Document bBVzy4JwqR4myJNoDx00qDGVg

Int. J. Cancer: 43,49-54 (1989) ' 0 1989 Alan R. Liss, Inc. Publication of the International Union Against Cancer Publication de I'Union Internationale Contre le Cancer SOFT-TISSUE SARCOMA, NON-HODGKIN'S LYMPHOMA AND OTHER CANCERS IN NEW ZEALAND FORESTRY WORKERS John Neil PEARCEI*c,hiro KAWACHI'and James FRASER~ `Department of Environmental Health, Colorado State University, College of Veterinary Medicine and Biomedical Sciences, Fort Collins, CO 80523, USA; 'Depamnent of Community Health, Wellington School of Medicine, Wellington: and 3NationalHealth Statistics Center, Wellington,New Zealand. Several studies have suggested that forestry workers are at increased risk for certain types of cancer including soft-tissue sarcoma (STS) and non-Hodgkin's lymphoma (NHL). We now report a series of national casesontrol studies based on the New Zealand Cancer Registry (NZCR). These involved 19,904 male patients with cancer for the period 1980-1984 who were aged 20 years or more at the time of registration. For each cancer site, the registrations for the remaining sites formed the control group. Current or most recent occupational titles were coded. There was an increased risk for STS (OR =3.24) in forestry workers which was confinedto men under 60 years of age at registration. An elevation in risk for N H L (OR = 1.84) was due to an increase in risk for lymphosarcoma and reticu- losarcoma (ICD 200) (OR = 3.18). Acute myeloid leukemia was also associated with forestry work, although the estimate of risk was imprecise (OR=2.24). Among other cancer sites. an increase in risk of neoplasia of the upper gastro-intestinal tract (ICD 150, 151, 152) was demonstrated. Odds ratios were elevated for cancer of the esophagus (OR= 1-77), stomach (OR =2.22). small intestine(OR =5.22), gall-bladder (OR =4.13) and pancreas(OR = I.79), as well as for nasopharyngealcancer (OR = 5.56). These increases in cancer risk were not present in sawmill workers in New Zealand during the same period. The factors responsible for the increased cancer risks in forestry workers remain unclear and require further study. Occupational mortality analyses of forestry workers in the United States and Sweden have shown that overall cancer rates are generally not elevated in this occupational group (Milham, 1976; Edling and Granstam, 1980; Stellman and Garfinkel, 1984). Excess mortality from cancer of the stomach and prostate among loggers, and cancer of the respiratory, digestive, lymphatic and hematopoietic systems among professional foresters were found in the state of Washington (Milham, 1976). An analysis of mortality in Swedish lumberjacks (Edling and Granstam, 1980) also showed an increase in risk of lymphatic and hematopoietic cancer. Excess risks of lung (Harrington et al., 1978) and bladder (Stellman and Garfinkel, 1984) cancer have been described among lumber, sawmill and forestry workers. Case-control and cohort studies of soft-tissue sarcoma (STS) and malignant lymphoma among forestry workers have been conducted to assess potential associations with occupational exposure to phenoxyherbicides and chlorophenols, compounds used in forestry and the lumber industry. Excess risks of STS (Balarajan and Acheson, 1984; Wiklund and Holm, 1986) or non-Hodgkin's lymphoma (NHL) (Wiklund et al., 1988) were not detected in 3 recent studies of agricultural and forestry workers. These studies did not include specific exposure data for chemicals. previous studies from New Zealand have demonstrated small excess risks for malignant lymphoma (Pearce et al., 1985) and leukemia (Pearce et al., 1986a) among persons engaged in the broad occupational category of agriculture, forestry and fish1%. Therefore, we conducted a series of case-control studies based on the NZCR to further examine the risks of soft-tissue sarcoma, malignant lymphoma and leukemia in forestry workers, and to assess the association between forestry work and other cancers. MATERIAL AND METHODS The study included all 24,762 male cancer cases aged 20 years or more registered with the NZCR for the period 1980 to 1984. During this period the NZCR obtained practically complete population coverage from public and private hospitals throughout the country, as well as from death certificates and autopsy findings (Foster, 1977). Virtually all patients who die of cancer are reported to the NZCR prior to death. Analysis was restricted to the 19,904 men who had a recorded occupation, 80% of the total sample. Persons for whom no job classification was available, including some retired and some unemployed men, were not included in the analysis (Table I). The study design involved a series of case-control studies, each based on the overall group of 19,904 cancer registrants. Site and subsite were