K. F. Cardwell, A. Desjardins, S. H. Henry, G. Munkvold, J. RobensCardwell, K.F., Desjardins, A., Henry, S.H., Munkvold, G. and Robens. J. 2001. Mycotoxins: the Cost of Achieving Food Securty and Food Quality. APSnet Features. Online. doi: 10.1094/APSnetFeature-2001-0901
Since the 11th century AD, when the French discovered that Claviceps purpurea-contaminated rye baguettes made people do strange things, many other toxic fungal metabolites, or mycotoxins, have been added to the list of anti-nutritional food contaminants. Some mycotoxins, such as the aflatoxins, have been extensively studied by toxicologists, while others are less well understood. Some have been regulated for years, while others have only recently come under scrutiny.
Aflatoxin, produced by Aspergillus flavus, A. parasiticus, and other closely related fungi; fumonisins, produced by Fusarium verticillioides; and deoxynivelanol (DON, or vomitoxin), produced by F. graminearum, are the primary sources of both the losses and costs of management (26,46). Other fungal toxins, including cyclopiazonic acid in peanuts (6), zearalenone from corn, (11,51) and ochratoxin, (13,52) are of lesser importance to US producers. Their concerns result primarily from the need to protect exports to the EU countries.
Globalization of trade has complicated the way we deal with mycotoxins in that regulatory standards often become bargaining chips in world trade negotiations. While developed countries have well-developed infrastructures for monitoring of internal food quality standards, people in developing countries are not protected by food quality monitoring and enforcement of safe standards within their countries. On the other hand, foods being exported are expected to comply with CODEX Alimetarius standards, thereby possibly inadvertently resulting in higher risk of exposure in developing countries because only the best quality foods leave the country.
In developing countries, many individuals are not only malnourished but are also chronically exposed to high levels of mycotoxin in their diet (7). Aflatoxins are proven carcinogens, immunotoxins, and cause growth retardation in animals (19,27,44). Fusarium toxins, specifically fumonisins, are reported carcinogens and trichothecenes are reported immunotoxins (3,17,40,43). It is expected that mixtures of mycotoxins would have at least an additive, if not synergistic egregious effect (35).
The negative trade impact of tightening the standards has been calculated by the World Bank for peanuts from African exporting countries (41). At the Third United Nations Conference on the Least Developed Countries in Brussels on May 14, 2001, Secretary-General Kofi Annan said, “. . . a World Bank study has calculated that the European Union regulation on aflatoxins costs Africa $750 million each year in exports of cereals, dried fruit and nuts. And what does it achieve? It may possibly save the life of one citizen of the European Union every two years . . . Surely a more reasonable balance can be found” (2).
In this APSnet Feature, the cost of mycotoxin management to the United States will be assessed by Drs Jane Robens and Gary Munkvold. These management costs will be juxtaposed with cancer risks by Dr Sara H. Henry; while the potential costs in mycotoxin occurrence in countries where food quality is not effectively managed will be discussed by Drs Anne Desjardins and Kitty Cardwell. What are the real costs of mycotoxins to the USA and to the world? Is the main cost due to lost revenues during commodity trade? Is it a societal drain in terms of research and enforcement, costs that only rich countries can afford? Is it a justifiable drain in terms of returns in improved public health? What if we had to destroy all of the mycotoxin contaminated food of the world in a year? Would this exacerbate the problems of food security globally? Are food quality and food security goals that can be achieved simultaneously?
Corresponding author: Jane Robens. firstname.lastname@example.org
Fig. 1. Grain sampling is part of the cost of testing commodities for mycotoxins (click image for larger view).
Mycotoxin losses and costs of mycotoxin management are overlapping areas of concern. Costs of mycotoxin management include research production practices, testing and research necessary to try to prevent the toxins from appearing in food and feed products of affected commodities. Mycotoxin losses result from (A) lowered animal production and any human toxicity attributable to the presence of the toxin, (B) the presence of the toxin in the affected commodity which lowers its market value, as well as (C) secondary effects on agriculture production and agricultural communities.
Losses from mycotoxins in the US are associated with regulatory losses, as opposed to lowered production, illness, and/or deaths from the effects of the toxins. This is particularly the case for human food, but increasingly it has become the case for animal feeds, as strict feed quality control programs become the norm for large-scale animal production units. The Stoloff papers from the 1980s infer that there is no aflatoxin-related toxicity or carcinogenicity in humans in the US (48,49,50). Paul Sundberg of the National Pork Producers Council (June 2001, personal communication) stated that swine producers do not recognize on-going losses from aflatoxin, although they may occur in localized production areas in severely affected crop years. That there are only a very small number of cases of actual recognized toxicity to animals in the US is the direct result of our food safety regulatory system.
Mycotoxin management costs are incurred by both producers and the Federal and state governments to prevent mycotoxins from becoming a human and animal health threat. The Food and Drug Administration (FDA) has functioning mycotoxin regulatory programs for aflatoxin, fumonisins, and vomitoxin (1,57,58,59).
Aflatoxin is the mycotoxin generating the greatest losses and the highest management costs due to its extremely high toxicity on a unit basis, and its long history of stringent regulation. The peanut, corn, cottonseed, and tree nut industries all recognize losses associated with meeting regulatory levels. The costs are inversely related to the regulatory level that must be met, and lower concentration allowances will increase the costs of crop management. In the United States, the FDA has used a 20 ppb tolerance almost since the initiation of their mycotoxin regulatory program, but industries that sell to EU countries face regulatory allowances of much lower ppb concentrations.
There have been few attempts to estimate with accuracy the mycotoxin related losses faced by various commodity groups in the US. The Council on Agricultural Science and Technology (CAST) report, Mycotoxins: Economics and Health Risks, published in 1989, outlined the information regarding losses known at that time (10). A chapter by the FDA’s Peter Vardon, to be included in a new CAST report, analyzes the potential economic cost of mycotoxins in the US. Vardon estimated an annual range of losses from $0.5 million to over $1.5 billion from aflatoxin (corn and peanuts), fumonisin (corn), and deoxynivalenol (wheat). Uncertainties were built into the cost model based on commodity outputs, prices, and contamination levels based on surveillance samples and compliance with FDA regulatory limits. Vardon assumed that the livestock loss was directly proportional to the percentage of feed that was contaminated above FDA standards, and he calculated small livestock losses from aflatoxin and DON. Costs of testing for the toxins, either to commodity producers or to the public through the FDA budget; costs of growing less valuable alternative crops; costs of handling affected crops; etc. were not included.
