4
Epidemiology

In the tradition of previous Veterans and Agent Orange (VAO) reports, this chapter summarizes certain epidemiology studies considered in the ongoing effort to evaluate and integrate all study results on human subjects pertinent to health effects that might result from exposure to any of the chemicals of interest (2,4-dichlorophenoxyacetic acid [2,4-D]; 2,4,5-trichlorophenoxyacetic acid [2,4,5-T] and its contaminant 2,3,7,8-tetrachlorodibenzo-p-dioxin [TCDD]; 4-amino-3,5,6-trichloropicolinic acid [picloram]; and cacodylic acid [dimenthylarsenic acid]). Primary emphasis is put on describing work new to this review contained in publications appearing since Veterans and Agent Orange: Update 2002 (hereafter, Update 2002) (IOM, 2003).

The framework adopted in this chapter provides a means of organizing the thousands of citations considered over the successive updates. The organization into occupational studies, environmental studies, and studies of Vietnam veterans, which is carried over into the discussions and results tables in the health outcomes chapters, is not intended to imply that any of these populations is intrinsically more valuable for the committee’s purpose. Each study design has strengths and weaknesses (see Chapter 2) influencing its potential to contribute evidence of an association with the health outcomes considered in Chapters 69 of this report. Critical commentary has been reserved for the individual health outcome chapters and is not included in this chapter. The associated cumulative tables in Appendix A include the basic type of study design; criteria for sample selection; the numbers of subjects and comparison populations; how data were collected; and how exposure was determined.

The major purpose of Chapter 4 is to reduce repetition of design information



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Veterans and Agent Orange: Update 2004 4 Epidemiology In the tradition of previous Veterans and Agent Orange (VAO) reports, this chapter summarizes certain epidemiology studies considered in the ongoing effort to evaluate and integrate all study results on human subjects pertinent to health effects that might result from exposure to any of the chemicals of interest (2,4-dichlorophenoxyacetic acid [2,4-D]; 2,4,5-trichlorophenoxyacetic acid [2,4,5-T] and its contaminant 2,3,7,8-tetrachlorodibenzo-p-dioxin [TCDD]; 4-amino-3,5,6-trichloropicolinic acid [picloram]; and cacodylic acid [dimenthylarsenic acid]). Primary emphasis is put on describing work new to this review contained in publications appearing since Veterans and Agent Orange: Update 2002 (hereafter, Update 2002) (IOM, 2003). The framework adopted in this chapter provides a means of organizing the thousands of citations considered over the successive updates. The organization into occupational studies, environmental studies, and studies of Vietnam veterans, which is carried over into the discussions and results tables in the health outcomes chapters, is not intended to imply that any of these populations is intrinsically more valuable for the committee’s purpose. Each study design has strengths and weaknesses (see Chapter 2) influencing its potential to contribute evidence of an association with the health outcomes considered in Chapters 6–9 of this report. Critical commentary has been reserved for the individual health outcome chapters and is not included in this chapter. The associated cumulative tables in Appendix A include the basic type of study design; criteria for sample selection; the numbers of subjects and comparison populations; how data were collected; and how exposure was determined. The major purpose of Chapter 4 is to reduce repetition of design information

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Veterans and Agent Orange: Update 2004 in the health outcomes chapters from endpoint to endpoint, and also from update to update. Of particular importance to the VAO project are a number of continuing studies of populations that have been exposed to the herbicides sprayed in Vietnam or to their components. It is essential that laboriously amassed information on a single population be recognized as such. Placing each new publication in historical context helps the committee avoid factoring what is actually a single observation into their deliberations repeatedly. Such studies are extremely important in describing the time course of a population’s response to an exposure. Furthermore, joint consideration of an entire body of research on a population may permit more insightful evaluation of relationships with potential confounding factors. This chapter augments the existing information on these study populations with descriptions of any new publications investigating any of their members, explaining how the new work meshes with earlier efforts. Many studies, particularly cancer cohort studies, report on multiple health endpoints. The weight appropriately attributed to a study’s findings is determined in the context of its design and execution. Because repetition of this information in the health outcomes chapters for every specific endpoint report would be cumbersome and tedious, discussions of design and evaluation comments for these studies are presented in this chapter and distilled in the design tables in Appendix A. Of course, a multi-endpoint study might also qualify for inclusion in this chapter because it addresses a previously studied population. Studies new to this update that report on a single endpoint and were conducted on a population that has not been studied by others are not included in this chapter. Their designs characteristics are present in the one place where their results are reported in one of the chapters on health outcomes. The chapter is organized into three major sections—occupational studies, environmental studies, and studies of Vietnam veterans. Detailed descriptions of many of the study populations can be found in Chapter 2 of the original report of this committee, Veterans and Agent Orange: Health Effects of Herbicides Used in Vietnam (hereafter referred to as VAO; IOM, 1994), and the criteria for inclusion in the review are discussed in Appendix A of that report. In addition to a review of studies that involved exposures to the chemicals of interest (2,4-D; 2,4,5-T and its contaminant TCDD; cacodylic acid; and picloram), the committee also examined some studies that addressed compounds chemically related to the herbicides used in Vietnam, such as 2-methyl-4-chlorophenoxyacetic acid, hexachlorophene, and chlorophenols, including trichlorophenol. In some published reports, the study investigators did not indicate the specific herbicides to which study participants were exposed or the magnitude of exposure; those complicating factors were considered when the committee weighed the relevance of a study. Available details of exposure assessment and use of exposure in analyses are discussed in Chapter 5. The occupational section covers studies of production workers, agriculture and forestry workers (including herbicide and pesticide appliers), and paper and