categorized according to the ICD. For each site, the registrants for other sites formed the control group. For example, in the analysis for cancer of the esophagus (ICD code 150) the case group consisted of the 385 registrants with this cancer type and the control group comprised the other 19,519 cancer registrants. A similar procedure was followed for the other cancer sites, except for subtypes of leukemia, where other forms of leukemia were excluded from the control group. Occupation was defined in the National Cancer Registry as the individual's current or most recent occupation at the time of registration, and coded using the New Zkaland Standard Classification of Occupations (NZSCO) (Department of Statistics, 1980), a modification of the International Standard Clussification of Occupations (International Labour Office, 1968). The NZSCO category of forestry workers included loggers and other forestry workers. As a check on the findings in forestry workers, a similar analysis was conducted with wood preparation workers (principally sawmill workers). Loggers and other forestry workers were deleted from this latter analysis. All analyses were conducted using the Statistical Analysis System (SAS Institute, 1985). Age-adjusted odds ratios were estimated (Mantel and Haenszel, 1959) using 10-year age intervals, and 95% confidence intervals were calculated by the approximate method (Miettinen, 1976). Analyses were performed according to the ICD codes as shown in Tables I and 11, except as otherwise indicated. RESULTS There were 134 forestry workers among the 19,904 adult male cancer registrants for the years 1980-1984. The age- 4T0whom reprints should be sent, at Colorado State University Abbreviations:International Classification of Diseases 9th edition (ICD); odds ratio (OR); confidence interval (CI). Received: June IO. 1988 and in revised form August 2, 1988. 50 REIF ET A L . TABLE I - NUMBER OF CANCER CASES BY SITE IN L1ALES 4GED 10 YEARS OR MORE. NZCR 1980-19E4 Site ICD categor) Cases with occupation recorded (96 J Total cases Buccal cavity Nasopharynx Esophagus Stomach Small intestine Colon Rectum Liver Gall-bladder Pancreas Larynx Lung Bone Soft-tissue sarcoma Malignant melanoma Prostate Testis Bladder Kidney Brain, nervous system Hodgkin's disease Non-Hodgkin's lymphoma Multiple myeloma Leukemia Other cancers Total 140-146,148-149 147 150 151 152 153 154 155 156 157 161 162 I70 171 172 185 186 188 189 I9 1,192 20 1 200,202 203 204-208 140-208 649 (74) 49 (82) 385 (83) 1,014 (81) 63 (83) 2,043 (82) 1,376 (82) 184 (83) 120 (87) 571 (82) 303 (82) 4,224 (84) 49 (83) 142 (83) I , 116 (77) 2,435 (73) 399 (92) 912 (72) 542 (81) 452 (89) 170 (91) 535 (82) 295 (83) 534 (82) 1,342 (81) 19,904 (80) 872 60 463 1,258 76 2,500 I .679 223 138 695 379 5,031 59 171 1,448 3,340 435 1,259 666 506 186 652 355 649 1.662 24,762 adjusted odds ratios for specific cancer sites are shown in Table II. A general increase in risk of cancer of the digestive organs and peritoneum (ICD 150-159) was found (OR=1.49, 95% CI 1.04-2.14). Odds ratios were elevated for cancer of the esophagus (OR=1.77, 95% CI 0.66-4.75), stomach (0R=2.22, 95% CI 1.26-3.91), small intestine (OR=5.22, 95% CI 1.44-18.88), and gall-bladder (OR=4.13, 95% CI 1.42-12.04). The odds ratio for pancreatic cancer was also elevated (OR= 1.79), although the estimate was imprecise. Several other related sites, including liver and colon, did not show increased risks. An increase in risk of nasopharyngeal cancer (ICD 147) was found (OR=5.56, 95%CI 1.59-19.48). No cases of cancer of the nose and nasal sinuses (ICD 160) were recorded among forestry workers, although the expected frequency was only 0.3. Excess risks were also found for soft-tissue sarcoma (ICD 171) (0R=3.24, 95% CI 1.17-8.98) and for several types of cancer of the lymphatic and hematopoietic systems (Table III). The overall odds ratio for non-Hodgkin's lymphoma was 1.84 (95% CI 0.85-3.97), but 6 of the 7 cases occurred in ICD 200 (lymphosarcoma and reticulosarcoma), producing a risk estimate of 3.18 (95% CI 1.42-7.12). No cases of Hodgkin's disease (ICD 201) occurred in forestry workers (0.3 expected). The odds ratio for all forms of leukemia (ICD 204208) was not elevated among forestry workers but the odds ratio for acute myeloid leukemia was 2.24 (95% CI 0.726.94). The associations between cancer and forestry work were examined further by separating cases and controls into those aged less than 60 and those 60 and over at the time of registration. Cases of STS and cancer of the small intestine were confined to the younger age group, whereas the elevated risks for cancer of the stomach and pancreas were confined to the older age group. The risk for NHL was similar among the 2 age groups. When forestry workers were