Mortality and Cancer Incidence among
Sawmill Workers Exposed to
Chlorophenate Wood Preservatives
Clyde Hertzman, MD, Kay Teschke, PhD, Aleck Ostry, MSc, Ruth Hershler;
MSc, Helen Dimich- Ward, PhD, Shona Kelly, John J. Spinelli, PhD, Richard P
Gallagher, MA, Mary McBride, MSc, and Stephen A. Marion, MD
Introduction
A cohort study of more than 26 000
sawmill workers in British Columbia,
Canada, was conducted to determine
whether workers exposed to chloro-
phenate wood preservatives were at in-
creased risk of non-Hodgkin's lymphoma
or soft tissue sarcoma. A secondary
objective was to investigate the possible
association of exposure with Hodgkin's
disease, lung cancer, and nasal cancer.
Chlorophenates were widely used as
fungicides in British Columbia from the
1940s to 1989. By 1987, 95 sawmills in
the province were using approximately
1100 tonnes of it per year,"2 to which
more than 100 000 workers were exposed
before chlorophenate use was discontin-
ued in 1989. Other uses of chlorophen-
ates, such as for tanning, have been
limited in Canada but widespread in other
countries. Like the chlorophenoxy herbi-
cides (2,4-D and 2,4,5-T), chlorophenates
belong to the class of dioxin-contami-
nated substances. The dioxin isomers
readily detected in them are hexa-, hepta-,
and octa-chlorinated isomers rather than
2,3,7,8-tetrachlorodibenzo-p-dioxin, which
has generated widespread concem as a
carcinogen.3 Workplace exposure to penta-
and tetrachlorophenates occurs through
direct skin contact during spraying and
dipping of sawed logs and planed boards.4
Breathing chlorophenate vapor, aerosols,
and contaminated sawdust has also been a
route of exposure, although a worker's
dose from inhalation is typically less than
that from skin contact.5
At the time this work began, no
epidemiological study of British Colum-
bian sawmill workers had previously been
done. There were, however, 10 case-
control studies in the literature of cancer
outcomes following exposure to chloro-
phenates and/or chlorophenoxy acids.6'5
Among the four that included soft tissue
sarcoma as an outcome, two found an
association6'10 and two did not.12'15 Simi-
larly, two studies found an association
with non-Hodgkin's lymphoma7'8 and two
others13"5 did not. Of two other "posi-
tive" case-control studies, one found an
association between "high-grade" expo-
sure to chlorophenates and Hodgkin's
disease" and another9 found an associa-
tion with nasal and nasopharyngeal can-
cer. Studies of nasal cancer in the
woodworking industry1622 show a consis-
tent association with wood dust exposure.
The inconsistent results of the non-
Hodgkin's lymphoma and soft tissue
sarcoma studies thus raise the prospect of
bias resulting from reliance upon study
subjects' recall of their personal exposure
histories, which is characteristic of case-
control studies. However, the cohort study
of British Columbia sawmill workers
avoided this problem by relying on
employment histories abstracted from
routinely collected records. By recruiting
sawmills that began using chlorophenates
in the 1940s, 1950s, and early 1960s, this
study was able to enroll a large enough
Clyde Hertzman, Kay Teschke, Aleck Ostry,
Ruth Hershler, Helen Dimich-Ward, Shona Kelly,
John J. Spinelli, and Stephen A. Marion are with
the Department of Health Care and Epidemiol-
ogy, University of British Columbia, Vancouver.
Richard P. Gallagher and Mary McBride are with
the Department of Epidemiology and Biometrics,
British Columbia Cancer Agency.
Requests for reprints should be sent to
Clyde Hertzman, MD, Department of Health
Care and Epidemiology, University of British
Columbia, Mather Bldg, 5804 Fairview Ave,
Vancouver, BC, Canada, V6T 1Z3.
This paper was accepted September 19,
1996.
American Journal of Public Health 71
Hertzman et al.
TABLE 1-Demographic Characteristics of the British Columbia Sawmill
Workers Cohort, by Employment in 11 Chlorophenate-Using
(Exposed) and 3 Non-Using (Unexposed) Mills
Exposed mills
Years of employment, no.
Year of entry to cohort
Age of entry, y
Age at death, y
Years of follow-up, no.
Unexposed mills
Years of employment, no.
Year of entry to cohort
Age of entry, y
Age at death, y
Years of follow-up, no.
aThis is evidence of child labor in the mills earlier in the century, and not a recording error.
cohort to detect small increases in the
incidence of or mortality from soft tissue
sarcoma or non-Hodgkin's lymphoma.
Methods
Cohort Definition
The sawmills selected for this study
were large, had used chlorophenates for a
long period, and had usable personnel
records available. Records of 23 829
sawmill workers from 11 chlorophenate-
using mills and 2658 workers from 3
control mills were abstracted to create two
files: a personal identifier file and a job
history file. These files included all who
had worked for at least 1 year in a study
mill between January 1, 1950, and Decem-
