FIELD EVIDENCE: Bt CORN AND MYCOTOXIN REDUCTION
Felicia Wu
February, 2008

Introduction
Though many of the earliest transgenic crops introduced traits with primary benefits going to growers, some of those crops also provide secondary benefits to consumer health. Bt corn is such an example. It is one of the most commonly grown transgenic crops in the world today. It contains a gene from the soil bacterium Bacillus thuringiensis, which encodes for a protein that is toxic to certain members of the order Lepidoptera. These include the common corn pests European corn borer (ECB, Ostrinia nubilalis), Southwestern corn borer (SWCB, Diatraea grandiosella), corn earworm (CEW, Helicoverpa zea), and corn rootworm (CRW, Diabrotica spp). Bt corn is harmless to vertebrates and non-lepidopteran insects.

One indirect benefit from Bt corn adoption is lower levels of mycotoxin contamination. Mycotoxins are secondary metabolites of fungi that colonize crops. They are considered unavoidable contaminants in foods, as best-available technologies cannot completely eliminate their presence in crops. Insect damage is one factor that predisposes corn to mycotoxin contamination, because insect herbivory creates kernel wounds that encourage fungal colonization, and insects themselves serve as vectors of fungal spores. Thus, any method that reduces insect damage in corn also reduces the risk of fungal contamination. Indeed, in a variety of field studies, Bt corn has been shown to have significantly lower levels of common mycotoxins, the subject of which is reviewed in this article.

Four common mycotoxins in corn
Four mycotoxins that contaminate corn are fumonisin, aflatoxin, deoxynivalenol, and zearalenone. Fumonisins are produced by the fungi Fusarium verticillioides (formerly F. moniliforme) and Fusarium proliferatum. Consumption of fumonisin has been associated with elevated human esophageal cancer incidence in various parts of Africa, Central America, and Asia and among the black population in Charleston, South Carolina. Because FB1 reduces uptake of folate in different cell lines, fumonisin consumption has been implicated in connection with neural tube defects in human babies. Fumonisins can be highly toxic to animals, causing diseases such as equine leukoencephalomalacia in horses and porcine pulmonary edema in swine.

Aflatoxins, produced by Aspergillus flavus and Aspergillus parasiticus, are the most potent naturally-occurring liver carcinogens known. For people infected with hepatitis B or C, aflatoxin consumption raises more than tenfold the risk of liver cancer compared with either exposure alone. Acute aflatoxicosis, characterized by hemorrhage, acute liver damage, edema, and possibly death, can result from extremely high doses of aflatoxin. Aflatoxin consumption is also associated with stunting in children and immune system disorders. Aflatoxins cause a variety of illnesses in animals as well. In poultry, aflatoxin consumption results in liver damage, impaired productivity and reproductive efficiency, decreased egg production in hens, inferior egg-shell quality, inferior carcass quality, and increased susceptibility to disease. In cattle, the primary symptoms are reduced weight gain, liver and kidney damage, and reduced milk production.

Deoxynivalenol (DON, or vomitoxin), the most common mycotoxin in cereals, is produced by the fungus Fusarium graminearum and the related species Fusarium culmorum in cooler climates. It is a significant contaminant of corn, wheat, and barley in generally more temperate regions of the world, such as the United States, Canada, and Europe. DON is an inhibitor of protein biosynthesis and causes human and animal effects ranging from feed refusal, vomiting, and nausea to immunosuppression and loss of productivity.

Zearalenone, like DON, is produced by F. graminearum. Zearalenone is sometimes referred to as a mycoestrogen, as it causes estrogenic responses and vulvovaginitis in swine. At higher concentrations, zearalenone causes similar effects in poultry and cattle. In humans, there has been limited evidence of an association between zearalenone consumption and premature puberty.

Many nations have established regulatory standards on the maximum tolerated levels of mycotoxins in food and feed. Thus, aside from the health risks described above, mycotoxin contamination can also reduce the price paid or cause market rejection of entire corn loads.