separated into those engaged in logging (n=47) and those involved with other forms of forestry work (n =87) the risk estimates were generally similar in both groups. As an additional check on the findings for forestry workers, risk estimates were calculated for workers engaged in wood preparation, predominantly as sawmill work- ers (Table IV). Sawmill workers would be expected to have at least as much exposure to wood dust as forest workers and loggers, and may also be exposed to chlorophenols (used as fungicides to prevent sapstain) and other chemicals employed in the treatment of sawn timber (IARC, 1981). There were 139 registrants whose occupation was listed as timber treater (n=2) or sawmiller (n= 137). With the possible exception of cancer of the gall-bladder, the elevated risks noted for loggers and foresters were not found among sawmill workers. In particular, there was little evidence for an increased risk of cancer of the esophagus, stomach, small intestine and MSOpharynx or for soft-tissue sarcoma, non-Hodgkin's lymphoma or acute myeloid leukemia. No cases of soft-tissue sarcoma or nasopharyngeal cancer were observed in sawmill workers but the expected numbers were 1.0 and 0.3 respectively. DISCUSSION This study design has been used in several previous NZCRbased case-control studies (Pearce et al., 1985, 1986a,b, 1987; Smith et al., 1984) and the relevant issues have been described (Pearce and Checkoway, 1988; Smith ef al., 1988). The main advantage of using other cancers as controls is the minimization of information bias, as well as the minimization of selection bias due to incomplete cancer registration. The main potential disadvantage is that selection bias may occur if the exposure under study is associated with an increased risk for other cancer sites. Any such bias is generally likely to be small in occupational studies (Smith et al., 1988), although more significant bias may occur if an exposure is associated with a common cancer such as lung cancer. Even in this situation, TABLE 11 - AGE-ADJUSTED ODDS RATIOS AND 95% CONFIDENCE INTERVALS FOR CANCER IN FORESTRY WORKERS. NZCR 1980-1984 ICD number Site Exposed case\ Odds ratio 95% CI 140-146.148- 149 Buccal cavitv 3 0.71 0.23-2.19 151 Stomacrh 13 2.22 1.26-3.91 154 Rectum IO 1.22 0.64-2.34 171 185 I86 191-192 204-208 Soft-tissue sarcoma Prostate Testis Braininervous svstem Leukemia - Other cancer 4 3.24 I . 17-8.98 12 0.72 0.39-1.31 6 0.99 0.38-2.61 4 1.19 0.44-3.25 4 0.96 0.36-2.61 6 0.65 0.29-1.47 - -.I -- -_.. - - -- .- - p u p , the effect estimates concern. ?his misclassification will tend-to bias the esiimate he odds ratio for STS rose from 3.24 of risk towards the null value (Copeland et al., 1977). More to 4.00 (95%CI 1.4k-11.05) and the odds ratio for NHL rose importantly, the data do not permit the examination of dose- from 1.84 to 2.25 (95% CI 1.05-4.86)when other cancers response relationships based on duration of employment in an with elevated risks among forestry workers were excluded. industry, or estimation of risks for specific departments or pro- The more conservative relative risk estimates obtained by cesses. including all other cancers as controls have been presented Increased risks for cancer of several sites within the gashere but the risks may actually be slightly higher. Previous trointestinal system and related organs were found among New New Zealand studies of the occupational category involving Zealand forestry workers. There was a general increase in risk suggested that valid effect for cancer of the digestive organs and peritoneum (ICD150- other Cancers as 159) (OR= 1.49), consistent with a previous report of mortal- eCkOWaY, 198819 ity in forestry workers (Milham, 1976). Conversely, a recent crude nature of the ockupational data and the absence of Intestinal and lymphopoietic systems, although increased risks TABLE 111 - AGE-ADJUSTED ODDS RATIOS AND 95%CONFIDENCE INTERVALS FOR CANCER IN E-GROUP,NZCR 1980-1984 Site \---I Excpasoe- s 20-59 OR Age group (years) 95% C1 cases M)+ OR 95% c 1 i i Non-Hodgkin's lymphoma (200,202) Lympho/reticulosarcoma (200) Acute myeloid leukemia (205 .O) 4 1.97 0.70-5.57 3 1.70 0.54-5.35 4 4.21 1.56-11.33 2 2.16 0.54-8.59 2 2.79 0.70-11.03 1 1.61 0.23-11.54 52 REIF ET A L TABLE N - AGE-ADJUSTED ODDS RATIOS AND 95%CONFIDENCE INTERVALS FOR SELECTED SITES AND SUBTYPES OF CANCER IN SAWMILL WORKERS, NZCR 1980-1984 ICD number 147 150 15 1 152 156 157 171 200,202 200 204-248 205.0 Site Nasopharynx Esophagus Stomach Small intestine Gall-bladder Pancreas Soft-tissue sarcoma Non-Hodgkin's lymphoma Lymphoheticulosarcoma Leukemia Acute myeloid leukemia Exposed cases 0 2 7 0 2 2 0 4 2 2 1 ordatdios - 0.72 0.95 - 2.30 0.47 - 1.17 1.11 0.52 0.89 95% CI 0.I8-2.90 0.44-2.05 0 S9-9.07 0.12- 1.83 0.43-3.17 0.27-4.48 