Reprinted from the Radcliffe’s IPM World Textbook (University of Minnesota)
D. Pimentel1, T. W. Culliney2, and T. Bashore1
1College of Agriculture and Life Sciences
Cornell University, Comstock Hall
Ithaca, New York 14853-0901
2Hawaii Department of Agriculture
Division of Plant Industry
Honolulu, Hawaii 96814
Chemical technology has expanded tremendously during the past fifty years. For example, approximately 70,000 different chemicals are currently used and released into the environment in the United States alone (Newton and Dillingham 1994). An estimated 100,000 chemicals are used worldwide (Nash 1993). In the US, nearly 10% of the approximately 3 billion kg of toxic chemicals released per year is known to be carcinogenic (USBC 1994). More than 500,000 kg of approximately 600 different pesticide chemicals are applied annually in the US, while approximately 2.5 million tons are applied throughout the world (Pimentel 1996). Additionally, the World Health Organization (1992) reports that roughly three million pesticide poisonings occur annually and result in 220,000 deaths worldwide. Both economically and in terms of human life, these poisonings represent an enormous cost for society.
Some investigators, however, claim that the health risks from natural chemicals in foods are even greater than the risks from pesticide residues (see Pimentel and Greiner 1996). They maintain that some constituents of commonly consumed vegetables like cabbage and broccoli are more toxic to humans than chemical pesticides in foods, although this has not been conclusively proven (see Pimentel and Greiner 1996).
Not only do such alarming claims muddle the food choices the public can safely make, but they also run contrary to the latest advice given by nutritional authorities. The importance of a nutritious food supply to human health has been emphasized in reports which recommend a diet high in complete carbohydrates, fruits, and vegetables– particularly those vegetables high in carotene like cabbage, broccoli, and other brassicas. These are, as previously mentioned, a few of the same foods which some investigators believe to contain natural chemicals that pose a risk to human health. Therefore, the aim of this discussion is to assess the known public health risks of pesticides and naturally occurring toxins in foods.
Pesticides and Public Health
Human poisonings and their related illnesses are clearly the highest price paid for pesticide use. About 67,000 pesticide poisonings resulting in an estimated twenty-seven accidental fatalities are reported each year in the US (Litovitz et al. 1990). Due to gaps in the demographic data, however, this figure may represent only 73% of the total number of poisonings (Pimentel and Greiner 1996). Although it is impossible to place a precise monetary value on human life, the cost of human pesticide poisonings has been estimated. Insurance industry studies have computed monetary ranges between $1.6 and $8.5 million for the value of a “statistical life” (Nash 1994). Alternatively, the conservative estimate of $2.2 million per human life– the average value that the surviving spouse of a slain New York City policeman receives– may be used (Nash 1994). Based on this figure and the available data, human pesticide poisonings and related illnesses in the US are estimated to total about $933 million each year (Pimentel 1996).
The situation is even worse in other regions of the world. Approximately 80% of the pesticides produced annually in the world are used in developed countries (WRI/UNEP/UNDP 1994), but less than half of all pesticide-induced deaths occur in these countries (Pimentel and Greiner 1996). A higher proportion of pesticide poisonings and deaths occur in developing countries where there are inadequate occupational safety standards, protective clothing, and washing facilities; insufficient enforcement; poor labeling of pesticides; illiteracy; and insufficient knowledge of pesticide hazards (Pimentel and Greiner 1996).
Additionally, average pesticide residue levels in food are often higher in developing countries than in developed nations. For example, a study in Egypt reported that a majority of assayed milk samples, when tested for fifteen different pesticides, contained residue levels between 60% and 80% (Dogheim et al. 1990). By way of contrast, 50% of the milk samples analyzed in a US milk study had pesticide residues, all in trace quantities well below EPA and FDA regulatory limits (Trotter and Dickerson 1993).