ber 31, 1985. For those who worked on a
casual or intermittent basis, a total of 260
days of work constituted a qualifying
year.
Ascertainment of Vital and Cancer
Case Status
The personal identifier file was
linked, with the use of probablistic
linkage methods, to the British Columbia
Death File (1950 to 1989) and the British
Columbia Cancer Incidence File (1969 to
1989). Case ascertainment in this latter
file is estimated to be more than 95%.23
Probablistic linkage was based on the
level of agreement on full name and
birthdate between individuals in the per-
sonal identifier, or cohort, file and individu-
als in the two outcome files who were the
closest matches. Rules for scoring agree-
ments and disagreements on surname;
given names; and day, month, and year of
birth were based on the generalized
72 American Journal of Public Health
Mean Minimum Maximum
9.8 1 48.1
1962 1940 1985
27.0 1 oa 75
64.6 18 102
24.5
7.3 1 51.7
1973 1941 1985
27.0 12a 66
54.4 19 90
15.5 ... ...
iterative record linkage system.26 This
process identified 3948 deaths and 1547
incident cases of cancer. Pension records
and motor vehicle records were also
checked, and inquiries were made at local
union halls to ascertain the vital status and
the last known date alive of all those who
had left a sawmill but were not labeled
dead after linkage.
Because of gaps between the last
known date alive for some subjects and
the end of the study follow-up period,
17% of person-years were unaccounted
for, much of which was attributable to
individuals in their 8th, 9th, and 10th
decades of life. Since this might represent
a larger than expected proportion of
deaths outside of British Columbia, a
second link was conducted with the
Canadian Mortality Data Base. As a
result, 1 extra year of deaths (1990) was
added to the file, and the total number of
deaths rose to 4710 (4539 in chloro-
phenate-using mills, 171 in nonchloro-
phenate-using mills). Of the 474 deaths
that were added, up to and including the
year 1989, 278 had occurred in British
Columbia and only 196 had occurred
outside. All told, the proportion of deaths
outside the province was only 4.4%.
Next, those sawmill workers who
were lost to follow-up but who had social
insurance numbers (72.9% of the total)
were linked by Statistics Canada to the
Canadian income tax file to find their last
year of filing, thereby further reducing the
number of person-years for which vital
status was unconfinned. As a result of the
tax file linkage, the number of sawmill
workers who were still contributing any
person-years in an unverified vital status
declined from 10 343 (39.1% of the total
cohort of 26 487) to 3791 (14.3% of the
total).
Exposure Assessment
Old records and key informants were
used to reconstruct industrial histories for
each mill. Time lines were created that
showed the history of the introduction of
chlorophenates as well as changes in
formulation, application technology, and
locations in the milling process where
chlorophenates were applied.3 From these
time lines, the study team identified for
each mill three or four exposure-constant
time periods, during which the chloro-
phenate application process and formula-
tion were approximately constant, and
exposures to chlorophenates were stable
for a given job title.
Retrospective exposure assessments
were carried out for each exposure-
constant time period in each mill accord-
ing to a protocol developed in the
previous feasibility study.24'25 A summary
exposure score was then calculated for
each job title in each time period. This
score, which combined then averaged the
worker raters' estimates of duration (hours
per day) and frequency (days per year) of
exposure to chlorophenates for each job
title, can be roughly interpreted as a
number of "exposure hours per year"
(range = 0 to 2000). The score for each of
the workers' job titles was multiplied by
the time spent in that job and summed
across all job titles to get a worker's
cumulative exposure score. This was used
as the time-dependent exposure variable
in the analysis.
Analysis
Since sawmilling is a standard pro-
cess and the different mills used similar
formulations over time, it was decided to
combine data from different mills using
the common measure of exposure rather
than to analyze each mill separately. It
was estimated that the combined cohort
would have 90% power to detect standard-
ized incidence ratios of 1.50 for non-
Hodgkin's lymphoma and 2.50 for soft
tissue sarcoma. Standardized mortality
and incidence ratio analyses were carried
out using a person-years program created
for the International Agency for Research
on Cancer.27 The male population of
British Columbia served as the external
comparison group. Causes of death were
coded according to the International
Classification of Diseases, 8th edition
(ICD-8), whereas cancer incidence was
January 1997, Vol. 87, No. I
 Chlorophenates and Cancer