Field evidence of Bt cornís reduction, or lack thereof, of mycotoxins
Several different factors can predispose corn to fungal growth and subsequent mycotoxin accumulation. In pre-harvest corn, high or unusually fluctuating temperatures, drought stress, incompatibility of the corn hybrid for the region in which it is planted, and insect pest damage increase mycotoxin levels. Notably, insect damage is well recognized as a collateral factor in mycotoxin development. Insect pests create wounds on the corn kernels and act as vectors for certain types of fungal spores. In post-harvest corn, storage conditions such as high humidity, pre-harvest presence of fungi, and the presence of stored grain insects may contribute to further fungal development and accumulation of mycotoxins in corn. Again, insects in storage create grain wounds and spread fungal spores to cause further post-harvest accumulation of mycotoxins.

Where insect pests are present, Bt corn has lower levels of certain mycotoxins than non-Bt isolines. The insect pests ECB, SWCB, and CEW have been shown in field trials to contribute to the concentration of mycotoxins in corn. Insect-damaged corn is also prone to mycotoxin accumulation in storage. Therefore, to the extent that Bt corn has lower levels of insect damage, it indirectly controls for one of the most important predisposing factors of mycotoxin accumulation.

In the Corn Belt region of the United States, field studies have demonstrated that when insect damage from ECB or SWCB is high, fumonisin concentrations are significantly lower in Bt corn compared with conventional corn. Importantly, in multiple locations across the US, Bt corn (compared with non-Bt isolines) had fumonisin levels that were below the Food and Drug Administration (FDA)ís 2-ppm guideline for fumonisin in food1. Yet another study showed that Bt hybrids can reduce fumonisin levels when ECB is favored, but not in seasons when CEW is favored. In Europe and in other parts of the world, Bt corn has been shown in field trials to have significantly lower fumonisin levels than non-Bt isolines. Significantly lower levels of fumonisin were measured in Bt hybrids when compared to controls in 288 separate test sites in France, Italy, Turkey, Argentina, and the United States. Fumonisin concentrations in Bt grain were often lower than 4 mg/kg, with a significant proportion of these below 2 mg/kg2.

Compared with fumonisin, insect pest damage is less strongly correlated with aflatoxin concentrations in corn, as multiple factors predispose corn to accumulation of aflatoxin. The lepidopteran insects that are controlled by currently commercially available Bt corn varieties are not as important in predisposing plants to infection by A. flavus as they are for F. verticillioides; and A. flavus can infect corn not just through kernel wounds caused by insects, but through the silks. Indeed, field tests of aflatoxin reduction in Bt corn show a mixed record. Bt hybrids were shown to have lower aflatoxin levels than non-Bt isolines in the southern US in years when aflatoxin levels would otherwise have been high, but there was no significant difference when aflatoxin levels were low in both Bt and non-Bt isolines. Other studies show no significant effect of Bt corn, or mixed results. Studies have shown that other factors, such as drought stress and individual hybrid vulnerability, are more important in determining aflatoxin contamination levels than insect damage. Two field studies in Italy independently showed no impact of Bt corn in reducing aflatoxin levels. Importantly, however, new events of Bt corn are being developed that provide better protection against corn earworm and fall armyworm, insects that are closely associated with aflatoxin accumulation in corn3. Field trials have demonstrated that these Bt corn varieties do indeed have significantly lower aflatoxin levels than non-Bt isolines4.

F. graminearum is similar to A. flavus in that it can infect corn without insect damage. Correspondingly, the evidence for lower levels of deoxynivalenol in Bt corn is also mixed. In Canada, where European corn borer pressure was high, the use of Bt hybrids reduced the level of DON by 59% compared with non-Bt isolines. In these cases, Bt corn consistently had levels of DON that were acceptable by FDA standards (i.e., below 1 mg/kg)5. Where ECB pressure was low, however, there was no significant difference between DON levels in Bt vs. non-Bt hybrids (which were below 1 mg/kg in either case). One study showed that in animal feed, the only nutritional difference between Bt and non-Bt corn feeds was that Bt corn had lower levels of DON and zearalenone6. However, in a central European field study, the association between European corn borer damage and DON concentrations was not consistent across years.