About 35% of the foods purchased by American consumers, however, do have detectable levels of pesticide residues (FDA 1990). Between 1-3% of these foods have pesticide residue levels that are above the legal tolerance level (FDA 1990). Residue levels may be even higher than this because the analytical methods now employed in the US detect only about one-third of the pesticides in use (Minyard and Roberts 1991). The contamination rate is undoubtedly higher for fruits and vegetables because these foods receive the highest dosage of pesticides. In fact, one USDA study has shown that some pesticide residue remains in fruits and vegatables even after they have been washed, peeled, or cored (Wiles and Campbell 1994). Consequently, there are many justifiable reasons why 97% of the public is concerned about pesticide residues in its food (Pimentel and Greiner 1996).
Throughout the world, the highest levels of pesticide exposure are found in farm workers, pesticide applicators, and people who live adjacent to heavily treated agricultural land. Because farmers and farm workers directly handle 70-80% of the pesticides they use, they are at the greatest risk of exposure (McDuffie 1994). The epidemiological evidence suggests a significantly higher rate of cancer incidence among farmers and farm workers in the US and Europe than among non-farm workers in some areas (Cantor et al. 1992). In these high-risk populations, there is strong evidence for associations between lymphomas and soft-tissue sarcomas and certain herbicides (Zahm et al. 1990), as well as between lung cancer and exposure to organochlorine insecticides (Pesatori et al. 1994).
Consequently, both the acute and chronic health effects of pesticides warrant attention and concern. While the acute toxicity of most pesticides is well documented (Ecobichon et al. 1990), information on chronic human illnesses such as cancer is not as sound. For example, based on animal studies, the International Agency for Research on Cancer found “sufficient” evidence of carcinogenicity in eighteen pesticides and “limited” evidence in an additional sixteen pesticides (WHO/UNEP 1989). Similarly, studies have reported an increased prevalence of certain cancers in farmers (Cantor et al. 1992). However, a recent study in Saskatchewan found no significant difference in non-Hodgkin’s lymphoma mortality between farmers and nonfarmers (Wigle et al. 1990). In addition, D. Schottenfeld of the University of Michigan (Pimentel and Greiner 1996) estimates that fewer than 1% of the human cancer cases in the US are attributable to pesticide exposure. Since there are approximately 1.2 million cancer cases annually (USBC 1995), Schottenfeld’s assessment suggests that less than 12,000 cases of cancer per year are due to pesticides.
However, there is evidence to suggest that many other acute and chronic maladies are associated with pesticide use. For example, the recently banned pesticide dibromochloropropane (DBCP), which is used for plant pathogen control, was found to cause testicular dysfunction in animal studies (Shemi et al. 1989) and was linked to infertility in human workers who had been exposed to the chemical (Potashnik and Yanai-Inbar 1987). Also, a large body of evidence obtained from animal studies suggests that pesticides can produce immune dysfunction (Thomas and House 1989). In a study of women who had chronically ingested groundwater contaminated with low levels (mean of 16.6 ppb) of aldicarb, Fiore et al. (1986) reported evidence of significantly reduced immune response, although these women did not exhibit any overt health problems.
There is also growing evidence of sterility in humans and various other animals, particularly in males, due to various chemicals and pesticides in the environment. Sperm counts in Europe have declined by about 50% and continue to decrease an additional 2% per year. Young male river otters in the lower Columbia River and male alligators in Florida’s Lake Apopka have smaller reproductive organs than males in unpolluted regions of their respective habitats (Colborn et al. 1996).
Although it is often difficult to determine the impact of individual pesticides and other chemicals, the chronic health problems associated with organophosphorus pesticides– which have largely replaced the banned organocholorines– are of particular concern (Ecobichon et al. 1990). The malady Organophosphate Induced Delayed Polyneuropathy (OPIDP) is well-documented and is marked by irreversible neurological defects (Lotti 1992). The deterioration of memory, moods, and the capacity for abstract thought have been observed in some cases (Savage et al. 1988), while other cases indicate that persistent neurotoxic effects may result even after the termination of an acute organophosphorus poisoning incident (Ecobichon et al. 1990).