0.13-2.07 0.12-6.39 were found among pulp and paper-mill workers for these sites. In the current study, odds ratios were elevated for cancer of the esophagus (OR= 1.77), stomach (OR=2.22), small intes- tine (OR=5.22), gall-bladder (OR=4.13) and pancreas (OR= 1.79), although some of the estimates were imprecise. Previous studies of persons engaged in forestry and logging have shown an increase in risk of stomach cancer (Milham, 1976; Siemiatycki et ai.,1986), a finding also associated with carpentry and cabinet-making (Stellman and Garfinkel, 1984; Dubrow and Wegman, 1983), plywood millworking (Mil- ham, 1976) and pulp and paper-mill work (Schwartz, 1988; Milham and Demers, 1984). A 4-fold excess in mortality from small intestinal cancer among pulp and paper-mill workers (Milham, 1976) and elevated PMRs for pancreatic cancer in sawmill workers (Milham, 1976)and pulp and paper- mill workers (Milham and Demers, 1984) have also been described. The finding of an increased risk of gall-bladder cancer in both forestry workers and sawmill workers requires further investigation. An elevated PMR for cancer of the gall-bladder was also found in a study of mortality among pulp and papermill workers in Washington State (Milham, 1983). In the current study, the risk estimates for hepato-biliary cancer (ICD 155 and 156) were 2.07 (95% CI 0.77-5.53) for forestry workers and 2.47 (95% CI 1.04-5.90) for sawmill workers, suggesting that a common mechanism may exist for the 2 closely related sites. For liver cancer risk, this might possibly reflect the fact that much of the forestry is conducted in an area of New Zealand where hepatitis B virus carrier rates and hepatocellular carcinoma rates are high (Milne et al., 1987). With that exception, regional differences in the prevalence of forestry in New Zealand are unlikely to be responsible for the cancer risks found. One risk factor common to forestry workers and other occupations involving wood is contact with wood dust. Forestry workers have an increased risk of Hodgkin's disease (Abramson et al., 1978), an association shared with other occupational groups exposed to wood dust (Petersen and Milham, 1974; Grufferman et al., 1976; Greene et al., 1978). In the current study no cases of Hodgkin's disease were registered among forestry workers, although less than one was expected, and the risk estimate in sawmill workers was not elevated. Previous reports have also linked wood-related work with cancer of the nasopharynx, a finding reproduced in this study. An excess of woodworkers was reported among cases of adenocarcinoma of the nasopharynx in the UK (Mould and Bakowski, 1976), while a 7-fold increase in risk of nasopharyngeal cancer associated with exposure to chlorophenols was reported in Northern Sweden where forestry and wood milling are predominant industries (Hardell et al., 1982). There appeared to be effect modification by woodwork, consistent with the well-known relationship between nasal and paranasal sinus cancer and exposure to wood dust (Acheson et al., 1967). No support for a relationship with chlorophenols was found in a Danish case-control study (Olsen and Jensen, 1984). Furthermore, no sawmill workers were found among cases of nasopharyngeal or nasal cancer in the current study, although less than one case of each was expected. Cigarette smoking has been associated with increased risks of cancer of the nasopharynx, esophagus and pancreas (Doll and Peto, 1983). To evaluate the role of smoking in the excess risks of these cancers among forestry workers, we examined data on smoking and occupation from the 1981 New Zealand census (Department of Statistics, 1983). A higher proportion of forestry workers were current smokers (49.2%) or ever- smokers (65.5%) compared to the total full-time male labor force, among whom 37.7% smoked currently and 59.6% had ever smoked. The principal impact of cigarette smoking is on the risk of lung cancer, and some elevation in the risk of lung cancer among forestry workers was found (OR= 1.27). Therefore, the increased risks of these cancers may be due, at least in part, to cigarette smoking. However, no increase in risk was noted for several other sites associated with smoking (larynx, bladder, oral cavity, lip) and exposures to chain-saw exhausts containing polycyclic aromatic hydrocarbons such as benzo[a]pyrene could have been partially responsible. The finding of an increased risk of STS among New Zealand forestry workers is puzzling. An initial possibility is that this association represents a chance finding, particularly since a recent case-control study from the National Cancer Register of England and Wales (Balarajan and Acheson, 1984) and a large cohort study of Swedish agricultural and forestry workers (Wiklund and Holm, 1986) did not find