coded according to the ICD-9. Person-

years at risk began after 1 year of TABLE 2-Standardized Mortality Ratios (SMRs) and 95% Confidence
exposure. In the overall analyses of Intervals (Cis) for All-Cause and Cause-Specific Mortality among
mortality and cancer incidence, chloro- the British Columbia Sawmill Workers Cohort, by Employment in
phenate and nonchlorophenate mills were 11 Chlorophenate-Using and 3 Non-Using Mills
analyzed separately. In analyses of expo-
sure gradients, person-years and out- Person-Years
Person-Years to Last Known Year to 1 99oa
comes from the nonchlorophenate mills
were included in the lowest exposure Cause of Death Observed Expected SMR 95% Cl SMR 95% Cl
category.
Analyses were lagged 5, 15, and 20 Exposed mill workers (n = 23 829)
years for those cancer outcomes that All causes 4539 4718 0.96 0.94, 0.99 0.81 0.79, 0.83
showed some evidence of an association All infective causes 25 38.16 0.66 0.45, 0.92
All accidents 405 531.1 0.76 0.70, 0.83
with chlorophenate exposure. This in- Occupational lung disease 11 9.33 1.18 0.66,1.95 1.00 0.56,1.66
volved counting persons as exposed 5, 15, All cancers 1155 1079 1.07 1.02,1.12 0.89 0.85, 0.94
and 20 years after the exposure occurred, Specific cancers
on the assumption that the biologic effect Pharynx and buccal cavity 23 24.81 0.93 0.63,1.32
Digestive and peritoneum 343 337.4 1.02 0.93,1.11
of exposure, if any, would begin then. A Respiratory system 388 352.8 1.10 1.01, 1.20 0.92 0.85,1.00
standardized rate ratio analysis was done Nose and nasal 1 1.50 0.67 0.03, 3.16 0.57 0.02, 2.71
for non-Hodgkin's lymphoma in which Larynx 15 11.40 1.32 0.81, 2.03 1.09 0.67,1.69
the cohort members served as intemal Lung 369 336.1 1.10 1.01, 1.20 0.92 0.84,1.00
Bone 5 3.46 1.45 0.57, 3.04 1.27 0.50,2.66
controls. This approach addressed the Soft tissue sarcoma 6 4.28 1.40 0.61, 2.77 1.18 0.51,2.33
problem of comparing standardized inci- Melanoma 17 12.51 1.36 0.86, 2.04 1.15 0.73,1.72
dence ratios among subgroups with differ- Male genital 116 97.24 1.19 1.02,1.39 0.96 0.82,1.12
Bladder 33 30.2 1.09 0.80,1.46 0.90 0.65,1.20
ent age distributions, and by setting the Kidney 38 27.98 1.36 1.02,1.78 1.14 0.85,1.49
standardized rate ratio for the lowest Brain and CNS 44 41.84 1.05 0.80,1.35
exposed group to 1.0, it also removed the Endocrine 6 4.04 1.49 0.64, 2.94 1.28 0.56,2.53
effect of the difference in the disease rate Hodgkin's disease 8 9.86 0.81 0.40,1.47 0.71 0.35,1.28
All non-Hodgkin's lymph 36 33.26 1.08 0.80,1.43 0.91 0.67,1.20
between the British Columbian popula- Lymphosarcoma 23 15.77 1.46 1.00, 2.07 1.26 0.86,1.79
tion and the least exposed members of the Other non-Hodgkin's 13 17.32 0.75 0.44,1.19 0.61 0.36, 0.98
cohort. Multiple myeloma 18 16.82 1.07 0.69,1.59 0.89 0.57,1.32
Leukemia 39 40.59 0.96 0.72,1.26
Other and unspecified 34 34.92 0.97 0.72,1.30
Myelofibrosis 5 2.92 1.71 0.67, 3.60 1.37 0.54, 2.89
Results Thyroid diseases 2 1.30 1.54 0.26, 4.84 1.35 0.23, 4.26
Diabetes 48 54.80 0.88 0.68,1.11
Follow-Up Metabolic deficiencies 12 10.39 1.15 0.66,1.87 0.96 0.55,1.56
Aplastic anemia 3 2.53 1.19 0.32, 3.07 0.97 0.26, 2.51
Table 1 presents basic demographic Anemias 7 5.23 1.34 0.63, 2.52 1.07 0.50,2.01
characteristics for the cohort: years of Other disease of blood 5 3.54 1.41 0.55, 2.97 1.17 0.46,2.46
employment, year and age at entry, age at Mental disease and retardation 32 47.80 0.67 0.49, 0.90
death, and average years of follow-up. Nervous system disease 52 59.74 0.86 0.68,1.10
Circulatory system disease 2013 1764 1.14 1.10,1.18 0.74 0.71, 0.76
The cohort provided 583 190 person- Respiratory disease 258 313.7 0.82 0.74, 0.91
years of follow-up in the chlorophenate Digestive system disease 179 208.6 0.86 0.75, 0.97
mills and 41 280 person-years of fol- Genitourinary disease 53 55.56 0.95 0.75,1.20
Bladder infection 9 4.21 2.14 1.11,3.74 1.61 0.73 3.05
low-up in the nonchlorophenate mills, Musculoskeletal and connective 11 10.97 1.00 0.56,1.66
with the assumption that any cohort tissue disease
member not found in the mortality fol-
low-up was alive in 1990. Of these Unexpansed mill workerSb (n = 2658)
624 470 person-years, 70 119 (11.2%) All causes 171 192.91 0.89 0.78,1.01
were contributed by "lost to follow-up" Specific cancers
years. The person-years lost to follow-up Nose and nasal cavities 0 0.00 0.00
Lung 12 13.53 0.89 0.51,1.44
could have had unpredictable conse- Soft tissue sarcoma 0 0.25 0.00
quences for analysis, so each analysis was All non-Hodgkin's lymphoma 1 1.61 0.62 0.20, 2.94
done twice, including and excluding these Lymphosarcoma 0 0.54 0.00
person-years. Hodgkin's disease 0 0.45 0.00

Reliability of Exposure Assessment
Intraclass correlation coefficients
were calculated for each group of worker
exposure raters in each time period at each
mill. These coefficients showed levels of
reliability similar to those found in the
feasibility studies. The range of exposure
aResults are reported for only those conditions of special relevance to the study or for which
the SMR based on counting person-years to the last known year is greater than 1.0.
bResults are presented for only those conditions of special relevance to the study.
scores in each mill was similar, and These findings supported the original
comparable work areas in different mills expectation that mills could be combined
ended up with similar exposure scores. for analysis.