Chronic conditions such as OPIDP constitute an important public health issue because of their potential cost to society. For example, the effect of pesticides on children has become a growing concern. Children can be exposed to pesticides on a daily basis in a variety of ways: through the foods they eat, in the houses where they live, or in the communities where they play (Pimentel and Greiner 1996). With the increased realization of the distinct physiological differences between adults and children, it has become obvious that the present pesticide tolerance and regulatory system, as it relates to children, is severely lacking. All of the regulations to date have been based on adult tolerances. Children have much higher metabolic rates than adults, and their ability to activate, detoxify, and excrete xenobiotic compounds is different than that of adults. Also, because of their smaller physical size, children are exposed to higher levels of pesticides per unit of body weight. Evidence of this is found in a study which reported that 50% of all pesticide poisonings in England and Wales involved children under the age of ten (Casey and Vale 1994). The use of pesticides in the home has also been linked to childhood cancer (Leiss and Savitz 1995). In general, the realization that children’s sensitivities to toxins are much different than those of adults has provided the impetus for the movement towards setting specific pesticide regulations with children in mind (Wiles and Campbell 1994).
Natural Toxins in Foods
All human food is a complex mixture of chemicals including carbohydrates, amino acids, fats, oils, and vitamins, some of which may be toxic if consumed in large quantities (Strong 1974). Plants contain some chemicals that are known to be toxic to both animals and humans. Some of these chemicals evolved in plants to protect them from insects, plant pathogens, and other organisms (Pimentel 1988). A small number of these chemicals, such as the hydrazines found in a few mushrooms, are highly carcinogenic. In general, however, the adverse effects of toxic chemicals in plants are related to interference with nutrient availability, metabolic processes, detoxification mechanisms, and allergic reactions in particular animals and humans. Many natural toxins are found in staple foods of the human diet such as grains and legumes. Some of these are discussed below.
Lectin proteins (phytohemagglutinins) are present in varying amounts in legumes and cereals, and in very small amounts in tomatoes, raw vegetables, fruits, and nuts. Ricin, a lectin which is extremely toxic and can be fatal to humans, was used as an insecticide at one time. When untreated lectins are eaten, they agglutinate red blood cells and bind to the epithelial cells of the intestinal tract, impairing nutrient absorption. Fortunately, heat destroys the toxicity of lectins.
Lathyrogens, found in legumes such as chick peas and vetch, are derivatives of amino acids that act as metabolic antagonists of glutamic acid, a neurotransmitter in the brain (NAS 1973). When foods containing these chemicals are eaten in large amounts by humans or other animals, they cause a crippling paralysis of the lower limbs and may result in death. Lathyrism is primarily a problem in some areas of India.
Protease inhibitors are widely distributed throughout the plant kingdom, particularly in the Leguminosae and, to a lesser extent, in cereal grains and tubers. These substances inhibit the digestive enzymes trypsin and chymotrypsin (Bender 1987). For example, raw soybeans contain a protein that inactivates trypsin and results in a characteristic enlargement of the pancreas and an increase in its secretory activity. It is this latter effect, mediated by trypsin inhibition, that depresses growth. Clearly, soybeans and other related legumes should be properly cooked and processed before being eaten.
Potatoes– which contain two major glycoalkaloid fractions, alpha-solanine and alpha-chaconine– that have been exposed to sunlight show a significant increase in their alkaloid content (NAS 1973). Solanine is a cholinesterase inhibitor and can cause neurologic and gastrointestinal symptoms (Oser 1978), potentially including the fatal depression of the activity of the central nervous system.
Cyanogenic glycosides occur in many food plants like cassava, lima beans, and the seeds of some fruits– peaches, for example. Because of their cyanide content, ingestion of large amounts of cassava and, to a lesser extent, lima beans can be fatal if these foods are eaten raw or are not prepared correctly (Strong 1974). Cassava toxicity is much reduced by peeling, washing in running water to remove the cyanogen, and then cooking and/or fermenting to inactivate the enzymes and to volatilize the cyanide. In regions like Africa where cassava is a staple food, care is taken in its preparation for human consumption.
Goitrogens (glucosinolates), which inhibit the uptake of iodine by the thyroid, are present in many commonly consumed plants. They are estimated to contribute approximately 4% to the worldwide incidence of goiters in humans (Liener 1986). Cabbage, cauliflower, Brussels sprouts, broccoli, kale, kohlrabi, turnips, radish, mustard, rutabaga, and oil seed meals from rape and turnip all possess some goitrogenic activity (Coon 1975). Effects of thyroid inhibition are not counteracted by the consumption of dietary iodine. The nature and extent of toxicity of glucosinolates are still the subject of debate. Although there are few, if any, acute human illnesses caused by glucosinolates, chronic and subchronic effects remain a possibility (Heaney and Fenwick 1987).