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Veterans and Agent Orange: Update 2004 pulp workers. The environmental section covers studies of populations unintentionally exposed to unusually high concentrations of herbicides or dioxins as a result of where they live, such as Seveso, Italy; Times Beach, Missouri; and the southern portion of Vietnam. The section on Vietnam veterans covers studies conducted in the United States by the Air Force, the Centers for Disease Control and Prevention (CDC), the Department of Veterans Affairs (VA), the American Legion, and the state of Michigan; it also discusses studies of Australian and Korean Vietnam veterans. Many cohorts potentially exposed to any of the chemicals of interest are monitored periodically, typically every 3–5 years. Those groups include the cohorts of the National Institute for Occupational Safety and Health (NIOSH), the International Agency for Research on Cancer (IARC), the National Cancer Institute (NCI), residents of Seveso, and Ranch Hand personnel. For the sake of thoroughness, the discussions of specific health outcomes in Chapters 6–9 include references to studies discussed in previous Agent Orange reports and to new studies. However, in making its conclusions, the committee focused on the most recent update when multiple reports on the same cohorts and endpoints were available. Individual researchers who are a part of research consortia evaluating cohorts in large multicenter studies (such as the IARC and NCI cohort studies) sometimes publish reports based solely on the subset of subjects they themselves are monitoring. All of the studies are discussed in this report, but when making its conclusions, the committee focused on the studies of the larger, multicenter cohorts. OCCUPATIONAL STUDIES Several occupational groups in the United States and elsewhere have been exposed to the compounds of interest. Exposure characterization varies widely in the exposure metric used; the extent of detail; confounding by other exposures; and whether individual, surrogate, or group (ecologic) measures are used. Some studies use job titles as broad surrogates of exposure, others rely on disease registry data. Occupational groups include workers in chemical production plants; agriculture and forestry workers, including farmers and herbicide appliers; and workers in paper and pulp manufacturing. Production Workers National Institute for Occupational Safety and Health Starting in 1978, NIOSH began a study to identify all US workers who might have been exposed to TCDD between 1942 and 1984 (Fingerhut et al., 1991).

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Veterans and Agent Orange: Update 2004 From a total of 12 companies, 5,132 workers were identified from personnel and payroll records as having been involved in production or maintenance processes associated with TCDD contamination. Their possible exposure resulted from working with substances for which TCDD was a contaminant: 2,4,5-trichlorophenol (TCP); 2,4,5-T, Silvex®; Erbon®; Ronnel®; and hexachlorophene. Another 172 workers identified previously by their employers as being exposed to TCDD also were included in the study cohort. The 12 plants involved were large manufacturing sites of major chemical companies, so many of the subjects were potentially exposed to many other compounds, some of which could be toxic and carcinogenic. Before the publication of the first study of the main cohort, NIOSH conducted a cross-sectional study that included a comprehensive medical history, medical examination, and measurement of pulmonary function of workers employed in chemical manufacturing at a plant in Newark, New Jersey, between 1951 and 1969, and at a plant in Verona, Missouri, between 1968 and 1969 and 1970 and 1972. Control subjects were recruited from surrounding neighborhoods (Alderfer et al., 1992; Calvert et al., 1991, 1992; Sweeney et al., 1989, 1993). The New Jersey plant manufactured TCP and 2,4,5-T; the Missouri plant manufactured TCP, 2,4,5-T, and hexachlorophene. Later studies examined specific health outcomes among the cohort, including pulmonary function (Calvert et al., 1991), liver and gastrointestinal function (Calvert et al., 1992), mood (Alderfer et al., 1992), effects on the peripheral nervous system (Sweeney et al., 1993), porphyria cutanea tarda (Calvert et al., 1994), and effects on reproductive hormones (Egeland et al., 1994). Sweeney et al. (1996, 1997/1998) evaluated non-cancer endpoints, including liver function, gastrointestinal disorders, chloracne, serum glucose concentration, hormone and lipid concentrations, and diabetes in a subgroup of the original cohort studied by Calvert et al. (1991). More recent studies of the main cohort examined cardiovascular effects (Calvert et al., 1998); diabetes mellitus, thyroid function, and endocrine function (Calvert et al., 1999); immune characteristics (Halperin et al., 1998); and cancer incidence (Kayajanian, 2002). Cross-sectional medical surveys reported serum TCDD concentrations and surrogates of cytochrome P450 induction (Halperin et al., 1995) in that cohort. A follow-up study (Steenland et al., 1999) examined the association between TCDD exposure and cause of death; it examined specific health outcomes, including cancer (all and site-specific), respiratory disease, cardiovascular disease, and diabetes. Steenland et al. (2001) published a paper that reanalyzed data from two studies on TCDD and diabetes mellitus: one in US workers (the NIOSH cohort; Calvert et al., 1999) and one in veterans of Operation Ranch Hand in which the herbicides were sprayed from planes in Vietnam (Henriksen et al., 1997). VAO, Veterans and Agent Orange: Update 1996 (hereafter, Update 1996 [IOM, 1996]), Update 1998 (IOM, 1999), Update 2000 (IOM, 2001), and Update 2002 (IOM, 2003), describe the details of those studies.