January 1997, Vol. 87, No. 1 American Journal of Public Health 73

Hertmzan et al.

male genital, and kidney cancers are all

TABLE 3-Standardized Mortality Ratios (SMRs) and 95% Confidence greater than 1.0, with a lower confidence
Intervals (Cis) for All Causes and Selected Cancers, by limit that is also greater than 1.0 in the last
Cumulative Exposure to Chlorophenatesa (Person-Years Counted known year analysis but not in the
to 1990) analysis to 1990. Among causes of death
with standardized mortality ratios greater
Cumulative Hours Person- x2Trend than 1.5 in chlorophenate mills in the last
of Exposure Years Observed Expected SMR 95% Cl (F)
known year analysis (myelofibrosis, dis-
All causes eases of the thyroid, and bladder infec-
<120 61 980 379 458 0.83 0.76, 0.90 0.22 (.64) tion), only myelofibrosis and thyroid
120-1 999 193 176 991 1233 0.80 0.76, 0.85 disease are elevated in the analysis to
2 000-3 999 130 243 737 890 0.83 0.78, 0.88
4 000-9 999 137 375 1121 1504 0.75 0.71, 0.78 1990.
210 000 101 696 1482 1741 0.85 0.82, 0.89 Table 3 gives the mortality gradients
All cancers (to 1990) by level of exposure to chloro-
<120 105 103 1.02 0.86,1.20 2.47 (.12) phenates for all causes, all cancers, and
120-1 999 241 266 0.91 0.81, 1.01 those cancers of particular interest. Work-
2 000-3 999 190 193 0.99 0.87,1.10 ers from the nonchlorophenate sawmills
4 000-9 999 274 337 0.81 0.73, 0.90
.10 000 384 439 0.88 0.80, 0.95 were included in the lowest exposure
Nasopharynx category. No statistically significant posi-
(1470-1479) tive exposure-response gradients are seen
<120 1 0.45 2.21 0.09,10.53 0.65 (.42) among any of the causes of death of
120-1 999 0 1.20 0.00 interest on Table 3, or among similar
2 000-3 999 1 0.86 1.16 0.04, 5.51
4 000-9 999 1 1.13 0.89 0.03, 4.20 analyses when person-years were fol-
210 000 0 1.17 0.00 lowed up to the last known year alive.
Nose and nasal However, lymphosarcoma comes closest
cavities (1600-1609) to showing a trend, given that the highest
<120 0 0.14 0.00 1.35 (.25) two exposure categories have standard-
120-1 999 0 0.38 0.00 ized mortality ratios of 1.64 and 1.45. It is
2 000-3 999 0 0.28 0.00
4 000-9 999 0 0.48 0.00 possible that the lack of an overall trend
210 000 1 0.52 1.91 0.07, 9.12 may be due to small case numbers in some
Lung (1620-1629) exposure categories.
<120 37 31.6 1.17 0.87,1.54 4.25 (.04)
120-1 999 81 80.8 1.00 0.83,1.21 Cancer Incidence
2 000-3 999 53 58.3 0.91 0.71, 1.14
4 000-9 999 96 102 0.94 0.79,1.12 Standardized incidence ratios for
.10 000 114 142 0.80 0.68, 0.94 cancers in the 11 chlorophenol-using mills
Soft tissue sarcoma were calculated for the period 1969 to
(1641,1710-1719) 1989. The number of person-years in
<120 0 0.46 0.00 1.23 (.27)
120-1 999 3 1.24 2.42 0.65, 6.26 which the outcome status is uncertain
2 000-3 999 1 0.88 1.14 0.04, 5.39 varies according to cancer; this is because
4 000-9 999 1 1.28 0.78 0.03, 3.70 the cause-specific endpoints are different
.10 000 1 1.49 0.67 0.03, 3.18
(Continued) for each cancer and thus create different
subsets of the cohort who are "com-
pletely" followed up. The tables for
cancer incidence (Tables 4 and 5) are in
Mortality flects the impact of person-years lost to
follow-up. parallel with those for mortality (Tables 2
Table 2 presents the standardized and 3), so that like Table 2, Table 4 covers
mortality ratios for all cause and cause-
Notwithstanding this difference, there cancer incidence to the last known year of
are few positive associations between follow-up and for all person-years to
specific mortality for the 11 chlorophenate
sawmills. The set of columns on the left is chlorophenate exposure and mortality. 1989. Cancers that were identified solely
based on counting person-years until the The "last known year" analysis gives a by death records (a circumstance primar-
last known year alive; the set on the right standardized mortality ratio for non- ily confined to deaths outside of British
counts person-years until the end of the Hodgkin's lymphoma of 1.08. When this Columbia) were included as incident
follow-up period (1990) unless the person is divided between lymphosarcoma and cancers as of the worker's date of death.
is known to have died at an earlier date. other non-Hodgkin's lymphomas, the stan- In the last known year analysis,
These latter figures are reported only for dardized mortality ratios are 1.46 (95% several cancers appear to be "in excess";
conditions of special relevance to this confidence interval [CI] = 1.00, 2.07) and that is, the lower 95% confidence limit for
study or when the standardized mortality 0.75 (95% CI = 0.44, 1.19), respectively. the chlorophenate sawmill workers is
ratio to the last known year is greater than However, the standardized mortality ratio greater than 1.00. These cancers are
1.0. The all-cause standardized mortality for lymphosarcoma drops to 1.26 (95% rectum, lung, mediastinum, and chronic
ratios for workers in chlorophenate mills CI = 0.86, 1.79) when person-years are lymphocytic leukemia. The only one of
by each of these two counts are 0.96 and counted until 1990. Similarly, standard- these that is also found in excess on the
0.81, respectively, a difference that re- ized mortality ratios for respiratory, lung, analysis to 1989 is cancer of the mediasti-