Additional foods with the potential for antithyroid activity include plants in the genusAllium (onion group); other vegetables such as chard, spinach, lettuce, celery, green pepper, beets, carrots, and radishes; legumes such as soybeans, peas, lentils, beans, and peanuts; nuts such as filberts and walnuts; fruits such as pears, peaches, apricots, strawberries, and raisins; and animal products such as milk, clams, oysters, and liver (Coon 1975). However, it has not been proven that a diet of these foods would be goitrogenic unless they comprised an excessively high proportion of the diet, a substantial amount of them were eaten raw, or they were not well cooked. Although goitrogens in foods are largely destroyed by thorough cooking, it must be acknowledged that many of the foods listed above are eaten uncooked (Coon 1975).
The most potent natural toxins responsible for human health risks are the mycotoxins. These are not strictly plant compounds but toxic metabolites produced by fungi infesting foodstuffs, especially cereals and nuts, which have been stored under conditions of elevated temperature and high humidity (NAS 1989). Among the ailments caused by these mycotoxins, the most notable historically is ergotism, or “St. Anthony’s Fire,” which afflicted people centuries ago. This was caused by ergot alkaloids produced by Claviceps purpurea growing on cereal grains (NAS 1973). Although some mycotoxins have been identified as potent liver carcinogens in experimental animals, their role as human carcinogens has not been established.
In addition to microbes, other potentially dangerous contaminants in plants used as food can originate from the uptake of such chemicals as nitrate from soil and drinking water (Coon 1975). Nitrate is not considered a human carcinogen, but nitrosamines which are formed from nitrates and nitrites (such as those used in curing meats) are carcinogenic in animals (NAS 1989). Other hazardous chemicals like lead, iodine, mercury, zinc, arsenic, copper, and selenium are found in varying quantities in foods, and if consumed in large amounts, can cause human health problems or death.
The extent of the risks to human health associated with ingesting naturally occurring toxins remains a scientifically contentious matter (Watson 1987). Debate on this subject has been clouded by the absence of a systematic approach to defining and, in particular, quantifying human hazards. Although data have been assembled on the chemical properties and biological sources of most of these compounds, their long-term risks to public health have not been established. In fact, the National Research Council has concluded that the current data on human dietary exposure is insufficient and has underscored the need for new studies with larger sample sizes and refined testing methods (NAS 1996). Above all, it is important to emphasize that there is presently no firm evidence to demonstrate a link between long-term ingestion of natural toxins in commonly eaten foods and any type of chronic human illness (NAS 1989; NAS 1996).
Most individuals feel that they have little or no choice other than depending on the integrity of scientists and government agencies to ban dangerous pesticides and regulate the dosages and application procedures of those pesticides that are permitted. The last decade has witnessed a growing awareness in the public sector about the chemicals it is exposed to in food, air, and water. Although these are perceived as risks over which the individual has no control, some of the public’s concerns are being translated into action in order to eliminate the most toxic pesticides. On an individual level, some consumers are buying pesticide-free foods, while collectively– as in the “Big Green” initiative in California– they are voicing their opinions through the ballot box.
As pest control research focuses on the ecology of pests and on the agroecosystem as a whole, results from different regions of the world indicate that pesticide use can be reduced substantially. Sweden, Norway, Denmark, the Netherlands, and the Canadian province of Ontario have all adopted effective programs to reduce pesticide use by 50-75%. In Indonesia, for example, the investment of $1 million per year in ecological research in conjunction with extension programs that train farmers to conserve natural enemies is paying large dividends. Pesticide use for rice in Indonesia has been reduced 65%, while rice yields have increased by 12%. As a consequence, the Indonesian government has been able to eliminate $20 million in pesticide subsidies to farmers (Pimentel 1996).