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Veterans and Agent Orange: Update 2004 Bodner et al. (2003) compared the mortality in Dow Chemical Company workers with mortality among the NIOSH and IARC cohorts. Study details are in the Dow Chemical Company section of this chapter. Monsanto The NIOSH study cohort (Fingerhut et al., 1991) included employees of Monsanto’s production facilities. One set of studies was based on an unintentional release that occurred on March 8, 1949, in the TCP production process at the Monsanto plant in Nitro, West Virginia (Collins et al., 1993; Moses et al., 1984; Zack and Suskind, 1980). Others focused on exposure of workers involved in numerous aspects of 2,4,5-T production (Moses et al., 1984; Suskind and Hertzberg, 1984; Zack and Gaffey, 1983). The Monsanto studies are discussed in more detail in VAO. No new studies have been published on those subjects. Dow Chemical Company Several studies of Dow Chemical Company production workers are summarized in VAO, Update 1996, Update 1998, and Update 2002. The populations of many of those studies were included in the NIOSH cohort (Fingerhut et al., 1991). Originally, Dow conducted a study of workers engaged in the production of 2,4,5-T (Ott et al., 1980) and one on TCP-manufacturing workers with chloracne (Cook et al., 1980). Extension and follow-up studies compared potential exposure to TCDD with medical examination frequency and morbidity (Bond et al., 1983) and with reproductive outcomes after potential paternal TCDD exposure (Townsend et al., 1982). A prospective mortality study of Dow employees diagnosed with chloracne or classified as having chloracne on the basis of clinical description (Bond et al., 1987) and a large-scale cohort mortality study of workers exposed to herbicides in several of its plants (Bloemen et al., 1993; Bond et al., 1988; Burns et al., 2001; Ramlow et al., 1996) also were conducted. Dow assembled a large cohort at the Midland, Michigan, plant (Bond et al., 1989a; Cook et al., 1986, 1987). Exposure to TCDD was characterized in that cohort on the basis of chloracne diagnosis (Bond et al., 1989b). Within that cohort, a cohort study of women (Ott et al., 1987) and a case–control study of soft-tissue sarcoma (STS) (Sobel et al., 1987) were conducted. Since Update 2002, Bodner et al. (2003) have published a 10-year follow-up of the work of Cook et al. (1986), comparing the mortality experience of 2,187 male Dow Chemical Company workers potentially exposed to large amounts of dioxin before 1983 with that of the NIOSH and IARC cohorts. Worker exposures were determined by combining detailed work histories with an analysis of historical plant operations and industrial hygiene monitoring. All of the workers in the analysis are male; 5 female workers were excluded from the analysis. Diagnosis of chloracne resulting from high exposure incidence corroborated many of the