74 American Journal of Public Health January 1997, Vol. 87, No. I

 Chlorophenates and Cancer

num, which, upon disaggregation, proved

to be a heterogeneous mixture of tumors TABLE 3-Continued
with no common etiology. Standardized
incidence ratios for non-Hodgkin's lym- Cumulative Hours Person- x2 Trend
phoma and soft tissue sarcoma were of Exposure Years Observed Expected SMR 95% Cl (F)
greater than or equal to 1.0 in each
analysis, but in both cases the confidence Hodgkin's disease
interval always included 1.00. Tongue, (2010-2019)
gum, nasal, eye, and endocrine gland <120 0 0.95 0.00 0.38 (.54)
120-1 999 2 3.17 0.63 0.11, 1.99
cancers had standardized incidence ratios 2 000-3 999 1 2.26 0.44 0.02, 2.10
greater than 1.5 but these were not 4 000-9 999 4 2.94 1.36 0.46, 3.12
statistically significant elevations (see -10 000 1 2.38 0.42 0.02,1.89
Table 4); all remained elevated, but not All non-Hodgkin's
significantly, when person-years were lymphoma
determined to 1989. (2000-2009,
2020-2029,
Table 5 parallels Table 3 in showing 2053, 2290)
exposure-response gradients for cancer <120 3 3.35 0.90 0.24, 2.32 0.33 (.57)
incidence to 1989. It shows a positive and 120-1 999 7 9.01 0.78 0.36,1.46
statistically significant exposure-response 2 000-3 999 3 6.42 0.47 0.13, 1.20
4 000-9 999 13 9.95 1.31 0.77, 2.08
gradient for non-Hodgkin's lymphoma. .1 000 11 12.56 0.88 0.49,1.45
When the same analysis is done excluding
person-years lost to follow-up, however, Lymphosarcoma
(2000-2001,
the positive trend for non-Hodgkin's 2003-2007,
lymphoma does not achieve statistical 2009)
significance. The difference in the find- <120 1 1.41 0.71 0.03, 3.36 0.89 (.35)
ings is due to the disproportionate num- 120-1 999 5 4.03 1.24 0.49, 2.61
2 000-3 999 1 2.93 0.34 0.01, 1.62
bers of person-years that are not ac- 4000-9999 8 4.87 1.64 0.81, 2.87
counted for in the three intermediate -10 000 8 5.50 1.45 0.72, 2.63
exposure categories in the latter analysis. Other non-Hodgkin's
From lowest to highest exposure category, lymphoma (2002,
the person-years lost to follow-up repre- 2008, 2020, 2022-
sent 6.1%, 15.7%, 13.8%, 10.4%, and 2029, 2053, 2290)
<120 2 1.91 1.04 0.18, 3.30 0.08 (.77)
3.4% of the totals in Table 5. When these 120-1 999 2 4.93 0.41 0.07,1.28
person-years are removed, they have the 2 000-3 999 2 3.44 0.58 0.10,1.83
effect of inflating the incidence ratios in 4 000-9 999 5 5.03 0.99 0.39, 2.09
the intermediate exposure categories com- -10 000 3 7.02 0.43 0.11, 1.10
pared with the extremes, which, in this Multiple myeloma
case, weakens the trend. (2030-2039)
<120 3 1.56 1.92 0.52, 4.97 0.01 (.94)
Exposures were lagged for the can- 120-1 999 2 3.98 0.50 0.09,1.58
cers reported in Table 5 so that the 2 000-3 999 3 2.90 1.04 0.28, 2.68
person-years of exposure were counted 4 000-9 999 3 5.24 0.57 0.15,1.48
not in the year they occurred but 5, 15, or -10 000 8 7.21 1.11 0.55, 2.00
20 years later. Lagging had no meaningful
effect on the results. The gradient for Note. ICD-9 codes are given in parentheses after cancer site/type.
aWorkers from unexposed mills were included in the lowest exposure category.
non-Hodgkin's lymphoma persisted at
approximately the same level of strength
across all lags, and no new associations
emerged among any of the other cancers 1.57; 4000 to 9999 hours, 1.38; and similar to that seen in previous analyses
of interest. 10 000 hours or more, 1.62. As with the based on cumulative hours of chloro-
standardized incidence ratio analysis, the phenate exposure: less than 5 years of
Non-Hodgkin's Lymphoma results were weakly positive. The trend employment, 0.65; 5 to 9 years, 0.97; 10
Because of the positive trend for approached statistical significance (X2 to 14 years, 0.81; 15 to 19 years, 1.34; and
non-Hodgkin's lymphoma with chloro- trend = 3.61, P = .057), but none of the 20 years or more, 1.40. As with the
phenate exposure in the standardized 95% confidence intervals for individual cumulative chlorophenate exposure analy-
incidence ratio analysis, several additional exposure groups excluded 1.0. sis, none of the confidence intervals for
analyses were done to further examine A standardized incidence ratio analy- individual duration of employment catego-
this relationship. sis for non-Hodgkin's lymphoma was also ries excluded 1.0, but the trend was
An analysis using the lowest expo- conducted by years of employment in statistically significant (X2 trend = 5.74,
sure category as an internal reference chlorophenate mills. Thus, workers from P = .02). This raised the prospect that the
group gave the following standardized nonchlorophenate mills were excluded association may not be related to chloro-
rate ratios: less than 120 cumulative hours from this analysis. In terms of the strength phenate exposure but rather to other
of chlorophenate exposure, 1.00; 120 to of association, the pattern of increasing aspects of work in a sawmill, such as
1999 hours, 0.87; 2000 to 3999 hours, risk with increasing work experience was exposure to wood dust.