The investment in research programs by the Federal government, primarily to prevent mycotoxins in crops, can be considered a major cost of mycotoxin management. The USDA's Agricultural Research Service (ARS) has a mycotoxin research program, $17.7 million for approximately 60 scientists in fiscal year 2000, primarily focused on prevention of the fungus and toxin production in the crop. This level of support is the total appropriated amount; it includes the mycotoxin research share of administrative salaries, as well as the scientists and technicians and various support personnel, increasingly expensive energy costs, costs of services and building maintenance, etc. The USDA's Cooperative State Research Education and Extension Service (CSREES) reports $4.7 million for mycotoxin research, along with $5.1 million from states at their land grant institutions, and an additional $2.1 million from other Federal agencies at these institutions (William Wagner, CSREES, June 2001, personal communication).
The FDA also carries out research at the Center for Food Safety and Applied Nutrition, primarily on methodology development, effects of processing, and toxicology on mycotoxins. They assess this activity for 14 to 15 scientists at $1.5 million, however the FDA calculation includes only the scientists’ salaries and some immediate laboratory costs and does not include the agency administrative costs and infrastructure as does the ARS amount (John Newland, Center for Food Safety and Applied Nutrition, FDA, June 2001, personal communication).
Analysis of product samples is needed to assure that product offered to the market meets regulatory and market requirements. These considerable costs are incurred both by industry and by various government regulatory and action agencies. Industry costs, in particular, go up significantly during years when contamination of the crops is high. Average total value of commercial aflatoxin test kits on the market is approximately $10 million per year annually, about 2 million tests for an average year. Sales increase rapidly in outbreak years (Robert Elder, USDA-ARS, May 2001, personal communication). In addition to the test kit costs, the range of charges for testing by official agencies and cooperative services is from $10 to $20 per sample not including collection of the sample. For aflatoxin alone, testing will cost $30 to $50 million per year.
For example, testing costs associated with corn production and marketing comes from the Grain Inspection Packers and Stockyards Administration (FGIS), which conducts aflatoxin and DON testing for exported grains. For aflatoxin, FGIS analyses approximately 30,000 samples per year, which generates approximately $290,000 in revenues. State and private laboratories with official sanction from FGIS, analyse approximately 27,000 samples per year, which generates approximately $540,000 in revenues. For DON, FGIS analyses approximately 6000 samples per year, which generates approximately $100,000 in revenues, while official agencies analyse an additional 18,000 samples generating about $360,000 in revenues annually (John Giler, FGIS, May 2001, personal communication).
Testing corn for aflatoxin in southeast Texas is a considerable expense at $20 to $30 per test and one test per truckload of 30,000 to 60,000 pounds of commodity (Fig. 1). This equates to a testing cost of $2-3 per acre (Jeff Nunley, South Texas Cotton and Grain Association, May 2001, personal communication). Also in southeast Texas, every 100 tons of cottonseed requires a test for aflatoxin, at about $125 total costs (including sampling and transportation to the laboratory) per sample. Sample preparation for cottonseed costs more than for corn, which does not require dehulling or delinting. There is also a difference in the size of the sample that is generally used (Peter Cotty, USDA- ARS, June 2001, personal communication).
The cost of litigation may also be significant for cottonseed producers. The identity of cottonseed is generally maintained through the market chain. If contamination above 0.5 ppb is detected in milk, the product may be traced to the dairies where the cattle are being fed contaminated cottonseed. The sellers, producers, and any other party who can be identified are likely to be sued. Feedlots for fattening beef cattle are wary of feeding cottonseed containing >20 ppb aflatoxin even though it may be legal up to 150 ppb (Jeff Nunley, South Texas Cotton and Grain Association, May 2001, personal communication).
Insurance premiums, and compliance with the recommendations of the insurance company for those producers who chose it, is another major cost of managing mycotoxins. A private crop insurance company in Des Moines, IA, recommends that their insured producers sample a high percentage of their loads for the first 2 weeks of each season. Even if only a very small percentage of loads are found positive for the mycotoxin, they recommend that sampling continue on a random basis. This company states that testing costs for producers are $5 to $7 per test if carried out on a regular basis and $9 to $12 per test if done sporadically (David Frank, American Feed Industry Insurance Association, Des Moines, IA, June 2001, personal communication).
Peanuts. Marshall Lamb at the ARS National Peanut Research Laboratory in Dawson, GA, has prepared a recent paper addressing losses from aflatoxin (in publication). This paper surveys and analyzes actual losses in peanuts during the 1993-1996 crop years. Lamb estimated the net cost of aflatoxin to the farmer, the peanut buying point, and the sheller segments of the Southeast peanut industry to be about $25 million per year. Peanuts are subject to a Federal marketing order that proscribes very strict and complicated procedures for testing, segregating, and handling peanuts to prevent peanuts that do not meet FDA requirements for aflatoxin from becoming a part of the human food supply. The costs of aflatoxin result from both decreased value of the crop as calculated from the quota support price, and from costs incurred in handing contaminated peanuts, including blanching, re-milling, equipment, testing, and insurance. Lamb’s calculation does not include costs of production practices, particularly irrigation, that may be used to help prevent aflatoxin in the crop.
Cotton. Cottonseed is a by-product of cotton fiber production, and thus cotton breeding and agronomic practices have not traditionally considered the need to prevent contamination of the seed. Aflatoxin contaminates cottonseed in Texas and in Arizona with sufficient frequency that it is a continuing concern of state regulatory officials in these states. The major market for cottonseed, either whole seed or meal, is feed for dairy cattle; and in the late 1970s aflatoxin from contaminated cottonseed fed to dairy cattle was detected in milk by state regulatory officials and the FDA. Dairy cattle excrete a much higher percentage of ingested aflatoxin in milk (metabolized to aflatoxin M1) than is ever deposited in muscle meat. In addition, the amounts of any residue allowed in milk are low and at the sensitivity of the method, in this case < 1 ppb. Cottonseed is still fed to dairy cattle but it is tested and recognized contamination of milk is rare (10).