In the US, it is estimated that pesticide use can be reduced by as much as 50% at an estimated savings of at least $500 million per year without reducing crop yields or substantially reducing the “cosmetic standards” of fresh fruits and vegetables. By implementing IPM programs in the state of New York, for example, sweet corn processors saved $500,000 per year and maintained high yields while reducing pesticide treatments 55-65%. Pesticide use has been reduced on other crops in New York as well (Pimentel 1996).
Nevertheless, pesticides will continue to be used on certain crops, and individuals must determine the degree of risk they are willing to accept. With food selection, most individuals have the option of making personal choices. However, the acknowledged health benefits of the foods recommended by nutritional authorities are such that consumers should not be frightened into eliminating them from their diets because of the implied danger from naturally occurring toxins. Risk from naturally occurring toxins in foods– as well as from pesticide residues– depends on the dosage of the chemical, the time of exposure, and the susceptibility of the individual human. These data, along with the sound experimental investigation of particular pesticides or natural toxins, are essential in estimating the potential risks to humans of various toxic chemical exposure in human foods.
Plants do contain many chemicals– hydrazines and mycotoxins, for example– that are highly toxic to animals and humans. While these compounds may play important roles in influencing the incidence of certain types of human cancer, the exact proportion of cancers that are due to “natural” versus synthetic carcinogens is not known (Perera et al. 1991). However, there is evidence to suggest that synthetic chemicals present in food may increase cancer risk over that which may be posed by the presence of natural toxins alone. For example, laboratory rodent diets also contain many of the same naturally-occurring toxins present in the human diet. Nevertheless, compounds such as aflatoxin, TCDD, and DBCP, when added to the diet of mice and rats, significantly increase tumor incidence, even when present at very low levels. This suggests that, in several cases, the risk of tumorigenesis from certain synthetic food contaminants is increased in the animal over any risk presented by the background level of “natural pesticides” (Weinstein 1991). Lacking contrary evidence, there is no reason to assume a difference in humans.
However, important caveats should be noted in drawing conclusions from risk analyses of dietary exposure to toxins. Short-term screens such as the “Ames test”, whether for genetic damage or increased cell proliferation, are far from 100% accurate in predicting carcinogenicity and are not a replacement for long-term bioassays (Cohen and Ellwein 1991). Also, no matter how suggestive epidemiological or experimental studies may be, they cannot provide unequivocal proof that a certain diet will increase the risk of cancer. No study has directly demonstrated that implementing dietary changes in a given individual inhibited the onset of cancer or kept an established cancer from spreading.
Furthermore, unlike animal experimentation, humans cannot be kept physically isolated for long periods of time and fed diets containing possibly toxic substances. Nor can heredity or environmental factors be controlled. Data from laboratory animal tests and epidemiological studies with humans must serve as guides for assessing the safety of the food supply. Ultimately, it is extremely difficult in the absence of further information to predict the sensitivity of humans to the tumor-promoting, mitogenic, or cytotoxic potential of a given compound. Thus, risk extrapolation under conditions in which individuals are exposed to multiple factors and in heterogeneous populations (the situation in the real world) is much more complicated than envisioned by some authors, e.g. Ames and Gold 1990.
The causes of chronic illnesses, including cancers, are extremely complex. In their lifetime, individuals who differ in genetic make-up and susceptibility are exposed to a wide variety of carcinogens. Some chemicals by themselves are safe but may act as synergists or promoters in concert with other chemicals to cause illness. Future research as to how human health is affected by increasing exposure to all chemicals is of prime importance. The public is skeptical of what it reads and hears, and it is becoming more wary of being exposed to pesticides and other chemicals.
Ames, B.N. and L.S. Gold. 1990. Too many rodent carcinogens: mitogenesis increases mutagenesis. Science 249: 970-971.
Bender, A.E. 1987. Effects on nutritional balance: antinutrients. Pages 110-124 in D.H. Watson, ed. Natural toxicants in food: progress and prospects. Chichester, England: Ellis Horwood Ltd. 254 pp.
Cantor, K.P., A. Blair, G. Everett, R. Gibson, L.F. Burmeister, L.M. Brown, L. Schuman and F.R. Dick. 1992. Pesticides and other agricultural risk factors for non-Hodgkin’s lymphoma among men in Iowa and Minnesota. Cancer Research 52: 2447-2455.