January 1997, Vol. 87, No. I American Journal of Public Health 75

Hertzman et al.

sure (>10 000 cumulative hours) and

TABLE 4-Standardized Incidence Ratios (SIRs) and 95% Confidence longest work history (20 years or more),
Intervals (Cis) for Cancer Incidence among the British Columbia with 20 non-Hodgkin's lymphoma cases
Sawmill Workers Cohort, by Employment in 11 (standardized incidence ratio = 1.54,
Chlorophenate-Using and 3 Non-Using Mills P = .04). Poisson regression analysis re-
vealed that cumulative exposure did not
Person-Years add any explanatory power after years of
Person-Years to Last Known Year to 1 989a
employment were added to the model.
Cancer Site Observed Expected SIR 95% Cl SIR 95% Cl When the variables were entered in
reverse order, years of employment did
Exposed mill workers (n = 23 829) not add explanatory power to cumulative
All cancer except skin 1498 1424.0 1.05 1.01, 1.10 0.87 0.83, 0.90 exposure.
Lip 22 22.31 0.99 0.67,1.41
All mouth 30 27.55 1.09 0.78,1.48 0.90 0.65,1.23
Tongue 16 10.07 1.59 0.99, 2.42 1.32 0.83, 2.01 Discussion
Gum 5 2.04 2.45 0.96, 5.16 2.03 0.80, 4.30
Nasopharynx 2 5.96 0.34 0.06,1.06 More weight has been given to the
Esophagus 21 21.10 1.00 0.67,1.43 0.82 0.55,1.20 analyses that include all person-years than
Stomach 72 65.28 1.10 0.90,1.34 0.92 0.74,1.12 to those that exclude person-years lost to
Colon 111 120.0 0.93 0.78,1.08
Rectum 105 85.8 1.22 1.03,1.44 1.01 0.85,1.20 follow-up. This is because -the efforts
Liver 13 14.39 0.90 0.53,1.44 made to ensure completeness of follow-up
Gallbladder 8 9.20 0.87 0.43,1.57 were thorough within British Columbia
Pancreas 46 46.4 0.99 0.76, 1.27 and were supplemented with linkage to
Nose and nasal cavities 7 3.44 2.03 0.95, 3.83 1.71 0.80, 3.20
Larynx 30 27.46 1.09 0.79,1.48 0.90 0.65,1.23 Canada-wide mortality and tax records.
All respiratory 352 315.0 1.12 1.02,1.22 0.93 0.85,1.00 Even without the tax record supplement,
Lung 344 309.0 1.11 1.02,1.22 0.93 0.84,1.00 ascertainment of vital status through
Pleura 3 4.82 0.62 0.17,1.61 Statistics Canada's mortality database is
Mediastinum 5 1.62 3.09 1.20, 6.50 2.72 1.06, 5.70 estimated to be 97.6% for deaths in
Bone 4 3.29 1.22 0.41, 2.78 1.05 0.36, 2.40
Soft tissue sarcoma 11 9.38 1.17 0.66,1.94 1.00 0.56,1.66 Canada and 93.1% for deaths overall.28
Melanoma 38 39.85 0.95 0.71, 1.25 Those lost to follow-up were mostly
Prostate 282 278 1.01 0.92,1.12 0.82 0.74, 0.91 short-term workers who left employment
Testis 18 18.7 0.96 0.62,1.43 in the sawmill before social insurance
Bladder 94 79.35 1.18 0.99,1.41 0.98 0.82,1.20 numbers were introduced in Canada in the
Kidney 46 42.9 1.07 0.82,1.37 0.89 0.68,1.10
Eye 8 4.08 1.96 0.97, 3.54 1.64 0.80, 2.90 early 1960s. Unlike mortality analyses,
Brain and central nervous 36 29.6 1.22 0.90,1.61 1.03 0.77,1.37 analyses of cancer incidence missed those
system who were diagnosed with cancer after
Thyroid 6 7.74 0.78 0.34,1.53 leaving British Columbia but were not
Endocrine gland 2 1.26 1.59 0.27, 5.00 1.35 0.23, 4.30
Hodgkin's disease 16 12.3 1.30 0.81, 1.98 1.16 0.70, 1.80 dead by 1989. There is reason to believe
Non-Hodgkin's lymphoma 63 52.5 1.20 0.96, 1.48 1.00 0.80, 1.20 that this was a small number since only
Myeloma 17 17.7 0.96 0.61, 1.44 4.4% of deaths were found outside the
Leukemia 47 39.9 1.18 0.91, 1.50 0.98 0.75,1.20 province, suggesting that outmigration
Acute lymphocytic 2 2.06 0.97 0.17, 3.06 was uncommon among the cohort.
Acute granulocytic 5 6.21 0.81 0.32, 1.70
Chronic lymphocytic 24 14.3 1.67 1.16, 2.36 1.37 0.90,1.90 No association was found between
Chronic granulocytic 7 6.46 1.08 0.51, 2.04 0.92 0.40,1.70 soft tissue sarcomas, nasal cancer, and
Other and unspecified 5 10.9 0.46 0.18, 0.97 lung cancer and exposure to chlorophen-
All lymph and haematological 142 122 1.16 1.01, 1.34 0.97 0.84,1.10 ates in British Columbian sawmills. With
Other and unspecified 60 58.6 1.02 0.82,1.27 0.99 0.80,1.20
Primary unknown 69 45.1 1.53 1.24, 1.87 1.26 1.02, 1.50 respect to soft tissue sarcomas, however,
the problems with ICD classification are a
Unexposed mill workersb(n = 2658) possible barrier to complete ascertain-
All cancer except skin 49 75.1 0.65 0.51, 0.83 ment. This problem was minimized be-
Nose and nasal cavities 0 0.20 0.00 cause the British Columbia Cancer Agency
Lung 9 14.6 0.62 0.32, 1.08 codes all incident cases of soft tissue
Soft tissue sarcoma 0 0.71 0.00 sarcomas based on histology, not on
Hodgkin's disease 0 1.24 0.00 anatomical location. For the small number
Non-Hodgkin's lymphoma 2 3.49 0.57 0.10, 1.80
of cases that are first ascertained at death,
aResults are reported for only those conditions of special relevance to the study or in which the
similar assurances cannot be given.
SIR based on counting person-years to the last known year is greater than 1.0. In general, analyses of mortality
bResults are presented for only those conditions of special relevance to the study. from non-Hodgkin's lymphoma were
negative. However, the subgroup of lym-
phosarcoma showed a pattern of mortality
by exposure level that, in retrospect, was
To gain further insight into this issue, of employment and cumulative exposure. similar to the pattern for incident cases of
the patterns of incidence of non-Hodgkin's The excess risk was concentrated in the non-Hodgkin's lymphoma. Moreover, the
lymphoma were cross-tabulated by years cell with the highest chlorophenate expo- case-fatality rate was lower than expected,