Estimates for a single year do not provide a true picture of the extent of aflatoxin contamination because of its variability. Thus, the Arizona Cotton Research and Protection Council combined their estimates from 1977 to 1999. During this 22-year period, Arizona had an average annual cottonseed production of 397,000 tons, with an average annual value of $42,205,000 for a total value of $928,510,000. Discounts on cottonseed with aflatoxin levels above 20 ppb vary from $20 to $50 per ton with the majority falling in the $30 to $35 range. Based on these figures, the most conservative estimate of revenue lost due to aflatoxin contamination over the 22 year period is $96,074,000 or slightly over 10 percent (Table 1: Reports of direct crop revenue losses due to mycotoxins).
In addition to direct revenue losses due to aflatoxin discounts, regulatory restrictions prevent contaminated cottonseed from leaving the state (except under a restrictive permitting system), severely affecting marketing options for the Arizona growers. Elimination treatment (ammoniation) costs plus interim shipping and/or storage fees would result in cost benefit of $20 per ton or more if aflatoxin-free cottonseed could be shipped directly from gins to prime customers such as dairies.
In south Texas, Jeff Nunley estimated that testing costs alone could be as high as $150,000 for each of two major cottonseed processors that use cottonseed originating from south Texas. Cottonseed that contains high aflatoxin levels is segregated and processed separately leading to additional costs at the processor level. These increased costs are ultimately reflected in lower values for cottonseed at the producer level. During the 1999 crop year, only about 30 percent of the cottonseed tested at the major cottonseed processing mills in south Texas had acceptable levels of aflatoxin (Table 1). While not all processors formally discounted their price for aflatoxin-contaminated cottonseed, discounts of $20 per ton for contaminated seed were common with some discounts being larger. Based on an average $20 per ton discount, the loss of value to south Texas cotton producers for the 1999 crop from aflatoxin-contaminated seed would be slightly over $7,000,000. With a harvested acreage estimated at 960,000 acres this loss equates to approximately $7.30 per harvested acre. In south Texas, contaminated cottonseed may be processed at an oil seed mill for crushing so that some value is recouped on the contaminated crop, or it may be sent to Indigo, California for ammoniation, or finally contaminated meal may be used for mushroom fertilizer.
Corn. Corn is contaminated with aflatoxin only sporadically, primarily when droughts occur, in the Corn Belt states of Iowa, Illinois, Indiana, etc. Severe losses from aflatoxin in Midwest corn occurred in 1983 and again in 1988. Corn is contaminated every year at one or more locations in the southern states, that is Georgia, Louisiana, Mississippi, Georgia, and North Carolina across to Texas. In 1998 corn losses in Mississippi, Louisiana, and Texas were extremely harsh and painful. Corn is grown to a very limited degree in Arizona but would be planted more frequently in many areas if it were not for aflatoxin contamination, eliminating it as a potential rotation crop. Also in the south Texas Corpus Christi area, corn could be a valuable rotation crop for the primary cash crop of cotton; but in order to avoid aflatoxin contamination 300,000 acres are planted to sorghum each year rather than to corn (Jeff Nunley, South Texas Cotton and Grain Association, May 2001, personal communication).
In Mississippi in 1998 a severe drought resulted in high aflatoxin contamination. These losses were in irrigated as well as dryland corn, and were particularly onerous for farmers who had just planted corn for the first time. Twenty per cent of the 50 million bushel crop had aflatoxin levels of 20 to 150 ppb and was sold at a discounted price. Another 4 percent was abandoned because it contained over 150 ppb. However, initially, approximately 50 percent of the crop was contaminated to the extent that many samples over legal limits. Half of that amount was eventually sold for feed by farmers. Little of Mississippi corn is used directly for human consumption. Probe samples taken from truckloads for aflatoxin analysis of corn are generally smaller than optimal, and more likely to be near 5 pounds than near 50 pounds. This is considered necessary to maintain the commercial flow of commodity (Erick Larson, Mississippi Agricultural and Forestry Experiment Station, May 2001, personal communication).
Tree nuts. Tree nuts such as almonds, walnuts, and pistachios may be contaminated with aflatoxin, though at lower levels than for cottonseed and corn. However the problem is very significant to the producers because (A) the crop has a high unit value, and (B) because much of the crop is sold to the European markets that enforce limits significantly lower than in the US.
In walnuts in the 2000-1 crop year aflatoxin was found in 4 percent of the samples tested by the industry. Since the crop size for the year 2000 was 236,000 tons, the walnut industry lost an estimated 18,880,000 pounds of walnut kernels to alfatoxin for the year’s harvest. There was short tonnage (production) and higher market prices for the 2000-1 crop year, and the cost of product lost is estimated at $2.05 per pound of product. Thus the total direct dollar market value lost to the walnut industry was $38,704,000.
Exported almonds had a value of $696.8 million in 1999. It is difficult to estimate the cost of aflatoxin to the almond industry; however, there is a strong correlation in almonds between insect damaged kernels and aflatoxin. Almond producers utilize several sophisticated sorting techniques to sort the good from the inedible kernels, and handlers remove and dispose of their inedible almonds to non-human consumption channels. In the six crop years from 1995-96 to 2000-01, almond production ranged from 366,000,000 to 830,000,000 pounds. If 3 percent of each year’s production is considered inedible (aflatoxin contaminated) then the value of this 3 percent of the total crop was thus lost. That is, 910,980,000 to 24,900,000 pounds of almonds per year was considered inedible and its value was lost. Thus, based on a wholesale value of $1.50 to $3.00 per pound for uncontaminated, edible almonds, the lost market value to the producer for contaminated almonds ranged from $23,265,000 to $47,310,000 in this six-year time period. There are additional costs of transportation, sorting, and analytical tests for contaminated almonds that are not included in the above loss figures.
Barley. Contamination with deoxynivalenol (DON), or vomitoxin produced by Fusarium head blight infection with F. graminearum, has caused serious losses to the barley producers in the Tri-State affected area of Minnesota, North Dakota, and South Dakota. The loss is primarily due to vomitoxin and DON contamination, while that in wheat is due to both lowered production and toxin production. Wheat flowers outside of the boot, and thus is inherently more susceptible to being infected with the fungal spores.