Casey, P. and J.A. Vale. 1994. Deaths from pesticide poisoning in England and Wales: 1945-1989. Human & Exp. Toxicol. 13: 95-101.
Cohen, S.M. and L.B. Ellwein. 1991. Carcinogenesis mechanisms: the debate continues. Letters. Science 252: 902-903.
Colborn, T., J.P. Myers and D. Dumanoski. 1996. Our stolen future: how we are threatening our fertility, intelligence, and survival: a scientific detective story. New York: Dutton.
Coon, J.M. 1975. Natural toxicants in foods. J. Am. Dietet. Assoc. 67: 213-218.
Dogheim, S.M., E.N. Nasr, M.M. Almaz and M.M. El-Tohamy. 1990. Pesticide residues in milk and fish samples collected from two Egyptian Governorato. Jour. Assoc. Off. Anal. Chem. 73: 19-21.
Ecobichon, D.J., J.E. Davies, J. Doull, M. Ehrich, R. Joy, D. McMillan, R. MacPhail, L.W. Reiter, W. Slikker and H. Tilson. 1990. Neurotoxic effects of pesticides. Pages 131-199 in C. F. Wilkinson and S. R. Baker, eds. The Effect of Pesticides on Human Health. Princeton Scientific Pub. Co., Inc.: Princeton, NJ.
FDA. 1990. Food and Drug Administration Pesticide Program Residues in Foods: 1989. Jour. Assoc. Off. Anal. Chem. 73: 127A-146A.
Fiore, M.C., H.A. Anderson, R. Hong, R. Golubjatnikov, J.E. Seiser, D. Nordstrom, L. Hanrahan and D. Belluck. 1986. Chronic exposure to aldicarb-contaminated groundwater and human immune function. Environ. Res. 41 : 633-645.
Heaney, R.K. and G.R. Fenwick. 1987. Identifying toxins and their effects: glucosinolates. Pages 76-109 in D.H. Watson, ed. Natural toxicants in food: progress and prospects. Chichester, England: Ellis Horwood Ltd. 254 pp.
Leiss, J.K. and D.A. Savitz. 1995. Home pesticide use and childhood cancer: a case-control study. Am. J. Public Health 85: 249-252.
Liener, I.E. 1986. The nutritional significance of naturally occurring toxins in plant foodstuffs. Pages 72-94 in J.B. Harris, ed. Natural toxins: animal, plant, and microbial. Oxford: Clarendon Press. 353 pp.
Litovitz, T.L., B.F. Schmitz and K.M. Bailey. 1990. 1989 Annual report of the American Association of Poison Control Centers National Data Collection System. Am. J. Emergency Med. 8 : 394-442.
Lotti, M. 1992. The pathogenesis of organophosphate polyneuropathy. Crit. Rev. Toxicol. 21: 465-487.
McDuffie, H.H. 1994. Women at work: agriculture and pesticides. J. Occup. Med. 36: 1240-1246.
Minyard, J.P. and W.E. Roberts. 1991. A state data resource on toxic chemicals in foods. Pages 151-161 in B.G. Tweedy, H.J. Dishburger, L.G. Ballantine, and J. McCarthy, eds. Pesticide Residues and Food Safety: A Harvest of Viewpoints. Washington, DC: American Chemical Society.
NAS. 1973. Toxicants occurring naturally in foods. Second edition. Washington, D.C.: National Academy Press. 624 pp.
NAS. 1989. Diet and health implications for reducing chronic diseases. Washington, D.C.: National Academy Press. 749 pp.
NAS. 1996. Carcinogens and anticarcinogens in the human diet: a comparison of naturally occurring and synthetic substances. Washington, DC: National Academy of Sciences.
Nash, L. 1993. Water quality and health. In P. Gleick, ed. Water in crisis: a guide to the world’s fresh water resources. Oxford: Oxford University Press.
Nash, E.P. 1994. What’s a life worth. New York: New York Times.
Newton, L.H. and C.K. Dillingham. 1994. Classic Cases in Environmental Ethics. Belmont: Wadsworth Publishing Co.
Oser, B.L. 1978. Natural toxicants in foods. New York St. J. Med. 78: 684-685.