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Veterans and Agent Orange: Update 2004 exposures. The IARC international study and the NIOSH Dioxin Registry include most of the Dow workers; Dow workers make up the largest component of those two cohorts. A modified life table program was used to calculate standardized mortality ratio and 95% confidence intervals relative to the US male population. A pool of local workers with no previous work history in the targeted departments and no known dioxin exposures served as the reference population. Internal analyses were stratified by age, calendar year, and hourly salary status. BASF In Germany, an accident on November 17, 1953, during the manufacture of TCP at BASF Aktiengesellschaft resulted in the exposure of some workers in the plant predominantly to TCDD. VAO, Update 1996, Update 1998, and Update 2000 summarized studies on those workers, including a mortality study of persons initially exposed or later involved in cleanup (Thiess et al., 1982), an update and expansion of that study (Zober et al., 1990), and a morbidity follow-up (Zober et al., 1994). In addition, Ott and Zober (1996) examined cancer incidence and mortality in another cohort of workers exposed to TCDD after the accident during reactor cleanup, maintenance, or demolition. No new studies have been published on those cohorts since Update 2000. International Agency for Research on Cancer To avoid problems of small studies with insufficient power to detect increased cancer risks, IARC created a multinational registry of workers exposed to phenoxy herbicides, chlorophenols, and their contaminants (Saracci et al., 1991). The registry includes information on mortality and exposure of 18,390 workers—16,863 men and 1,527 women. Update 1996 described the individual national cohorts included in the registry. One study of people from 10 countries evaluated cancer mortality from STS and malignant lymphoma (Kogevinas et al., 1992). Two nested case–control studies were undertaken using the IARC cohort to evaluate the relationship between STS and non-Hodgkin’s lymphoma (NHL) (Kogevinas et al., 1995). In an update and expansion, Kogevinas et al. (1997) assembled national studies from 12 countries that used the same protocol (jointly developed by study participants and coordinated by IARC) to study cancer mortality. Vena et al. (1998) studied non-neoplastic mortality in the IARC cohorts. A cohort study of cancer incidence and mortality was conducted among 701 women from 7 countries who were occupationally exposed to chlorophenoxy herbicides, chlorophenols, and dioxins (Kogevinas et al., 1993). VAO, Update 1996, Update 1998, and Update 2000 highlight those studies. Several of the smaller cohorts that make up the IARC cohort have been evaluated apart from the IARC-coordinated efforts. They include Danish produc-

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Veterans and Agent Orange: Update 2004 tion workers (Lynge, 1985, 1993); British production workers (Coggon et al., 1986, 1991); Dutch production workers (Bueno de Mesquita et al., 1993); German production workers (Becher et al., 1996; Flesch-Janys, 1997; Flesch-Janys et al., 1995; Manz et al., 1991); factory workers from the Netherlands (Hooiveld et al., 1998); and Austrian production workers (Jäger et al., 1998; Neuberger et al., 1998, 1999). VAO, Update 1996, Update 1998, and Update 2000 discuss those studies in more detail. No new studies have been published on the IARC cohort or on the smaller constituent cohorts. Since Update 2002, Bodner et al. (2003) published a study comparing the mortality experience of Dow Chemical Company workers with that of the NIOSH and IARC cohorts. Study details can be found in this chapter under the heading Dow Chemical Company. Other Chemical Plants Studies have reviewed health outcomes among UK chemical workers exposed to TCDD as a result of an industrial accident in 1968 (Jennings et al., 1988; May, 1982, 1983); 2,4-D production workers in the former Soviet Union (Bashirov, 1969); factory workers in Prague who exhibited symptoms of TCDD toxicity 10 years after occupational exposure to 2,4,5-T (Pazderova-Vejlupkova et al., 1981); 2,4-D and 2,4,5-T production workers in the United States (Poland et al., 1971); white men employed at a US chemical plant manufacturing flavors and fragrances (Thomas, 1987); and US chemical workers engaged in the production of pentachlorophenol, lower-chlorinated phenols, and esters of chlorophenoxy acids (Hryhorczuk et al., 1998). The long-term immune-system effects of TCDD were examined in 11 industrial workers involved in production and maintenance operations at a German chemical factory producing 2,4,5-T (Tonn et al., 1996), and immune effects were studied in a cohort of workers formerly employed at a German pesticide-producing plant (Jung et al., 1998). VAO, Update 1998, and Update 2000 detail those studies. No studies at other chemical plants have been published since Update 2000. Agriculture and Forestry Workers Cohort Studies Agriculture VAO, Update 1996, Update 1998, Update 2000, and Update 2002 detailed cohort studies that examined health outcomes in people involved in agriculture. They include studies of proportionate mortality among Iowa farmers (Burmeister, 1981) and among male and female farmers in 23 states (Blair et al., 1993); cancer mortality among Danish and Italian farmers (Ronco et al., 1992) and among a cohort of rice growers in the Novara Province of northern Italy (Gambini et al., 1997); cancer incidence among farmers licensed to spray pesti-

