigenic strains under field conditions; 4) they should be naturally occurring rather than mutated or genetically modified; and 5) they should be produced and applied in such a way as to ensure operational safety, as A. flavus
is a known human pathogen, particularly to immunocompromised individuals. Bandyopadhyay et al. (2005)
further note that the strains' propensity to multiply, colonize and survive are other selection criteria, to minimize the necessary number of applications after the atoxigenic strains have been introduced into the environment.
Postharvest intervention package to reduce aflatoxin
Suboptimal postharvest conditions may be responsible for the greatest part of aflatoxin accumulation in food crops in LDCs. Improper drying, poor storage conditions such as excessive heat and moisture, insects and other pests, and consumption of food that has remained in storage for months (if not years; Hell et al. 2000
) all contribute to dangerous aflatoxin exposures. Indeed, much aflatoxin contamination of food takes place during postharvest storage, as opposed to in preharvest conditions (Wild and Hall 2000
). Hence, controlling aflatoxin in postharvest settings is crucial.
Turner et al. (2005)
described a postharvest intervention package to reduce aflatoxin in groundnuts, tested in Guinea. The package consisted of six components: education on hand-sorting nuts, natural-fiber mats for drying the nuts, education on proper sun drying, natural-fiber bags for storage, wooden pallets on which to store bags, and insecticides applied on the floor of the storage facility under the wooden pallets.
After five months in the Guinea intervention study, individuals who had received the postharvest intervention package had on average 57.2% lower aflatoxin-albumin concentrations in the blood (8 pg/mg), compared with individuals in the control group (18.7 pg/mg; Turner et al. 2005
). Indeed, the adduct levels in the intervention group after five months was similar to the adduct levels in both groups immediately postharvest. Because this biomarker (the aflatoxin-albumin adduct) can be directly correlated with aflatoxin exposure in the diet (Shephard 2008
), the results of the Guinea study imply that the postharvest intervention package could essentially prevent aflatoxin from accumulating beyond its immediate postharvest level, even after five months of storage.
Any one of these six strategies in the intervention package, or any combination thereof, is useful in at least partially reducing aflatoxin contamination; because the strategies serve to control two of the major problems associated with storage: moisture, and insect pest damage and fungal spore vectoring. We evaluate the entire package in this study, because of its proven efficacy and information regarding cost.