Perera, F.P., D.P. Rall and I.B. Weinstein. 1991. Carcinogenesis mechanisms: the debate continues. Letters. Science 252: 903-904.
Pesatori, A.C., J.M. Sontag, J.H. Lubin, D. Consonni and A. Blair. 1994. Cohort mortality and nested case-control study of lung cancer among structural pest control workers in Florida (United States). Cancer Causes & Control 5: 310-318.
Pimentel, D. 1988. Herbivore population feeding pressure on plant hosts: feedback evolution and host conservation. Oikos 53: 289-302.
Pimentel, D. 1996. Pest management in agriculture. In D. Pimentel, ed. Techniques for Reducing Pesticides: Environmental and Economic Benefits. Chichester, England: John Wiley & Sons. In press.
Pimentel, D. and A. Greiner. 1996. Environmental and socio-economic costs of pesticide use. In D. Pimentel, ed. Techniques for Reducing Pesticides: Environmental and Economic Benefits. Chichester, England: John Wiley & Sons. In press.
Potashnik, G. and I. Yanai-Inbar. 1987. Dibromochloropropane (DBCP): an 8-year reevaluation of testicular function and reproductive performance. Fertility and Sterility 47 : 317-323.
Savage, E.P., T.J. Keefe, L.W. Mounce, R.K. Heaton, A. Lewis and P.J. Burcar. 1988. Chronic neurological seqelae of acute organophosphate pesticide poisoning. Arch. Environ. Health 43: 38-45.
Shemi, D., U.A. Sod-Moriah, M. Abraham, M. Friedlaender, G. Potashnik and J. Kaplanski. 1989. Ultrastructure of testicular cells in rats treated with dibromochloropropane DBCP. Andrologia 21: 229-236.
Strong, F.M. 1974. Toxicants occurring naturally in foods. Nutr. Rev. 32: 225-231.
Thomas, P.T. and R.V. House. 1989. Pesticide-induced modulation of immune system. Pages 94-106 in N. N. Ragsdale and R. E. Menzer, eds. Carcinogenicity and Pesticides: Principles, Issues, and Relationships. Washington, DC: Am. Chem. Soc., ACS Symp. Ser. 414.
Trotter, W.J. and R. Dickerson. 1993. Pesticide residues in composited milk collected through the U.S. pasteurized milk network. J. AOAC Intl. 76: 1220-1225.
USBC. 1994. Statistical Abstract of the United States 1994. Washington, DC: U.S. Bureau of the Census, U.S. Government Printing Office.
USBC. 1995. Statistical Abstract of the United States 1995. Washington, DC: U.S. Bureau of the Census, U.S. Government Printing Office.
Watson, D.H. 1987. Pages 9-10 in D.H. Watson, ed. Natural toxicants in food: progress and prospects. Chichester, England: Ellis Horwood Ltd. 254 pp.
Weinstein, I.B. 1991. Mitogenesis is only one factor in carcinogenesis. Science 251: 387-388.
WHO. 1992. Our planet, our health: Report of the WHO commission on health and environment. Geneva: World Health Organization.
WHO/UNEP. 1989. Public Health Impact of Pesticides Used in Agriculture. Geneva: World Health Organization/United Nations Environment Programme.
Wigle, D.T., R.M. Samenciw, K. Wilkins, D. Riedel, L. Ritter, H.I. Morrison and Y. Mao. 1990. Mortality study of Canadian male farm operators: non-Hodgkin’s lymphoma mortality and agricultural practices in Saskatchewan. J. Nat. Canc. Inst. 82: 575-582.
Wiles, R. and C. Campbell. 1994. Washed, Peeled–Contaminated: Pesticide Residues in Ready-To-Eat Fruits and Vegetables. Washington, D.C.: Environmental Working Group.
WRI/UNEP/UNDP. 1994. World Resources: 1994-1995. Oxford: Oxford University Press.
Zahm, S.H., D.D. Weisenburger, P.A. Babbitt, R.C. Saal, J.B. Vaught, K.P. Cantor and A. Blair. 1990. A case-control study of non-Hodgkin’s lymphoma and the herbicide 2,4-dichlorophenoxyacetic acid (2,4-D) in Eastern Nebraska. Epidemiology 1: 349-356.