Peter J Cotty Claudia Probst and Ramon Jaime Garcia

Abstract

Aflatoxins are potent poisons that contaminate crops in warm regions worldwide and reduce health and economic welfare in several portions of Africa. Crops are contaminated in two phases: (i) Aspergillus species infect crops during development; and (ii) after maturation contamination builds during exposure to warm humid conditions. Identification of the exact fungi causing contamination can provide clues to management strategies. Crops usually are infected by complex mixtures of aflatoxin-producing and closely related fungi. Among these are atoxigenic strains that produce no aflatoxins. In the United States atoxigenic strains are used to reduce contamination. Such technologies also may have value in Africa.

Introduction

Aflatoxins are a group of highly toxic, cancer-causing chemicals produced by several members of the fungal genus Aspergillus. The presence of these mycotoxins in human foods can cause acute and chronic health effects (aflatoxicoses) including immune-system suppression, growth retardation, cancer, and death (Wild and Turner, 2002; Gong et al., 2004; Williams et al., 2004; Azziz-Baumgartner et al., 2005). Aflatoxins are carcinogens and genotoxins that directly influence the structure of DNA (Williams et al., 2004) and, as a result, occurrence of aflatoxins in human foods is strictly regulated to very low concentrations in developed countries. Indeed, in developed countries the exposure of domestic animals, even pets, is of both regulatory and economic concern. Deaths of pets due to aflatoxins in U.S. pet foods has had international economic impact in terms of both trade and litigation (Anonymous, 2006). Thus, in developed countries, the drive to abate aflatoxin contamination is due to loss in crop value resulting from stringent government regulations on maximum permissible levels in crops and crop related products used as foods or feeds. In crops intended for human consumption, maximum permitted aflatoxin levels range from 2 ng/g in the European Union to 20 ng/g in the United States. Aflatoxins are readily transferred from feed to milk resulting in similarly stringent regulations on feed intended for dairies (van Egmond, 2004, Wu, 2004). Maximum permissible levels of aflatoxins in milk are 0.05 ng/g in the European Union and 0.5 ng/g in the United States.

The requisite destruction of highly contaminated agricultural products combined with reduced value for products with lower contamination levels makes aflatoxin economically expensive in developed countries. Contamination may limit the economic viability of agriculture in some regions and, in others, reduces the acreage on which susceptible crops, e.g., maize and peanuts, may be grown (Wu, 2004). In the United States, areas with severe contamination may yield crops with > 500 ng/g total aflatoxins (Jaime-Garcia and Cotty, 2003). However, in developing countries the contamination of crops with aflatoxin leads not only to economic losses, but also has a tremendous impact on human health. In Africa, a continent that relies on vulnerable crops such as peanuts and maize as dietary staples, af-latoxin contamination causes major health problems (Shephard, 2003). People in rural areas may have no option but to consume contaminated crops on a daily basis. This moderate, chronic intake of aflatoxin via food can lead to severe pathological conditions, including liver cancer, immune system deficiency and impaired development of children (Wild et al., 1992; Wild et al., 1993; Gong et al., 2004; Williams et al., 2004). Malnutrition, a common condition in rural Africa, increases disease prevalence and further reduces the ability of the human body to cope with aflatoxin exposure. Chronic aflatoxin poisoning reduces life expectancy.

Acute aflatoxin poisoning is caused by ingestion of high levels of the toxin. Immediate consequences are severe liver damage, acute jaundice and hepatitis, which subsequently may result in death (Bennett and Klich, 2003; Shephard, 2003; Williams et al., 2004). Although on a global basis deaths from acute aflatoxin poisoning are rare, Kenya has experienced such episodes repeatedly for at least 25 years. In 2004, 317 cases of acute aflatox-icosis were reported, resulting in 125 deaths (case fatality rate = 39%), with additional cases probably unreported. This epidemic was caused by ingestion of maize with aflatoxin concentrations of up to 4,400 ng/g (Anonymous, 2004; Azziz-Baumgartner et al., 2005).