Malters and brewers use a 0.5 ppm level of DON as a cut-off, but how it is used varies by company. DON-containing grain is discounted 5 to 10 cents per bushel for each 0.1 ppm that the grain exceeds 0.5 ppm. Anheuser-Busch is the most stringent and anything in excess of 0.5 ppm vomitoxin in the barley grain or in malt which they may buy from other malters is unacceptable. Some malters, however, will accept grain with 2 to 3 ppm vomitoxin since in some cases the process of malting will lower levels of vomitoxin. However, if the malting is carried out too long, the fungus will regrow and the levels will increase again.
Serious contamination with DON has occurred in the Tri-State area each year since 1993. Prior to that, contamination was only sporadic. Barley growers believe that this was due to a change in long term weather patterns with the area now having higher rainfall and relative humidity. The acceptance rate for barley in the Tri-State has not been greater than 35 percent since 1983. When barley is not acceptable for malting it is used for animal feed, which brings a lesser rate of return. Growers need approximately $160 per acre to break even and malting barley usually yields about $160 per acre while barley for animal feed yields only $100 per acre. The unavailability of barley as a reliable rotation crop is another loss to growers with the preferred rotation 3-year in this area being: 1st year, wheat; 2nd year, feed grain; 3rd year, oil seed; and back to wheat. In addition, there is the loss of the economic infrastructure that had grown up around handling and marketing the crop particularly in eastern North Dakota.
The Tri-State barley producers have calculated a total loss of $406 million for the 6 years from 1993 through 1998. The total barley acreage has now declined over half from 1993 because the growers do not want to take the high risk of growing malting barley. In 1993 there was 4,250,000 acres of barley while in 2000 there was 1,950 acres of barley (Table 1).
Wheat. Losses from Fusarium Head Blight (FHB), also known as Scab, in wheat include both lowered grain yield and the presence of DON. In 1993, farm gate losses in the Red River Valley of North Dakota, South Dakota, and Minnesota were $200 to $400 million for this fungal infection and mycotoxin. In 1996 there was a $300 million loss to farmers alone raising soft wheat, and also in that year there were significant replacement costs to millers. Replacement costs include transportation of wheat from another area to meet contracted deliveries, as well as the higher price that must be paid for this wheat because of decreased availability. The industry estimates they have sustained total losses of $1 billion from wheat scab (Table 1) (Jim Baer, North American Millers Washington DC, June 2001, personal communication).
A North Dakota State University economist, William Nganji, has estimated losses based on grain yields and price (dollars per bushel) that might have been expected under normal conditions, in the absence of wheat head scab (47). Precipitation and temperature data were used to estimate "normal" production. The loss of production is calculated as the difference between actual and normal production, and then adjusted for acreage abandoned as a result of scab. Total direct and secondary economic losses from FHB in North Dakota for wheat and barley, and in Minnesota for wheat, were estimated at $545 million from 1998-2000. As significant as the direct loss is the finding that there is a significant secondary economic impact. For each dollar of lost net revenues for the producer, an additional $2.10, approximately, is lost in secondary economic activity, including households, retail trade, finance, insurance and real estate, and personal business and professional services.
Corresponding author: Gary Munkvold. email@example.com
Recognizing the potential for fumonisins to cause animal or human health problems (34), in June 2000 the US Food and Drug Administration (FDA) released a proposal describing guidelines for fumonisin levels in human foods and animal feeds (Table 2). The FDA is expected to publish their final guidelines some time this summer. The impending publication of these recommendations has caused concern within the industry about possible impacts on corn marketing. In this section, I will not assess the current costs of fumonisin management; instead, I will explore how the implementation of FDA guidelines might change these management practices.
Table 2. Recommended maximum levels of fumonisins in human food products and animals feeds, US Food and Drug Administration, June 6, 2000.
Table 2. Recommended maximum levels of fumonisins in human food products and animals feeds, US Food and Drug Administration, June 6, 2000.
For individual corn producers selling grain on the open market, fumonisins currently have little economic impact. Most corn is sold at country elevators where testing for fumonisins is rare because commonly occurring fumonisin levels are acceptable for most uses. Due to commingling of loads at the elevators, individual loads with high fumonisins can be absorbed while maintaining a combined supply that has acceptable fumonisin levels.
Fig. 2. Fumonisin B1 in pre-harvest corn from the Midwest, 1995 (55) (click image for larger view).
Based on surveys from the mid-1990s (Fig. 2), 0.5 percent to 10.5 percent of corn grown in the North Central US had fumonisin levels of 5 ppm or higher B1 (not including other fumonisins), which would be unsuitable for horses or human food use, according to FDA proposed guidelines (36,37,38,55,56). In order to understand the implications of these fumonisin levels in relation to FDA recommendations, it is important to consider the various uses of maize grain and how the FDA recommendations differ among those uses.
In 2000, 58 percent of the US corn crop was used for animal feed, 22 percent was exported, 6 percent was used for corn sweeteners, 6 percent for ethanol, and 8 percent for milling and all other uses (39) (Fig. 3). The ethanol and wet-milling segments are basically unaffected by fumonisins. There are no FDA recommendations for corn intended for ethanol production. Fumonisins are generally not detected in ethanol made from fumonisin-contaminated corn (4). Similarly, cornstarch and corn oil do not generally contain fumonisins (4,42), so FDA did not state recommendations for corn sweeteners or oil.
Fig. 3. US corn usage in 2000 (39) (click image for larger view).
Within the animal feed segment, the majority of grain is fed to livestock on-farm, without going to market. The value and treatment of corn fed on-farm will not be directly affected by FDA guidelines. FDA recommendations for beef cattle and poultry are a maximum of 60 and 100 ppm, respectively, for the corn portion of the diet. Fumonisins rarely reach these levels in the US corn crop. FDA recommendations for swine and dairy cattle are lower, but still, at levels of 20-30 ppm, there is a small percentage of US corn that would fail to meet these standards. The low frequency of occurrence of these levels would not justify the expense of a testing program in most years. In the absence of testing at grain elevators (the likely situation), occasional loads of corn with fumonisins above this level would be commingled with other grain and the fumonisins would be adequately diluted. The lowest recommended levels for animal feed are for horses, rabbits, and pet foods. In terms of corn consumption, these species are included in the “other animal” category (Fig. 3), which accounts for about 1 percent of US corn. Because of the low percentage of the crop consumed by these sensitive animals, it is not likely that buyers of large quantities of commodity grain would alter their practices to meet standards for these species. Instead, quality control practices already used in the feed-formulation industry will likely be strengthened.