elevated risks for forestry workers. A second possibility is that the increase in risk is due to exposure to phenoxyacid herbicides or chlorophenois, as suggested by case-control studies in Sweden (Hardell and Sandstrom, 1979; Eriksson et al., 1981). The first Swedish study (Hardell and Sandstrom, 1979) was conducted in an area where forestry was prevalent, and where phenoxyherbicides had been sprayed extensively. Despite the fact that phenoxyherbicides and chlorophenols have been produced in New Zealand and widely used in agriculture and forestry since the 1940s it currently appears unlikely that the increased risk of STS observed in forestry workers is due to exposure to these chemicals, for several reasons. First, a previous case-control study of STS conducted in New Zealand (Smith et al., 1984) found little evidence of an association between STS and exposure to phenoxyherbicides or chlorophenols. The exposure data were obtained by interview and were presumably more accurate and appropriate than the occupational information available for the current analysis. CANCER IN NEW ZEALAND FORESTRY WORKERS NO association was found for employment in forestry work, reticulosarcoma (ICD 200), among forestry workers. No in- nor was there an increase in risk associated with spraying crease in risk following exposure to forestry work, employ- chemicals or other forms of exposure to herbicides. Second, ment in a sawmill or as a timber merchant was demonstrated in previous New Zealand case control studies of cancer which in previous New Zealand case-control studies of NHL based assessed exposure to phenoxyherbicides (Smith et al., 1984; on interview data (Pearce et al., 19866, 1987). In contrast to pearce er al., 19866, 1987), only 3 of 81 forestry workers findings in Sweden where 5- and 8-fold increases in risk of (3.7%) were reported to have sprayed chemicals. Third, PO- malignant lymphoma (ICD 200, 201 and 202 combined) were tential exposure to chlorophenols in a sawmill or as a timber associated with exposure to phenoxyherbicides and chlorophe- merchant was not associated with an increase in risk of STS nols (Hardell et al., 1981), no increase in risk of NHL could (Smith et al., 1984). An elevated risk was found for log- be shown for these exposures in New Zealand, whether the lumber inspectors and lumber graders in a recent study from analysis included cases registered under ICD 200 or ICD 202 Washington State (Woods et al., 1987), but other jobs involv- or whether other cancer cases or general population members ing comparable chlorophenol exposure showed no increase in were used as controls. A recent Swedish cohort study (Wik- risk of STS. Further, studies of sawmill workers, a highly lund et al., 1988)showed no excess risk of NHL among timber exposed group who treat wood with sodium pentachlorophenol cutters or other forestry workers. However, an elevated PMR and manually handle the wood during the sorting and cutting for lymphosarcoma was found in US pulp and paper-mill processes, show no increase in risk for STS (IARC, 1981; workers (Milharn and Demers, 1984), while Woods et al. Sterling, 1982). Finally, the current study showed no compa- (1987) found an elevated risk of NHL in persons who reported rable increase in risk of STS among New Zealand sawmill spraying forests with herbicides. workers. In summary, the data suggest that employment as a forestry A third possibility is that the increased risk of STS, and worker in New Zealand carries increased risks of STS, NHL other cancers, may be associated with the use of chain saws or and other cancers. It currently appears unlikely that these are other equipment used by forestry workers. Chain saws were caused by exposure to phenoxyherbicides or chlorophenols, widely introduced into the New Zealand forest industry in the although this hypothesis cannot be excluded. Further studies 1 9 6 0 ~and the finding that the risk of STS was confined to are needed to confirm that forestry workers are at increased men aged less than 60 at registration suggests that a recently risk of these cancer types, and to ascertain which aspects of introduced work practice might be responsible. The use of forestry may be involved. chain saws results in exposure to fuels, cutting and lubricating oils and emissions of polycyclic aromatic hydrocarbons. Diesel-powered skidders and tractors have been employed for the ACKNOWLEDGEMENTS extraction O f logs from the forest in recent years, but Only a This study was conducted during the tenure, by J.R., of a small proportion of the logging crew are machine operators. Senior Fogarty International Fellowship from the US National Many of the same considerations apply to the finding of an Institutes of Health. 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