Unfortunately, in an African setting, crops from small scale farmers frequently pass from field to storage to consumption with no regulatory oversight and without a test of the extent of aflatoxin contamination. Aflatoxin contamination often is mysterious to farmers because the extent of contamination is not readily evident and because it appears unrelated to crop yield or quality. Indeed, complex and expensive sampling and analyses often are required to estimate the extent of contamination (Whitaker and Johansson, 2005). The fungi that produce aflatoxins grow best under warm conditions and therefore, aflatoxins are of greatest concern in warm agricultural production areas especially during dry periods (Cotty et al., 1994). Such areas of high vulnerability are common in parts of Africa where subsistence farmers frequently rely on contaminated maize and peanuts as life-sustaining staples (Egal et al., 2005; Hell et al., 2003). Aflatoxin contamination varies in most areas and crops (Wilson and Payne, 1994). This variation has been attributed to climatic factors, especially drought and high temperature, in maize (Cole et al., 1982; Wilson and Payne, 1994; Widstrom, 1996) and peanuts (Cole et al., 1982, 1989; Wilson and Payne, 1994) with increased contamination being associated with reduced rainfall. However, in areas like Arizona and South Texas in the United States, increased contamination also is associated with exposure of the mature crop to warm temperatures and increased humidity provided by ir-ligation and/or rain (Bock and Cotty, 1999; Cotty, 2001; Jaime-Garcia and Cotty, 2003).

Management

Prevention or management of aflatoxin contamination may be directed at both the process of contamination and the fungi causing contamination. The contamination process can be divided into two phases based on crop maturity (Cotty, 2001). The first phase occurs during crop development and is generally associated with physical damage to the crop typically by either physiologic stress or insect activity (Russell, 1982; Cotty, 2001). Crop components contaminated during the first phase often fluoresce a bright green-yellow as a result of kojic acid production in crop tissue by the aflatoxin-producing fungi (Zeringue et al., 1999).

After maturation, the crops remain vulnerable to contamination, providing a window during which a second phase of contamination may occur (Bock and Cotty, 1999; Cotty, 2001). Exposure of the mature crop to both high humidity and temperatures conducive to aflatoxin producing fungi can result in both new crop infections and increases in the afla-toxin content of crop components already infected (Russell et al., 1976; Cotty, 1991). The second phase may occur prior to harvest in the field or after harvest during transportation, storage, or at any point until the crop is consumed.

Hot dry conditions during crop development favor the first phase of contamination, whereas rain and high humidity with warm temperatures after crop maturation favor the second phase. Reliable management practices must address both phases. Improving the resistance of cultivars to contamination is one method of simultaneously addressing both phases of contamination. Although proper cultivar selection and crop management can limit vulnerability to both phases, environmental changes can better even the best management practices and result in a highly contaminated crop (Wilson and Payne, 1994; Cotty et al., 2001).

When management procedures fail to prevent accumulation of unacceptable levels of aflatoxins, there are still options for the utilization of the contaminated crops. These options include detoxification. Chemical detoxification is a viable option for even very highly contaminated crops, with ammoniation the detoxification method currently in the widest use. Ammoniation inactivates aflatoxins by hydrolysis of the lactone ring, which is followed by further breakdown. Ammoniation has been used in North America, Europe, and Africa on crops including maize, cottonseed, and peanut meal (Park et al., 1988; Bailey et al., 1994). Following detoxification by ammoniation, the treated crop products are nutritionally valuable for domestic animals, but are not suitable for human consumption.

Etiology

Plant pathologists generally consider establishing the etiology, or cause, of a plant disease problem an initial step in developing management strategies for the problem. Since the establishment by Anton de Bary that potato late blight was caused by Phytophthora infestans and the formulation by Robert Koch of rules for establishing the cause of infectious disease, plant pathologists have drawn insight from improved knowledge of disease etiology to establish and improve disease management (Agrios, 2004). A clear understanding of disease etiology enables efficient screening for improved host resistance, identification of chemical pesticides toxic to causative agents, and development of biological control strategies that utilize less problematic organisms, e.g., saprophytes, epiphytes, endophytes, and even less damaging pathogens, to minimize the impact of disease through a variety of mechanisms. Management procedures for prevention of aflatoxin-contamination frequently are directed at either controlling the environment, i.e., either storage conditions or crop management are altered (Turner et al., 2005) or reducing host susceptibility, i.e., insect damage is reduced or crop barriers to infection are increased (Draughon and Ayres, 1981; Dowd, 1992). To direct management at the etiologic agent(s), i.e., the fungus(i) producing aflatoxin, the contaminating fungi present must be characterized. The process of identifying the most important aflatoxin producers can be complex. Members of the species that produce aflatoxins vary widely in their aflatoxin producing ability, with some aflatoxin producers being of little or no concern while others are of vital interest (Schroeder and Boller, 1973; Lisker et al., 1993; Cotty, 1997).