Foreign grain buyers usually impose their own standards for mycotoxins in grain, and these standards are frequently more stringent than the FDA guidelines (20). However, the existence of published FDA guidelines may encourage additional foreign buyers to alter contract requirements by imposing stricter fumonisin tolerances. This would result in increased costs for testing and handling by corn exporters, and possibly the diversion of contaminated grain from some elevators, which could involve transportation costs for corn producers. The magnitude of this effect will depend on the extent to which foreign buyers change contract requirements, and on the levels of fumonisins in the annual corn crop.
Table 3. Food and industrial consumption of US corn, 2000 (39)
Table 3. Food and industrial consumption of US corn, 2000 (39)
The lowest recommended fumonisin levels in corn for human food uses are for dry milled products, corn for masa, and popcorn. Dry milled products accounted for 186.2 million bu in 2000, or about 1.9 percent of US corn (Table 3). Dry millers marketing products made from degermed corn meal are currently managing their grain supply to achieve fumonisin levels within the range proposed by FDA, and are not likely to substantially change their practices. Because degermed, dry milled products have substantially lower fumonisin levels than the corn from which they are derived (31), it is possible that corn with fumonisin levels significantly higher than 2 ppm will yield dry-milled products below that level. In addition, large dry milling operations achieve quality control by buying grain directly from producers on contract. These operators may perform surveys of mycotoxin levels in the field before the grain is brought to the point of sale. Producers with a crop that does not meet contract specifications in terms of fumonisins or other quality characteristics will not be able to sell to the contract buyer.
Small dry milling operations usually obtain grain from country elevators, where the millers often pay a premium for higher quality grain. Elevators can provide these buyers with higher quality grain through sorting based on physical characteristics, without specifically testing for fumonisins. Small milling operations, especially those marketing products made from whole grain or bran, will be under increased pressure to strengthen quality control. This may result in increased testing and grain handling costs, but the magnitude of this effect will depend on the occurrence of fumonisins in the annual crop. The FDA recommendation of 4 ppm is not considered difficult to achieve in most years; therefore, testing costs may be minimal in the majority of cases.
Corn uses subject to the lowest recommended fumonisin levels comprise a small percentage of US corn (about 3.5 percent, including dry milling, masa, popcorn, and corn fed to horses). It will not be necessary to apply these low fumonisin tolerances to the corn crop in general, which means that most individual corn producers will not be affected by the implementation of FDA guidelines.
The segments of the corn market that may experience increased costs as a result of the FDA guidelines are the horse feed formulation, export and dry milling segments. Increased costs will be primarily related to fumonisin testing. Testing costs for industry could increase significantly, depending on the annual occurrence of fumonisins and the response of foreign buyers. The standardization of practical commercial tests for fumonisins is an unresolved issue that may result in confusion and extra costs during the initial years.
S. H. Henry, P. M. Bolger, and T. C. Troxell, Center for Food Safety and Applied Nutrition, US Food and Drug Administration, Washington, D.C.
Corresponding author: Sara H. Henry. Sara.Henry@cfsan.fda.gov
Regulatory standards for food additives, residues of veterinary drugs and pesticides, naturally occurring toxicants, and human-derived contaminants in commodities moving in world trade are set by the Codex Alimentarius Commission. This body, currently composed of some 165 member countries was formed after World War II to protect international public health and to facilitate world trade. A regulatory standard has been adopted by the CODEX alimentarius commission for aflatoxins in peanuts intended for further processing and moving in international trade.
Previously, the Joint Food and Agriculture Organization/World Health Organization Expert Committee on Food Additives (JECFA), the scientific advisory body to CODEX, recommended that aflatoxins in foods be kept at “irreducible levels”. However, since the risk associated with target levels was not described, this advice gave little guidance for risk management, and has created barriers to world trade, as well as wasting valuable food sources.
In 1997 and again in 2001, CODEX’s international advisory body, JECFA has performed two risk assessments for aflatoxins in peanuts and in milk and milk products. The risks of liver cancer to humans from aflatoxin exposure were estimated in relation to other risk factors for liver cancer (24,29,30).
Aflatoxins have been demonstrated to be among the most potent animal mutagenic and carcinogenic substances known. But the question has remained for years about the potency of aflatoxin as a human liver carcinogen. The currently available information on metabolic activation and detoxification of aflatoxin in various animal species does not allow the identification of a fully adequate model for humans.
Liver cancer (HCC) is a very important cancer in the world wide public health picture. HCC is rapidly fatal. Half of the approximately 473,000 new cases appearing per year arise in China and 25 percent in West Africa. The combined impact of treatment costs plus years of productivity lost is quite significant. Risk factors for human liver cancer may be predicted from epidemiological studies and have been shown to vary between Europe/US and Africa/Asia, as shown in Table 4. Fifty to 100 percent of liver cancers are estimated to be associated with persistent infection of hepatitis B (and/or C) virus.
Table 4. Liver cancer etiology: attributable fractions in Europe-US and in Africa-Asia (5)
Table 4. Liver cancer etiology: attributable fractions in Europe-US and in Africa-Asia (5)
JECFA (1998 and 2001) estimated the carcinogenic potency of aflatoxin in a number of animal species and in humans (from epidemiological studies) with and without HBV (29,30). Data on HCV were lacking, and there was no adequate model which would predict the relationship between aflatoxin, HBV (and/or HCV) and HCC. When these potencies were rated from 0 to 1, with 1 representing the carcinogenic potency in the most sensitive animal model (the Fischer rat). There was an approximate 30-fold difference between the carcinogenic potency of aflatoxin in humans who were negative for HBV (hepatitis B surface antigen negative [HBsAg-]) vs. humans who were positive for HBV (HBsAg+).
However, there were problems in estimating the doses of aflatoxin received by humans, and HBV status was not always determined using the most accurate methodology.