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Veterans and Agent Orange: Update 2004 cides in Italy’s southern Piedmont (Corrao et al., 1989) and among female gardeners in Denmark (Hansen et al., 1992); sperm abnormalities among Argentinian farmers (Lerda and Rizzi, 1991); cancer and birth defects among the offspring of Norwegian farmers (Kristensen et al., 1997); pregnancy outcomes in couples living on family farms in Ontario, Canada (Arbuckle et al., 1999, 2001; Curtis et al., 1999; Savitz et al., 1997); and immune, neurobehavioral, and lung function of residents from an agricultural area of Saskatchewan, Canada, and immunologic changes in 10 farmers who mixed and applied commercial formulations that contained the chlorophenoxy herbicides (Faustini et al., 1996). The Mortality Study of Canadian Male Farm Operators evaluated the risk to farmers of death and specific health outcomes: NHL (Morrison et al., 1994; Wigle et al., 1990), prostatic cancer (Morrison et al., 1992), brain cancer (Morrison et al., 1993), multiple myeloma (Semenciw et al., 1993), leukemia (Semenciw et al., 1994), and asthma (Senthilselvan et al., 1992). Data from the Swedish Cancer Environment Register (which links population census data, including occupation, with the Swedish Cancer Registry) were used in cohort studies that evaluated cancer mortality and farm work (Wiklund, 1983); STS and malignant lymphoma among agricultural and forestry workers (Wiklund and Holm, 1986; Wiklund et al., 1988a); and the risk of NHL, Hodgkin’s disease (HD); and multiple myeloma in relation to occupational activities (Eriksson et al., 1992). Brain, lymphatic, and hematopoietic cancers in Irish agricultural workers also have been studied (Dean, 1994). No new studies of agricultural workers have been published since Update 2002. Forestry Studies have been conducted among forestry workers potentially exposed to the types of herbicides used in Vietnam. A cohort mortality study examined men employed at a Canadian public utility (Green, 1987, 1991), a Dutch study of forestry workers exposed to 2,4,5-T investigated the prevalence of acne and liver dysfunction (van Houdt et al., 1983), and another study examined mortality and cancer incidence in a cohort of Swedish lumberjacks (Thörn et al., 2000). No new studies of forestry workers have been published since Update 2002. Herbicide and Pesticide Application Several cohort studies have assessed health outcomes among herbicide and pesticide appliers: cancer mortality among Swedish railroad workers (Axelson and Sundell, 1974; Axelson et al., 1980), mortality among pesticide appliers in Florida (Blair et al., 1983), general and cancer mortality and morbidity measured prospectively among Finnish male 2,4-D and 2,4,5-T appliers (Asp et al., 1994; Riihimaki et al., 1982, 1983), reproductive outcomes among male chemical appliers in New Zealand (Smith et al., 1981, 1982), and doctor visits resulting from pesticide exposure (Alavanja et al., 1998) and chemical predictors of wheeze (Hoppin et al., 2002) in Iowa and North Carolina. Other studies examined the risk of cancer—including STS, HD, NHL,

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Veterans and Agent Orange: Update 2004 and prostate cancer—among pesticide and herbicide appliers in Sweden (Dich and Wiklund, 1998; Wiklund et al., 1987, 1988b, 1989a,b), general and cancer mortality among Dutch male herbicide appliers (Swaen et al., 1992), cancer mortality among Minnesota highway maintenance workers (Bender et al., 1989) and Minnesota pesticide appliers (Garry et al., 1994, 1996a,b), lung cancer morbidity in male agricultural plant protection workers in the former German Democratic Republic who spent a portion of their work year applying pesticides (Barthel, 1981), British Columbia sawmill workers potentially exposed to chlorophenate wood preservatives used as a fungicide during spraying and dipping of sawed logs and planed boards (Dimich-Ward et al., 1996; Heacock et al. 1998; Hertzman et al., 1997), and cancer risk among pesticide users in Iceland (Zhong and Rafnsson, 1996). Some of those studies included agriculture and forestry worker cohorts; details of the studies, designs, and results are included in VAO, Update 1996, Update 1998, Update 2000, and Update 2002. Since Update 2002, Alavanja et al. (2003) examined the correlation between exposure to agricultural pesticides, including 2,4-D and 2,4,5-T and prostate cancer incidence among pesticide appliers in Iowa and North Carolina in the Agricultural Health Study. The study cohort consisted of 55,332 male commercial and private pesticide appliers who completed a self-administered enrollment questionnaire between December 1993 and 1997, and who had no history of prostate cancer. The enrollment questionnaire sought information on a variety of issues: pesticide exposures, uses, and practices; dietary and cooking practices; personal medical history; and tobacco and alcohol use. A subset of 24,034 appliers also completed a take-home questionnaire that sought more specific information on similar topics. Members of the cohort were matched to Iowa and North Carolina cancer registry files, and to state and national death registries for vital statistics. Standardized incidence for prostate cancer was computed. Researchers used multivariate and unconditional logistic regression and factor analysis to evaluate and interpret the data. Flower et al. (2004) examined the correlation between parental pesticide exposure and cancer risk in the children of pesticide appliers in the AHS cohort. That group consisted of 20,625 appliers and spouses who completed enrollment and secondary questionnaires on female and family health. Completed questionnaires identified 21,375 children born during or after 1975. Cancer cases within the group of children were identified both retrospectively and prospectively after enrollment in the study. In Iowa, 50 cases of children diagnosed with cancer between birth and 19 years of age were identified from the questionnaires and verified through cancer registries; childhood cancer cases in North Carolina were excluded from the study because too few were identified. Parental pesticide exposure data collected through the questionnaires included information on the mixing and application of pesticides and the use of protective equipment. Logistic regression was used to compute odds ratios and 95% confidence intervals.