76 American Journal of Public Health January 1997, Vol. 87, No. I

 Chlorophenates and Cancer

as there were only 37 deaths from

non-Hodgkin's lymphoma in the full 40 TABLE 5-Standardized Incidence Ratios (SIRs) and 95% Confidence
years of mortality follow-up while there Intervals (Cls) for Selected Cancers, by Cumulative Exposure to
were 65 incident cases over 20 years of Chlorophenatesa (Person-Years Counted to 1989)
cancer follow-up.
The increased risk of non-Hodgkin's Cumulative Hours Person- x2 Trend
lymphoma associated with chlorophenate of Exposure Years Observed Expected SIR 95% Cl (F)
exposure, despite its modest size, is All cancers
meaningful. A gradient of increasing risk <120 45 549 116 211 0.55 0.47, 0.64 1.33 (.25)
with increasing exposure is apparent 120-1 999 123 839 312 537 0.58 0.53, 0.64
when person-years lost to follow-up are 2 000-3 999 82 262 229 376 0.61 0.54, 0.68
included in analysis. Notwithstanding 4 000-9 999 82 849 359 590 0.61 0.56, 0.66
>10 000 70 817 534 869 0.61 0.57, 0.66
recent objections,29 the Mantel extension
test confirms the existence of the trend. Nasopharynx (1470-1479)
<120 45 737 1 0.73 1.37 0.05, 6.49 1.76 (.19)
When the effect of the difference in the 120-1 999 124 588 0 1.98 0.00
disease rates between the British Colum- 2 000-3 999 82 865 1 1.38 0.73 0.03, 3.44
bian population and the least exposed 4 000-9 999 83 780 0 1.65 0.00
members of the cohort is removed through .10 000 72 246 0 1.83 0.00
the standardized rate ratio analysis, the Nose and nasal cavities
exposure group-specific rate ratios are (1600-1609)
<120 45 737 0 0.36 0.00 0.45 (.50)
higher than their respective incidence 120-1 999 124 567 3 0.93 3.22 0.87, 8.34
ratios on standardized incidence ratio 2 000-3 999 82 863 2 0.66 3.04 0.52, 9.54
analysis, but the trend is weakened. Table 4 000-9 999 83 780 0 0.97 0.00
6 shows that the risk is concentrated in the .10 000 72 232 2 1.39 1.44 0.25, 4.53
highest category of exposure and length Lung (1620-1629)
of work. However, the results indicate that <120 45 700 30 29.8 1.01 0.72,1.37 2.09 (.15)
the risk gradient with cumulative expo- 120-1 999 124 523 75 76.5 0.98 0.80,1.19
2 000-3 999 82 833 47 53.9 0.87 0.67,1.11
sure cannot be statistically separated from 4 000-9 999 83 631 94 88.0 1.07 0.89,1.27
years of employment. .10 000 72 149 107 139 0.77 0.65, 0.90
The prospect that wood dust or other Soft tissue sarcoma (1710-
undefined sawmill exposures may be the 1719)
proximate risk factor is refuted by three <120 45 737 0 1.11 0.00 1.54 (.21)
observations. First, random errors in the 120-1 999 124 558 6 2.89 2.07 0.90, 4.10
2 000-3 999 82 857 2 2.00 1.00 0.17, 3.15
estimates of exposure by job title would 4 000-9 999 83 779 2 2.60 0.77 0.13, 2.42
reduce the strength of association between 210 000 72 237 1 3.15 0.32 0.01, 1.50
risk of non-Hodgkin's lymphoma and Hodgkin's disease
cumulative exposure more than it would (2010-2019)
the strength of association with length of <120 45 737 0 1.65 0.00 0.43 (.51)
employment. Potential sources of error 120-1 999 124 557 6 4.61 1.30 0.56, 2.57
2 000-3 999 82 856 3 3.04 0.99 0.26, 2.55
include the exposure estimation process, 4 000-9 999 83 765 4 3.11 1.29 0.44, 2.95
the definition of exposure-constant time 210 000 72 242 3 2.69 1.11 0.30, 2.88
periods, the grouping and collating of job Non-Hodgkin's lymphoma
titles, and the care with which job title (2020-2029)
changes were recorded in sawmill person- <120 45 736 4 5.89 0.68 0.23,1.56 4.36 (.04)
nel records. In contrast, there is little room 120-1 999 124 546 9 15.2 0.59 0.31, 1.03
2 000-3 999 82 831 11 10.5 1.04 0.59,1.74
for random error in the recording of work 4 000-9 999 83 741 15 14.7 1.02 0.63,1.57
time per se. Second, the risk was concen- .10000 72136 26 20.0 1.30 0.91, 1.80
trated in the subgroup with more than 20 Multiple myeloma
years of exposure, who were also in the (2030-2039)
greatest cumulative exposure category. <120 45 736 2 1.69 1.18 0.20, 3.73 0.00 (.99)
This is consistent with the pattem of 120-1 999 124 586 4 4.30 0.93 0.32, 2.13
2 000-3 999 82 864 2 3.04 0.66 0.11, 2.07
induction and latency usually found in 4 000-9 999 83 780 1 5.20 0.19 0.01, 0.91
relation to occupational cancer. Finally, .10 000 72 238 9 8.09 1.11 0.58,1.94
analysis by mill does not reveal a risk Chronic lymphocytic leukemia
concentrated in any one location, and (2100-2109)
analysis by work area within each mill <120 45 730 2 1.40 1.43 0.24, 4.50 0.10 (.76)
does not reveal a risk concentrated in any 120-1 999 124 566 3 3.55 0.84 0.23, 2.19
2 000-3 999 82 849 5 2.54 1.97 0.77, 4.14
unexpected location. If wood dust or other 4 000-9 999 83 767 6 4.30 1.40 0.60, 2.76
unknown sawmill exposures were the 210 000 72 218 9 6.47 1.39 0.72, 2.43
proximate risk factor, they might be
expected to elevate the risk in the Note. ICD-9 codes are given in parentheses after cancer site/type.
nonchlorophenate mills, but they did not. aWorkers from unexposed mills were included in the lowest exposure category.
Three other studies of wood-working