There are a number of factors affecting the relationship between aflatoxin, HBV/HCV and HCC, which remain to be elucidated. First, the p53 gene may be involved.
Biomarkers for aflatoxins have enabled the identification of a specific mutation in the p53 tumor suppressor gene in HCC cases from regions of the world with high aflatoxin exposure. In the Gambia this mutation has been observed in plasma DNA in HCC cases; the alteration is infrequent in control subjects (19). Duration of HBV infection seems to increase the risk of HCC, as does concomitant infection with HCV (25).
Currently available biomarkers for aflatoxin (e.g., aflatoxin/albumin adducts in blood serum), an individual measure of aflatoxin exposure, are still limited because they reflect aflatoxin exposure only for the lifetime of the marker, about 22 days for serum. A measure of aflatoxin exposure over a third to half a lifetime is still needed to more nearly reflect the probable induction time for human cancer (25).
The importance of hepatitis B virus as a risk factor for human liver cancer has been clearly demonstrated by the drastic reduction of liver cancer cases by HBV vaccination in Korea. In a country where both the prevalence of HBV infection and HCC are high (about 21 per 100,000), in 370,000 males followed for three years, HBV vaccination reduced HCC (incidence of 215 cases per 100,000 to 8 cases per 100,000) (32). In this case, HCC incidence was reduced significantly by vaccination for HBV without changing any other risk factor for HCC.
Vaccination for HBV can be very cost-effective, especially if undertaken in childhood as opposed to adulthood. For example, in the U.K., the cost of HBV vaccine for one adult HB carrier is about $15 US, as compared to about $0.75 US per child in Bangladesh (16). JECFA (29,30) concluded that the world-wide liver cancer burden could best be reduced by giving priority to hepatitis B virus vaccination campaigns and to prevention of hepatitis C virus infection (e.g., reinforcement of the control of blood and blood products and the use of sterile medical equipment).
A. E. Desjardins, R. D. Plattner, C. M. Maragos, and S. P. McCormick, National Center for Agricultural Utilization Research, USDA-ARS, Peoria, IL, USA, 61604; G. Manandhar, H. K. Manandhar, and K. Shrestha, Plant Pathology Division, Nepal Agricultural Research Council, Khumaltar, Lalitpur, Nepal
Corresponding author: Anne E. Desjardins. firstname.lastname@example.org
Infection of cereal grains with Fusarium species can cause contamination with mycotoxins that affect human and animal health. In 1997, samples of maize, wheat, and rice grain were collected from 25 smallholder farms in Lamjung district in the foothills of the Nepal Himalaya (Figs. 4 to 7). Additional grain samples were collected from markets and Nepal Agricultural Research Stations in central Nepal.
Fig. 4. Lamjung district Nepal, site for collecting grain samples from smallholder farms with Annapurna peaks in background (click image for larger view).
Fig. 5. Collecting grain samples from smallholder farms in Lamjung district (click image for larger view).
Fig. 6. Threshing wheat in Lamjung district (click image for larger view).
Fig. 7. Cultivating maize in Lamjung district (click image for larger view).
A total of 68 maize samples, 27 wheat samples, and 48 rice samples were analyzed for the presence of Fusarium species. Fumonisin-producing species present included F. verticillioides in 97 percent of maize and 5 percent of rice samples; F. proliferatum in 4 percent of maize, 26 percent of wheat, and 38 percent of rice samples; and F. fujikuroi in 12 percent of rice samples. Trichothecene-producing species included F. graminearum in 24 percent of maize, 56 percent of wheat, and 40 percent of rice samples (Fig. 8). Other Fusarium species included F. acuminatum, F. anguioides, F. avenaceum, F. chlamydosporum, F. equiseti, F. oxysporum, F. semitectum, and F. torulosum. Analysis of molecular markers indicates that the population of F. graminearum from Nepal has a high level of genetic diversity (9,14,15).
Fig. 8. Village boys with shelled grain and ears of maize, those on the left discolored by infection with Fusarium graminearum (click image for larger view).
Sixty-eight samples of maize were analyzed for fumonisins by enzyme-linked immunoadsorbent assay (ELISA) and/or by high performance liquid chromatography (HPLC). Forty-eight samples of rice were analyzed for fumonisins by ELISA. Seventy-four samples of maize and 27 samples of wheat were analyzed for the trichothecenes nivalenol and deoxynivalenol by ELISA, fluorometry, and/or liquid-chromatography-mass spectrometry (LC-MS).
Nivalenol and deoxynivalenol (DON) were not detected above 1 ppm in wheat, and fumonisins were not detected above 1 ppm in rice. The low mycotoxin contamination of wheat and rice is probably due in part to dry weather during the wheat and rice harvests, which provides poor conditions for mycotoxin production. In addition, traditional post-harvest practices include sun-drying of wheat and rice grain to lower moisture content and winnowing to remove seeds that are lighter in weight due to poor grain fill or disease.
Fig. 9. Village women grinding maize meal for consumption (click image for larger view).
In contrast, fumonisins, nivalenol, and DON were detected in maize. Levels of fumonisins were above 1 ppm in 22 percent of maize samples, and the mean level in the positive samples was 2.3 ppm. Levels of nivalenol and/or deoxynivalenol were above 1 ug/g in 16 percent of maize samples, and the mean level in the positive samples was 3.2 ppm. Contamination of maize probably is increased by maturation of the crop during the summer monsoon season when rains provide ideal conditions for fungal infection and hinder the drying that is necessary to prevent mycotoxin production in stored grain. Furthermore, the demand for increased food grain production is changing farming practices from the traditional rice and fallow rotation to intensive cropping of rice and maize within the same year. Farmers interviewed in the Lamjung district stated that to transplant rice they sometimes harvested their maize crop while the ears had a high moisture content.
