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OCCUPATIONAL AND ENVIRONMENTAL RISK FACTORS FOR CHRONIC LYMPHOCYTIC LEUKEMIA AND NON-HODGKIN’S LYMPHOMA A BLAIR, SH ZAHM, KP CANTOR, AND MH WARD INTRODUCTION
    Chronic lymphocytic leukemia (CLL) and non-Hodgkin's lymphoma (NHL) are two lymphatic and hematopoietic cancers that are sometimes combined into a single diagnostic category because they are considered as closely-related entities (Cartwright et al., 1987; Weisenburger et al., 1990). Since, they are both largely, B-cell malignancies, considering them together may provide etiologic clues. In this paper we provide a general overview of the known and suspected causes of CLL and NHL. The purpose is not to provide exhaustive documentation of the literature on each suspected factor, but to suggest leads for future research.
TIME TRENDS
    Incidence and mortality rates for non-Hodgkin's lymphoma (NHL) have been increasing for the past 40 years (Devesa and Fears, 1992). The rising rates for NHL have occurred for all histologic types, among men and women, among blacks and whites, and for all ages except the very young. The rates are rising faster in rural than in urban areas. No clear explanation exists for the rapid changes. Although HIV-related NHL explains much of the sharp increase since the mid 1980s, it cannot account for the underlying upward trend that began two decades earlier (Levine et al., 1992). The steadily rising rates for NHL over the past several decades point to a role for environmental factors. Rates for chronic lymphocytic leukemia (CLL), on the other hand, has been decreasing (Ries et al., 1994).
RISK FACTORS
    The etiology of CLL and NHL is poorly understood (Cartwright et al., 1987). There are few well-established risk factors and many of those linked to other cancers are not strongly associated with CLL or NHL. Although few factors have been clearly identified as etiologic agents for NHL and CLL, there is no shortage of hypotheses. These include a large number of occupational and general environmental exposures (Pearce, 1992), as well as viruses (Mueller NE et al., 1992), and medical conditions and therapeutic drugs (Bernstein and Ross, 1992).
Immunosuppressive Conditions
    The relative risk of NHL among immuno-suppressed patients with kidney transplants is increased over 40-fold. For NHL, therapeutically-induced or naturally-occurring immune system disorders are one of the few clearly established risk factors (Hoover and Fraumeni, 1973; Kinlen, 1992).
Tobacco and Radiation
    Cigarette smoking may be weakly associated with CLL (Brown, 1992b), but there is little evidence that it causes NHL (Brown et al., 1992a; Zahm et al., in press). Radiation, another strong risk factor for many cancers, does not appear to have much of an effect on the development of NHL and CLL (Boice, 1992).
Diet
    Few studies have been conducted to evaluate the role of diet in the development of CLL and NHL. A link with high fat and animal protein intake has been suggested in some studies (Davis, 1992). A geographic correlation study suggested that lymphoid leukemia was associated with total caloric intake (Hursting et al., 1993). A recent cohort investigation has linked red meat intake with NHL (Chiu et al., 1996). Consumption of fruits and vegetables has been associated with a reduced risk (Ward et al., 1995).
Family History
    One area where CLL and NHL resemble other cancers is family history. The risk of both cancers is approximately doubled from having a first degree relative with lymphatic or hematopoietic cancer (Pottern et al., 1991; Zahm et al., 1993; Linet, 1989).
Occupations and Industries
    Several occupations and industries have been linked with high rates for NHL and occasionally with CLL. Both cancers appear to be elevated among farmers (Blair et al., 1992; Brown et al., 1990). These excesses have been observed in many developed countries, but information from developing countries is largely absent. Although farmers may come into contact with a number of potentially carcinogenic factors, ie, pesticides, fuels and oils, engine exhausts, solvents, mycotoxins, zoonotic microbes and dusts, epidemiologic studies have focused largely on pesticides (Brown et al., 1990; Cantor et al., 1992; Zahm et al., 1990). Animal viruses have been hypothesized as possible risk factors, but the evidence is weak (Pearce and Bethwaite, 1992). Veterinarians, who have considerable contact with sick animals, have excesses of leukemia (Blair and Hayes, 1982) and slaughter house workers have had high rates of NHL (Pearce and Bethwaite, 1992). There is no evidence, however, that viruses causing these tumors in animals can infect humans (Blair et al., 1992).