Two studies have examined whether Bt corn has lower levels of zearalenone, also produced by F. graminearum. One study found that though zearalenone levels were generally low in field tests in France and Spain, Bt hybrids did show significantly lower zearalenone at certain test sites. As described above, animal feed made from Bt corn was shown to have lower zearalenone levels.

Table 1 summarizes the available literature on currently commercially-available Bt corn events and mycotoxin reduction, or lack thereof, evidenced in field trials around the world. Specific references for all these studies are summarized in reference 7 (below).

Table 1. Studies demonstrating current events of Bt cornís control, or lack thereof, of fumonisin, aflatoxin, DON, and zearalenone in field trials.

Bt corn lower mycotoxins than non-Bt isolines?

Yes

No

Fumonisin

U.S. Midwest

Throughout U.S.

U.S. Midwest when European corn borer favored

France, Italy, Turkey, Argentina

Germany

Philippines

U.S. Midwest when corn earworm favored

Aflatoxin

U.S. South when aflatoxin levels high, or fungus applied through non-wounding technique

U.S. South, some years

U.S. South, new varieties controlling corn earworm and fall armyworm

U.S. South when aflatoxin levels low, or fungus applied by wounding technique

U.S. South

U.S. South, some years

Italy

Deoxynivalenol

Canada

Germany (animal feed)

Eastern Europe, some years

Eastern Europe, some years

Germany

Zearalenone

France and Spain

Germany (animal feed)

Summary
Bt corn is being planted at an ever-growing rate around the world. Aside from its primary benefit of insect pest protection, it has the important secondary benefit of reducing mycotoxin concentrations, because of the relationship between insect pest damage and fungal colonization. The currently-available varieties of Bt corn have shown strong evidence in field conditions worldwide of having significantly lower fumonisin levels than non-Bt isolines. There is also limited evidence for lower levels of DON and zearalenone in Bt corn, although there are fewer field studies on these relationships. The more extensive work on aflatoxin reduction in Bt corn has yielded mixed results, but new varieties of Bt corn that may be commercialized soon are likely to have a more significant impact on aflatoxin levels. Hence, Bt corn is an important potential tool for mycotoxin control, both in the US and in other nations.

References

1. Munkvold GP, Hellmich RL, Rice LG. (1999) Comparison of fumonisin concentrations in kernels of transgenic Bt maize hybrids and nontransgenic hybrids. Plant Disease 83(2), 130-138

2. Hammond B et al. (2003) Reduction of fumonisin mycotoxins in Bt corn. The Toxicologist 72(S-1), abstract 1217

3. Munkvold GP. (2003) Cultural and genetic approaches to managing mycotoxins in maize. Annual Review of Phytopathology 41, 99-116

4. Headrick J.M. (2006) Application of multiple approaches toward reducing aflatoxin contamination of corn grain. Proceedings of the 2006 Annual Multi-Crop USDA Aflatoxin/Fumonisin Elimination & Fungal Genomics Workshop, Oct 16-18, 2006. Ft Worth Texas, p. 33

5. Schaafsma A et al. (2002) Effect of Bt-corn hybrids on deoxynivalenol content in grain at harvest. Plant Disease 86(10), 1123-1126

6. Aulrich K et al. (2001) Genetically modified feeds (GMO) in animal nutrition: Bacillus thuringiensis (Bt) corn in poultry, pig and ruminant nutrition. Archives of Animal Nutrition 54, 183-195

7. Wu F. (2007) Bt corn and mycotoxin reduction. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 2(060), 8 pp

 

Felicia Wu
Department of Environmental & Occupational Health, Graduate School of Public Health
University of Pittsburgh, 100 Technology Dr., Pittsburgh, PA 15219
few8@pitt.edu