An integrated approach to control mycotoxins in food grains should include efforts both to prevent contamination and to detoxify contaminated grain, especially where food resources are limited. We found that a traditional Nepalese fermentation method for producing maize beer did not affect the fumonisin level and only partially decreased the deoxynivalenol level of contaminated maize. Because visibly diseased maize kernels contain most of the fumonisins and trichothecenes, physical separation of diseased kernels can be an effective decontamination method. We found that 12 Nepalese rural and urban women were able to detoxify contaminated maize by hand-sorting visibly diseased kernels. Residual contamination in the cleaned grain was at acceptable levels. Half of the study participants, however, were inefficient in discriminating and removing only disease kernels. Hand-sorting is economically viable for populations with limited food resources only if most of the starting material is recovered in the cleaned product. Thus, initiatives to reduce the risks of Fusarium mycotoxins in Nepalese maize should inform consumers about the occurrence of mycotoxins, and educate them to recognize and discard visibly diseased kernels.
Fig. 10. Study participants with colleagues at Plant Pathology Division in Nepal: Anne E. Desjardins (seated), Hira K. Manandhar (second from left), Krishna Shrestha (third from left), Gyanu Manandhar (right) (click image for larger view).
K. F. Cardwell, A. Hounsa, and S. Egal, International Institute of Tropical Agriculture, Cotonou, Benin; C. Wild, P. C. Turner, Y. Gong, Molecular Epidemiology Unit, University of Leeds Medical School, Leeds, UK; and A. Hall, London School of Hygiene and Tropical Medicine, London, UK
Corresponding author: Kitty Cardwell. email@example.com
Regulatory standards for aflatoxins produced by Aspergillus flavus and A. parasiticus have been enacted primarily because of the hepatocarcinogenic potential in adults. Nevertheless, alfatoxin has also been reported to be associated with exacerbation of the energy malnutrition syndrome Kwashiorkor in human children (22,45) and vitamin A malnutrition in animals (33), and many other problems (19). In various animal models, in addition to being hepatotoxic, aflatoxin causes significant growth faltering and is strongly immune-suppressive at weaning (44).
Fig. 11. Poor quality corn in a market in Lome, Togo (click image for larger view).
In parts of West Africa, e.g., The Gambia and Guinea Conakry, aflatoxin exposure has been linked to the consumption of groundnuts with a seasonality occurring in exposure levels (53,61). In Benin and Togo, maize is consumed and stored across all agroecological zones and, depending on agroecology, crop management, and length of storage, aflatoxin contamination levels averaging over 100 ppb in up to 50 percent of grain stores sampled have been recorded (21,54) (Fig. 11). Another factor in risk of food contamination with aflatoxin is the inherent toxicity of the resident A. flavus strains in the different agroecological zones. The A. flavus L (large sclerotia) strain, which produces either no alfatoxin or only aflatoxin B1, is found predominantly in moist zones; while the highly toxigenic African S (small sclerotia) strain (Fig. 12), an abundant producer of aflatoxins B1, B2, G1, and G2, is prevalent in dry zones (12,8).
Fig. 12. S (left) and L (right) strains of Aspergillus flavus on maize kernels (click image for larger view).
Rural populations in Benin and Togo rely on both groundnuts and maize as dietary staples and both crops are stored up to one year in most households. Maize is the principle weaning food in these countries used by 98 percent of households surveyed. Thus, quality degradation of maize during storage (Fig. 11) may have a direct effect on weaning children.
To determine the variance in aflatoxin exposure in 12 to 48 month-old human children, a cross-sectional study was conducted across 4 agro-ecological zones in Benin and Togo. Household and maternal economics, child birth spacing, and food consumption patterns of the index children were measured as covariates (Figs. 13 and 14). Blood pg/ml aflatoxin-albumin (60) was assessed in relation to household food basket, standard antropometric variables, and current health of 480 children (Figs. 15 and 16). In each of the 480 households, maize and peanut samples were collected for analysis of A. flavus colony forming units (CFU) and strain identification.
Fig. 13. International Institute of Tropical Agriculture medical team (click image for larger view).
Fig. 14. Food sampling and interviews were conducted in 480 households (click image for larger view).
Fig. 15. Blood sampling to measure aflatoxin-albumin blood serum adducts (click image for larger view).
Fig. 16. Anthropometry (click image for larger view).
Of household samples collected, over 90 percent of milled white maize was infected with A. flavus (L strain), while more than 20 percent contained CFU of S strain (Fig. 12).
Of peanut samples collected, 52 percent contained A. flavus L strain and 26.3 percent S strain. Only two colonies of Aspergillus parasiticus were noted.
Of 480 children, 99 percent had aflatoxin in their blood (18) (Fig. 16).
The correlation between blood toxin and CFU A. flavus (all strains) in foods was highly significant; in northern zones, S strains in both maize and peanut was significantly related to blood toxin levels. Across all zones, L strain CFU in white maize was the variable most significantly related to blood toxin.
Correlation was also found with the use of a local mustard made from the seeds of the Leguminacious tree Parkia bigbilosa.
Across zones, risk of exposure was not significantly related to socio-economic status (SES). Although differences existed within zones and among ethnic groups, exposure risk by SES was interactive, usually depending on whether the household had enough wealth to either stock or purchase peanuts.
An effort to elevate awareness of the problem of aflatoxins in maize, the staple food of much of sub-Saharan Africa, is underway with the assistance of Rotary International. Ex-ante data on awareness concerning mycotoxins in maize shows that there is very limited public awareness of the problem (28). Low public awareness does not mean that informed authorities are unaware of the problem.
The UNFAO has assisted most countries in sub-Saharan Africa to enter CODEX alimentarius standards into law, but monitoring of food quality for foods destined to local consumption is rare. Toxin testing laboratories are in place, generally government operated, but targeting only consignments for commodity export. Thus, for example in the case of peanut export to Europe, the best quality nuts are exported and what is left behind is not monitored for quality. Assuming that the basic laboratory infrastructure and trained staff exist, the constraint to effective internal food quality monitoring in countries with a low income tax base is the cost of sampling and analysis. The direct costs are the physical collection of the samples in a representative market sampling protocol (determined by overall population exposure variance) and costs of reagent grade solvents, expendables and standards. At the very minimum this costs approximately $25 US per sample not including laboratory overheads. Within a hundred samples the entire yearly operations budget for a developing country laboratory will have been exceeded. A system for cost sharing to make monitoring possible and sustainable, and sampling protocols appropriate for developing countries are needed.