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Veterans and Agent Orange: Update 2004 Confounders were analyzed, but were excluded from the final models when the researchers deemed them insignificant. Swaen et al. (2004) published an updated mortality study of a cohort of 1,341 licensed herbicide appliers in the Netherlands (Swaen et al., 1992), extending the follow-up by 13 years (1988–2001). They reviewed information on the types and amounts of herbicides used in all municipal spraying projects in 1980; those data could not be linked to the work of any individual appliers. Mortality, using International Classification of Disease (ICD) coding, was determined from a cause-of-death registry. SMRs were calculated based on cause-specific mortality rates from the Netherlands. Case–Control Studies In 1977, case-series reports in Sweden (Hardell, 1977, 1979) of a potential connection between STS and exposure to phenoxyacetic acids prompted several case–control investigations of a possible association (Eriksson et al., 1979, 1981, 1990; Hardell and Eriksson, 1988; Hardell and Sandstrom, 1979; Wingren et al., 1990). After the initial STS reports (Hardell, 1977, 1979), case–control studies of other cancer outcomes including HD, NHL, and other lymphomas were conducted in Sweden (Hardell and Bengtsson, 1983; Hardell et al., 1980, 1981). Also studied were HD and NHL (Persson et al., 1989, 1993); NHL (Hardell and Eriksson, 1999; Olsson and Brandt, 1988); nasal and nasopharyngeal carcinomas (Hardell et al., 1982); gastric cancer (Ekström et al., 1999); and primary or unspecified liver cancer (Hardell et al., 1984). To address criticism regarding potential observer bias in some of the case–control series, Hardell (1981) conducted another case–control study on colon cancer. Hardell et al. (1994) also examined the relationship between occupational exposure to phenoxyacetic acids and chlorophenols and various characteristics related to NHL—including histopathologic measures, stage, and anatomic location—on the basis of the NHL cases from a previous study (Hardell et al., 1981). Prompted by the Swedish studies (Hardell, 1977, 1979), a set of case–control studies in New Zealand evaluated the association between phenoxy herbicide and chlorophenol exposure and STS incidence and mortality (Smith and Pearce, 1986; Smith et al., 1983, 1984). Additional case–control studies and an expanded case series were conducted on phenoxy herbicide and chlorophenol exposure and the risks of malignant lymphoma, NHL, and multiple myeloma (Pearce et al., 1985, 1986a,b, 1987). Geographic patterns of increased leukemia mortality in white men in the central part of the United States prompted a study of the leukemia mortality in Nebraska farmers (Blair and Thomas, 1979). Additional case–control studies were later conducted on leukemia in Nebraska (Blair and White, 1985), in Iowa (Burmeister et al., 1982) on the basis of the cohort study of Burmeister (1981), in

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Veterans and Agent Orange: Update 2004 Iowa and Minnesota (Brown et al., 1990), and on leukemia associated with NHL in eastern Nebraska (Zahm et al., 1990). Case–control studies have been conducted in various US populations for other cancers, including NHL (Cantor, 1982; Cantor et al., 1992; Tatham et al., 1997; Zahm et al., 1993); multiple myeloma (Boffetta et al., 1989; Brown et al., 1993; Morris et al., 1986); cancers of the stomach, prostate, NHL, and multiple myeloma (Burmeister et al., 1983); STS, HD, and NHL (Hoar et al., 1986); NHL and HD (Dubrow et al., 1988); and STS and NHL (Woods and Polissar, 1989; Woods et al., 1987). Other studies outside the United States have examined ovarian cancer in the Piedmont region of Italy (Donna et al., 1984); brain gliomas in two hospitals in Milan, Italy (Musicco et al., 1988); STS and other cancers in the 15 regional cancer registries that constitute the National Cancer Register in England (Balarajan and Acheson, 1984); STS and malignant lymphomas in the Victorian Cancer Registry of Australia (Smith and Christophers, 1992); lymphoid cancer in Milan, Italy (LaVecchia et al., 1989); STS among rice weeders in northern Italy (Vineis et al., 1986); primary lung cancer among pesticide users in Saskatchewan (McDuffie et al., 1990); and renal-cell carcinoma in the Denmark Cancer Registry (Mellemgaard et al., 1994). Nanni et al. (1996) conducted a population-based case–control study, based on the work of Amadori et al. (1995), of occupational and chemical risk factors for lymphocytic leukemia and NHL in northeastern Italy. Non-cancer endpoints also have been investigated in case–control studies: spontaneous abortion (Carmelli et al., 1981); congenital malformations (García et al., 1998); immunosuppression and subsequent decreased host resistance to infection among AIDS patients with Kaposi’s sarcoma (Hardell et al., 1987); mortality in US Department of Agriculture extension agents (Alavanja et al., 1988, 1989); spina bifida in offspring associated with paternal occupation (Blatter et al., 1997); mortality from neurodegenerative diseases associated with occupational risk factors (Schulte et al., 1996); Parkinson’s disease (PD) associated with occupational and environmental risk factors (Liou et al., 1997); PD associated with various rural factors, including exposure to herbicides and wood preservatives (Seidler et al., 1996); PD associated with occupational risk factors (Semchuk et al., 1993); and birth defects in offspring of agriculture workers (Nurminen et al., 1994). Those studies are discussed in detail in VAO, Update 1996, and Update 1998. No new case–control studies of agriculture and forestry workers have been published since Update 2000. Paper and Pulp Workers Workers in the paper and pulp industry can be exposed to TCDD and other dioxins that can be generated by the bleaching process during the production and treatment of paper and paper products. VAO describes studies of pulp and paper