    A number of investigations have reported elevated rates of NHL in various industrial occupations without focusing on particular exposures. These include links with the food processing industry (La Vecchia et al., 1989), rubber and plastics industry (Schumacher and Delzell, 1988; Downs et al., 1987), road transport workers (Balarajan, 1983), plumbers (Cantor et al., 1986), printing workers (Greene et al., 1979), foundry workers (Giles et al., 1984), chemists (Li et al., 1969; Olin, 1978), carpenters and cabinetmakers (Persson et al., 1989) and funeral directors and embalmers (Linos et al., 1989; Blair et al., 1990). In case-control studies, several metal working occupations were associated with elevated rates for NHL (Blair et al., 1993; La Vecchia et al., 1989), while another found high rates among various construction trades (Scherr et al., 1992).
Occupational Exposures
    Recent investigations have evaluated risks from specific chemicals. Studies focusing on the herbicide 2,4-D have found linked rising risks of NHL with frequency of exposure (Hoar et al., 1986; Zahm et al., 1990) or amount of herbicide used (Wigle et al., 1990). Leukemia and NHL have also been associated with a number of other agricultural pesticides (Brown et al., 1990; Zahm et al., 1990; Cantor et al., 1992). These linkages do not appear to be restricted to any particular chemical class and have been observed with carbaryl, DDT, lindane, chlordane, coumaphos, dichlorvos, malathion, and nicotine. Although the association with 2,4-D has been studied more intensely, further investigation of other pesticides is clearly needed.

    Fuels were associated with NHL in a Canadian study which observed an exposure-response relationship with amount of fuel purchased on the farm (Wigle et al., 1990). In a case-control study of NHL in the United States, oils and greases were associated with follicular NHL (Blair et al., 1993).

    Studies of workers exposed to butadiene have noted excesses of leukemia, and to a lesser extent NHL. The leukemia excesses appear to be stronger for myeloid leukemias than lymphatic leukemias (Blair and Kazerouni, in press). Very high rates of leukemia were reported in small cohorts of workers from Sweden exposed to ethylene oxide (IARC, 1994). Although IARC classifies this chemical as a human carcinogen, recent epidemiologic studies have found only a small risk for lymphatic and hematopoietic cancer (Blair and Kazerouni, in press).

    Several studies have linked various organic solvents with leukemia and NHL. Benzene is a classic leukemogen, but primarily for myeloid subtypes (IARC, 1987). A case-control study of NHL, however, found non-significant excesses of both follicular and diffuse NHL among benzene-exposed workers (Blair et al., 1993) and a large cohort study in China found NHL to be associated with exposure to this solvent (Yin et al., 1996). Solvents other than benzene have also sometimes been linked with CLL and/or NHL in studies of dry cleaners exposed to perchloroethylene and petroleum solvents (Blair et al., 1990) and mixtures of solvents and other hydrocarbons in the rubber industry (Wilcosky T et al., 1984), aircraft maintenance workers (Spirtas et al., 1991), and other occupations (Persson et al., 1989; Olsson and Brandt, 1988; Malone et al., 1989; Cartwright et al., 1988; Persson et al., 1989; La Vecchia et al., 1989).
General Environmental Exposures
    The general population is increasingly exposed to chemicals that have been studied primarily in workplace settings. There are growing opportunities for non-occupational exposure to many of these substances from environmental pollution by an occupation/industrial source or from direct use in and around the home. For example, pesticides, that were once used primarily in agriculture, are increasingly used in homes and on lawns and gardens. Solvents, although widely used in industry, have also been used in many common household products including glues, waxes, cleaning fluids, and propellants. Non-occupational exposure may also occur because many industrial chemicals spread from the workplace to the general environment due to incomplete control. In addition, many products can spread into the environment and those resistant to degradation can bioaccumulate. Organohalides, ie, DDT, chlordane, dieldrin, PCB, and PBB, are examples of chemicals that, although they had targeted uses, are now widely dispersed in the environment and can be found in the body tissues of most organisms, including humans. Finally, non-occupational exposures may occur among dependents of workers from chemicals inadvertently brought home from the workplace. For example, leukemia and NHL among children have been associated with parental use of pesticides and other hydrocarbons at work (Zahm and Devesa, 1995).