Once public awareness is in place, policy makers must support government extension services to reach producers with campaigns imparting information on effective crop management options. In most of the developing countries of the world, the average farm size is 0.5 to 5 ha (approximately 1 to 10 acres). Extension services, then, must reach millions of small-scale farmers in a multitude of languages. This can be done, but it will not be cheap. An attempt is currently being made at IITA to assess the costs to farmers of farm and commodity management modifications to improve maize quality (K. Hell, IITA Benin, personal communication).
K. F. Cardwell, A. Desjardins, S. H. Henry, G. Munkvold, J. Robens
In the US, the FDA has allowed a tolerance of 20 ppb for adults, while European markets are striving for a lower CODEX importation standard of 2 ppb. By conservative calculations of estimated lost crop revenues and the cost of research and monitoring activities, in the US, it costs between $500 million and $1.5 billion a year to manage mycotoxic fungi and the toxins they produce, and that is not including secondary industry and international trade losses. Nevertheless, primary liver cancer as well as Hepatitis B prevalence is low in North America. Therefore, US or Europe are unlikely to achieve a decrease in liver cancer cases from more stringent aflatoxin standards (24). The most recent JECFA report concluded that a more substantial reduction in liver cancer would be obtained by vaccination against HBV rather than by drastically lowering aflatoxin standards (23).
On the other hand, it is very difficult to estimate the value to society of the health of its children. The long-term economic consequences are enormous if aflatoxin were causing poor immune-system development in young children as it does in weaning animals. It is conceivable that immunisation programs would be less effective, opportunistic disease more deadly, and diseases that impair immune system function more aggressive and virulent. Immunotoxic food contaminants would result in increased childhood pre-five mortality, and birth rates would have to be high in compensation. Data on the effect of aflatoxin on child growth and development in Africa highlight the need to maintain zero tolerance on aflatoxin for foods destined to young children around the world, particularly foods that are consumed frequently such as milk and cereals. It can be assumed that much of the benefit of having strict standards in food quality is an immeasurable return on population health, lower birth rates but higher child survivorship, excellent nutritional and immunological status of the population with the concomitant results of high individual and societal productivity.
Although the risks due to Fusarium toxins are less well elucidated, suggested advisory levels range from 0-4 ppm. As fumonisins are found in maize and trichothecenes such as DON are found in maize, wheat, and barely, the costs to the US could easily mount up as quickly as those of aflatoxin. Fortunately, systems in place for managing aflatoxin could be pressed into service for fusarium toxins as well. Corn subject to the lowest recommended fumonisin levels comprises a small percentage of US corn (about 3.5 percent, including dry milling, masa, popcorn, and corn fed to horses). The segments of the corn market that may experience increased costs as a result of the FDA guidelines are the export and dry milling segments. Increased costs will be primarily related to fumonisin testing. The standardization of practical commercial tests for fumonisins is an unresolved issue that may result in confusion during the initial years. Depending on the annual occurrence of fumonisins and the response of foreign buyers, these costs could be negligible in most years. The existence of FDA guidelines may lead to increased awareness and greater care taken by corn producers feeding livestock on-farm, particularly swine. In this case, the net economic effect may be positive as a result of improved animal health.
In less developed countries residing in the tropics, from 22 percent fumonisin to 56 percent aflatoxin incidence has been reported. No economically feasible processing procedures are currently available at the household level to remove toxins from foods that are already contaminated. Sorting out poor-looking grain is the last resort, and is effective under circumstances of general food security and awareness of the population of the needy. Nevertheless, sorting is subjective. In Africa, Hell (IITA Benin, personal communication) found that the stringency of the sorting required to bring poor quality maize into compliance with safety standards, was not likely to be practised in situations where food security is an issue.
For all the medical literature about the toxic effects of mycotoxins on humans and animals, for all the knowledge about the chemistry and modes of action, for all the cost to the world and all the tea in China, reliable solutions are still few and far between. As plant pathologists, this problem is still on our plate after almost 30 years of research. Economically effective solutions are those that are agricultural technology based that exclude the fungi from the host and/or block the production of mycotoxins in the host substrates.
In the USA: Aflatoxins are being reliably managed by the guidelines in place, and the risk of exposure under current practices is not considered to be a public health threat.
Nevertheless, the management of aflatoxins costs millions of US dollars per year and research into definitive solutions must continue.
The FDA guidelines for fumonisins will probably not have a traumatic impact on corn marketing internally as the proposed levels are achievable without a major disruption of the system.
The food industry already imposes its own standards, which are consistent with the FDA guidelines.
However, there are some potential losses of revenue to producers in the form of reduced prices for high-fumonisin corn, and there could be increased costs for testing at grain elevators. The extent of this depends on how willing the elevator operators will be to accept high-fumonisin corn with the intent to blend it. This willingness will vary with the overall level of contamination of the crop. In low-fumonisin years, operators may be willing to accept occasional fumonisin contamination without any penalty to the seller. In high-fumonisin years, there will be more testing and a greater tendency to reduce the price paid for contaminated grain.
In developing countries: There is little doubt that high levels of exposure of people to food-borne mycotoxins is a serious threat to public health. It is a developmental issue, which embraces childhood survival, demographics, immune system function, the economic and human resource drain due to cancers, as well as food security where livestock feeds are contaminated.
Research is needed on inexpensive and appropriate sampling and testing protocols.
Research on identification and application of appropriate technologies for obtaining low grain moisture at harvest and maintaining low grain moisture during storage are needed.
Research is needed on traditional food preparation technologies, such as fermentations and nixtimalization, or chelating additives such as clays or yeasts that may lower mycotoxins in prepared foods.
Research must continue to develop crop plant cultivars that are resistant (or at least not susceptible) in the field to infection by mycotoxin-producing fungi. Breeding for high yield alone is not enough.
Research to reduce mycotoxin vulnerability of crops is as important today as ever!
International Institute of Tropical Agriculture (IITA)
International Food Policy Research Institute (IFPRI)
National Corn Growers Association (NCGA)
FDA Center for Food Safety and Applied Nutrition: The Food Defect Action Levels
FDA Center for Food Safety Applied Nutrition: Mycotoxins in Domestic Foods
USDA Peanut Research Lab: Control of Mycotoxin Contamination of Peanuts
1999 ICAS International Mycotoxin Seminar on Fusarium Mycotoxins
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