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Veterans and Agent Orange: Update 2004 Kang HK, Dalager NA, Needham LL, Patterson DG, Matanoski GM, Kanchanaraksa S, Lees PSJ. 2001. US Army chemical corps Vietnam veterans health study: preliminary results. Chemosphere 43:943–949. Kayajanian GM. 2002. The J-shaped dioxin dose response curve. Ecotoxicology and Environmental Safety 51:1–4. Ketchum NS, Michalek JE, Burton JE. 1999. Serum dioxin and cancer in veterans of Operation Ranch Hand. American Journal of Epidemiology 149(7):630–639. Khoa ND. 1983. Some biologic parameters collected on the groups of people in an area affected by chemicals. Summarized in: Constable JD, Hatch MC. Reproductive effects of herbicide exposure in Vietnam: recent studies by the Vietnamese and others. As cited in Constable and Hatch, 1985. Kim H-A, Kim E-M, Park Y-C, Yu J-Y, Hong S-K, Jeon S-H, Park K-L, Hur S-J, Heo Y. 2003. Immunotoxicological effects of Agent Orange exposure to the Vietnam War Korean veterans. Industrial Health 41:158–166. Kim J-S, Kang H-K, Lim H-S, Cheong H-K, Lim M-K. 2001. A study on the correlation between categorizations of the individual exposure levels to Agent Orange and serum dioxin levels among the Korean Vietnam veterans. Korean Journal of Preventative Medicine 34(1):80–88. Kim J-S, Lim H-S, Cho S-I, Cheong H-K, Lim M-K. 2003. Impact of Agent Orange Exposure among Korean Vietnam Veterans. Industrial Health 41:149–157. Kogan MD, Clapp RW. 1985. Mortality Among Vietnam Veterans in Massachusetts, 1972–1983. Boston: MA. Massachusetts Office of the Commissioner of Veterans Services, Agent Orange Program. Kogan MD, Clapp RW. 1988. Soft tissue sarcoma mortality among Vietnam veterans in Massachusetts, 1972–1983. International Journal of Epidemiology 17:39–43. Kogevinas M, Saracci R, Bertazzi PA, Bueno de Mesquita BH, Coggon D, Green LM, Kauppinen T, Littorin M, Lynge E, Mathews JD, Neuberger M, Osman J, Pearce N, Winkelmann R. 1992. Cancer mortality from soft-tissue sarcoma and malignant lymphomas in an international cohort of workers exposed to chlorophenoxy herbicides and chlorophenols. Chemosphere 25:1071–1076. Kogevinas M, Saracci R, Winkelmann R, Johnson ES, Bertazzi PA, Bueno de Mesquita BH, Kauppinen T, Littorin M, Lynge E, Neuberger M. 1993. Cancer incidence and mortality in women occupationally exposed to chlorophenoxy herbicides, chlorophenols, and dioxins. Cancer Causes and Control 4:547–553. Kogevinas M, Kauppinen T, Winkelmann R, Becher H, Bertazzi PA, Bas B, Coggon D, Green L, Johnson E, Littorin M, Lynge E, Marlow DA, Mathews JD, Neuberger M, Benn T, Pannett B, Pearce N, Saracci R. 1995. Soft tissue sarcoma and non-Hodgkin’s lymphoma in workers exposed to phenoxy herbicides, chlorophenols and dioxins: two nested case-control studies. Epidemiology 6:396–402. Kogevinas M, Becher H, Benn T, Bertazzi PA, Boffetta P, Bueno de Mesquita HB, Coggon D, Colin D, Flesch-Janys D, Fingerhut M, Green L, Kauppinen T, Littorin M, Lynge E, Mathews JD, Neuberger M, Pearce N, Saracci R. 1997. Cancer mortality in workers exposed to phenoxy herbicides, chlorophenols, and dioxins. An expanded and updated international cohort study. American Journal of Epidemiology 145(12):1061–1075. Kristensen P, Irgens LM, Andersen A, Bye AS, Sundheim L. 1997. Birth defects among offspring of Norwegian farmers, 1967–1991. Epidemiology 8(5):537–544. Lampi P, Hakulinen T, Luostarinen T, Pukkala E, Teppo L. 1992. Cancer incidence following chlorophenol exposure in a community in southern Finland. Archives of Environmental Health 47:167–175. Landi MT, Bertazzi PA, Baccarelli A, Consonni D, Masten S, Lucier G, Mocarelli P, Needham L, Caporaso N, Grassman J. 2003. TCDD-mediated alterations in the AhR-dependent pathway in Seveso, Italy, 20 years after the accident. Carcinogenesis 24(4):673–680.