The communities of aflatoxin-producing fungi resident in agricultural and native ecosystems have a complexity that reflects the diverse geography and numerous substrates and hosts in which these species are found both across Africa and elsewhere (Cotty et al., 1994). Aflatoxin-producing fungi occur in many regions of the world, but they are most commonly associated with agriculture in warm production areas. A few aflatoxin-producing fungi outside of Aspergillus section Flavi have been described (Cary et al., 2005); however, the role of these species in the contamination of crops is not clear. Similarly, the extent to which some of the species within Aspergillus section Flavi contribute to aflatoxin contamination of crops also is unclear, as few episodes of contamination are attributed to either Aspergillus nomius (Cotty et al., 1994), Aspergillus bombycis or Aspergillus pseudotamarii. This lack of attribution may be due to the relatively recent description of the latter two species and to their apparently low incidences in some crop environments (Ito et al., 2001; Peterson et al., 2001).

Aspergillus flavus and A. parasiticus are the most commonly implicated causal agents of aflatoxin contamination, with A. flavus by far the most common (Cotty et al., 1994). As-pergillus flavus may be divided into two distinct morphotypes, the S and L strains (Cotty, 1989). Each morphotype is composed of many clonal lineages (called vegetative compatibility groups or VCGs) defined by a vegetative compatibility system that limits gene flow between dissimilar individuals (Papa, 1986; Bayman and Cotty, 1991a,b). Both morphotypes and VCGs differ in many characteristics; the most frequently studied of which is aflatoxin-producing ability. The S strain, on average, produces much higher concentrations of aflatoxins than does the L strain (Cotty, 1989, 1997; Garber and Cotty, 1997). Consequently, if the S strain commonly infects a vulnerable crop, this morphotype is a primary target for management of aflatoxin contamination. Members of different L-strain VCGs vary widely in their ability to produce aflatoxins. Members of some L-strain VCGs produce very large amounts of aflatoxins, while the members of many other L-strain VCGs produce very little, if any, aflatoxins. Isolates that produce no aflatoxins at all are termed "atoxigenic".

Communities of aflatoxin-producing fungi are complex and composed of multiple strains and VCGs. Although, these fungal communities are complex, the proportion of strains and VCGs with different aflatoxin-producing abilities varies widely among communities resident in different fields, valleys, and regions (Cotty, 1997). Consequently, the average aflatoxin-producing ability of those communities varies as well. Contamination events are not caused by individual specific fungi but by complex communities of aflatoxin-producing fungi that may contain several species, multiple morphotypes, and strains that belong to numerous VCGs (Bayman and Cotty, 1991b; Horne and Green, 1995; Doster et al., 1996).

If all organisms that produce aflatoxins are fungi in the genus Aspergillus, how much more specificity is needed to manage aflatoxin contamination? Understanding the interaction between the diverse aflatoxin-producing fungi resident in soils, on plants, and throughout the environment with crop contamination can result in improved management strategies. Specific knowledge of the etiology of contamination is a first step, but the etiology of specific contamination events often is difficult to determine, since contamination events are not caused by individual fungi, but rather by complex communities of fungi that partially

Table 1. Percent of infection and aflatoxin contamination caused by the S and L strains of Aspergillus flavus in commercial cotton seed in Arizona, i.e. in 1990 11% of the crop was infected by only the S strain, but this 11% of the crop contained 81% of the aflatoxin present in the entire crop. Measurements were made on a seed by seed basis. Data from Cotty (1996).

Table 1. Percent of infection and aflatoxin contamination caused by the S and L strains of Aspergillus flavus in commercial cotton seed in Arizona, i.e. in 1990 11% of the crop was infected by only the S strain, but this 11% of the crop contained 81% of the aflatoxin present in the entire crop. Measurements were made on a seed by seed basis. Data from Cotty (1996).

Infecting

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