    Nitrate of agricultural origin is also spreading to the non-occupational environment. There is a growing problem of nitrate contamination of ground water in states with intensive agriculture. Nitrate may be a cancer risk factor because about 5% of ingested nitrate is reduced to nitrite, which can combine with secondary amines and amides to form N-nitroso compounds, most of which are potent animal carcinogens. Evidence for the relationship between endogenous nitrosation and nitrate intake comes from a study of rural men in Nebraska, which showed that men drinking water with high nitrate levels had an eight-fold increased risk of endogenous formation of N-nitrosoproline (Mirvish et al., 1992). An ecologic study of cancer mortality in China measured urinary levels of nitrate and N-nitrosoamino-acids such as nitrosoproline (NPRO) as an indication of exposure to N-nitroso compounds and found a positive correlation between urinary levels of some N-nitrosaminoacids and nitrate and leukemia mortality rates (Wu et al., 1993). These studies suggest that nitrate may play a role in the development of lymphatic and hematopoietic cancers possibly through its role in N-nitroso compound formation. Rates of NHL were correlated with geographic patterns of nitrate use in Nebraska (Weisenburger, 1991) and a recent case-control study in that state found an increased risk of NHL with higher nitrate levels in community drinking water supplies (Ward et al., in press), raising concern about nitrate contamination of drinking water sources.

    Several studies have evaluated other drinking water contaminants and risk of lymphatic or hematopoietic cancer. An ecologic study of leukemia in New Jersey (Fagliano et al., 1990) found a correlation between leukemia incidence rates among females and the level of volatile organic compounds (trichloroethylene and related solvents) in public water supplies. A high incidence
of leukemia was observed among children exposed in utero to private wells contaminated with solvents including trichloroethylene and perchloroethylene (Lagakos et al., 1986) and exposure was also linked to immunologic abnormalities in family members of the affected children (Byers et al., 1988). A population-based case-control study in Massachusetts found an elevated risk of leukemia with exposure to tetrachloroethylene-contaminated drinking water (Aschengrau et al., 1993). Exposure from plastic pipe linings was estimated using a model which accounted for residential history and duration, characteristics of the distribution system and pipe age and dimensions. Drinking water mutagenicity due to chlorination by-products was associated with a slightly elevated incidence of lymphoma in a study in Finland (Koivusalo et al., 1995).

    Two studies have evaluated the risk of leukemia and NHL in relation to proximity to industrial facilities (Linos et al., 1991; Shore et al., 1993). These were relatively unsophisticated approaches, which despite weaknesses in exposure assessment (a simple distance measure was used), found that residential proximity to certain industrial operations increased the risk of leukemia and NHL. Cancer risks tended to increase as the distance from the facility decreased.
Hair Dyes
    Several recent studies have linked leukemia and NHL to personal use of hair dyes (Cantor et al., 1988; Zahm et al., 1992; Thun et al., 1994). The risk was associated with semi-permanent and permanent dyes and was larger from dark than for lighter shades. The active ingredients of the dyes belong to a class of chemicals that are established carcinogens.
SUMMARY AND RECOMMENDATIONS
    The clear and strong impact of immunosuppressive therapeutic and acquired disorders (Kinlen, 1992) offers a mechanistic focus for studying CLL and NHL. This is not to imply that all risk factors must necessarily operate through the immune system, but this view may help direct research into profitable areas. For example, a number of pesticides affect the immune system (Thomas et al., 1990) and the excess of leukemia and NHL among farmers (along with other tumors that may be influenced by immune system aberrations) suggests that analytic studies of this group of chemicals could be informative. There appear to be a number of lifestyle, occupational, and environmental factors that might be related to the development of CLL and NHL. Most associations are far from conclusive and studies that show no association maybe found for most factors discussed. These associations, therefore, should be considered as leads, not as proven risk factors.
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