January 1997, Vol. 87, No. I American Journal of Public Health 77

Hertzman et al.
TABLE 6-Observed and Expected Cases of Non-Hodgkin's Lymphoma (n = 63), by Years of Employment and
Cumulative Exposure to Chlorophenates (Workers from Exposed Mills Only and Person-Years Counted
to 1989)
Cumulative <5
Hours of
Chlorophenate Observed Expected
Exposure Cases Cases
<120 1 1.36
120-1 999 7 11.82
2 000-3 999 6 6.33
4 000-9 999 0 2.16
.10 000 0 0.0
aStandardized incidence ratio = 1.54; P = .04.
occupations and non-Hodgkin's lym-
phoma have been published,3>32 each of
which has failed to find an association.
Non-Hodgkin's lymphoma has also been
associated with metal-working occupa-
tions and solvent exposures other than
benzene and formaldehyde,33 both of
which occur in sawmills. The prevalence
of these exposures, however, is low and
does not explain the association with
exposure to chlorophenates or years of
employment.
Since this study began, the literature
on the cancer experience of chlorophenate-
exposed workers and woodworkers has
expanded considerably. Five studies found
borderline to no association between soft
tissue sarcoma and chlorophenate expo-
sure in working populations, which is
consistent with our results.3438 Similarly,
three negative studies of the association
with non-Hodgkin's lymphoma mortality
were published.35'36.38 In each case, power
was a problem. In one study,38 a standard-
ized mortality ratio of 299 was reported,
but it entailed very wide confidence limits
that included 1.0. None of these studies
used non-Hodgkin's lymphoma incidence
as an outcome. Kogevinas et al.39 recently
reported the results of a nested case-
control study of 32 non-Hodgkin's lym-
phoma cases in an intemational cohort of
workers exposed to phenoxy herbicides,
chlorophenols, and dioxins. Elevations in
risk, not statistically significant, were
found for those with "medium or high"
cumulative exposures to any chlorophe-
nol and to pentachlorophenol.
The results of our study, which is the
most statistically powerful of all those
available to date, are consistent with these
borderline results. It is doubtful that new
studies will provide a more definitive risk
estimate unless advances in tissue typing
78 American Journal of Public Health
Years of Employment in Chlorophenate-Using Mills
5-9 10-14
Observed Expected Observed Expected
Cases Cases Cases Cases
0 0.44 0 0.19
0 1.74 0 0.58
3 2.24 1 0.71
5 4.93 3 2.27
2 0.99 1 2.39
are able to identify specific non-Hodgkin's
lymphoma subtypes in which the risk is
concentrated. Although the risk is small in
epidemiological terms, it is considerable
in terms of quantitative risk assessment,
exceeding one incident cancer per 1000
person lifetimes. This supports the case
for careful handling of chlorophenates at
work and, in particular, for workplace
controls that eliminate direct human con-
tact with chlorophenates in liquid or
aerosol form. D
Acknowledgments
This research was funded by NHRDP grant
6610-1602-55.
The authors wish to thank Danielle
Sciarretta, Jim Blair, Terry Anderson, Bill
Threlfall, Val Embree, Janice McAra, Susan
Gittinger, Sheryl Atkinson, and Roxanne
Rousseau for their assistance during the course
of the project.
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