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Veterans and Agent Orange: Update 2004 Michalek JE, Tripathi RC. 1999. Pharmacokinetics of TCDD in veterans of Operation Ranch Hand: 15-year follow-up. Journal of Toxicology and Environmental Health 57(6):369–378. Michalek JE, Wolfe WH, Miner JC. 1990. Health status of Air Force veterans occupationally exposed to herbicides in Vietnam. II. Mortality. Journal of the American Medical Association 264: 1832–1836. Michalek JE, Rahe AJ, Boyle CA. 1998a. Paternal dioxin, preterm birth, intrauterine growth retardation, and infant death. Epidemiology 9(2):161–167. Michalek JE, Ketchum NS, Akhtar FZ. 1998b. Postservice mortality of US Air Force veterans occupationally exposed to herbicides in Vietnam: 15-year follow-up. American Journal of Epidemiology 148(8):786–792. Michalek JE, Rahe AJ, Boyle CA. 1998c. Paternal dioxin and the sex of children fathered by veterans of Operation Ranch Hand (2). Epidemiology 9(4):474–475. Michalek JE, Albanese RA, Wolfe WH. 1998d. Paternal dioxin, preterm birth, intrauterine growth retardation, and infant death. Epidemiology 9(2):161–167. Michalek JE, Akhtar FZ, Kiel JL. 1999a. Serum dioxin, insulin, fasting glucose, and sex hormone-binding globulin in veterans of Operation Ranch Hand. Journal of Clinical Endocrinology and Metabolism 84(5):1540–1543. Michalek JE, Ketchum NS, Check IJ. 1999b. Serum dioxin and immunologic response in veterans of Operation Ranch Hand. American Journal of Epidemiology 149(11):1038–1046. Michalek JE, Ketchum N, Longnecker MP. 2001a. Serum dioxin and hepatic abnormalities in veterans of Operation Ranch Hand. Annals of Epidemiology 11(5):304–311. Michalek JE, Akhtar FZ, Arezzo JC, Garabrant DH, Albers JW. 2001b. Serum dioxin and peripheral neuropathy in veterans of Operation Ranch Hand. Neurotoxicology 22:479–490. Michalek JE, Akhtar FZ, Longnecker MP, Burton JE. 2001c. Relation of serum 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) level to hematological examination results in veterans of Operation Ranch Hand. Archives of Environmental Health 56(5):396–405. Michalek JE, Ketchum NS, Tripathi RC. 2003. Diabetes mellitus and 2,3,7,8-tetrachlorodibenzo-p-dioxin elimination in veterans of Operation Ranch Hand. Journal of Toxicology and Environmental Health, Part A, 66:211–221. Michigan Department of Public Health. 1983. Evaluation of Soft and Connective Tissue Cancer Mortality Rates for Midland and Other Selected Michigan Counties. Michigan Department of Public Health . Mo HJ, Park HJ, Kim JH, Lee JY, Cho BK. 2002. A study about the skin and general disease patterns of the Vietnam veterans exposed to dioxin. Korean Journal of Dermatology 40(6):634–638. Mocarelli P, Marocchi A, Brambilla P, Gerthoux P, Young DS, Mantel N. 1986. Clinical laboratory manifestations of exposure to dioxin in children. A six-year study of the effects of an environmental disaster near Seveso, Italy. Journal of the American Medical Association 256:2687–2695. Mocarelli P, Brambilla P, Gerthoux PM, Patterson DG Jr, Needham LL. 1996. Change in sex ratio with exposure to dioxin. Lancet 348(9024):409. Morris PD, Koepsell TD, Daling JR, Taylor JW, Lyon JL, Swanson GM, Child M, Weiss NS. 1986. Toxic substance exposure and multiple myeloma: a case-control study. Journal of the National Cancer Institute 76:987–994. Morrison H, Semenciw RM, Morison D, Magwood S, Mao Y. 1992. Brain cancer and farming in western Canada. Neuroepidemiology 11:267–276. Morrison H, Savitz D, Semenciw RM, Hulka B, Mao Y, Morison D, Wigle D. 1993. Farming and prostate cancer mortality. American Journal of Epidemiology 137:270–280. Morrison HI, Semenciw RM, Wilkins K, Mao Y, Wigle DT. 1994. Non-Hodgkin’s lymphoma and agricultural practices in the prairie provinces of Canada. Scandinavian Journal of Work, Environment and Health 20:42–47.

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