The Prostate 34:100–112 (1998)

Prostate Cancer in Pesticide Applicators in

Swedish Agriculture
Jan Dich* and Kerstin Wiklund
Department of Cancer Epidemiology, Institution of Oncology-Pathology, Radiumhemmet,
Karolinska University Hospital, Stockholm, Sweden

BACKGROUND. The use of chemicals in agriculture has been associated with elevated risks
of prostate cancer. The aim of this study was to analyze prostate cancer risk in a cohort of
20,025 pesticide applicators in agriculture licensed between 1965–1976.
METHODS. The cohort was followed up in the Swedish Cancer Register from date of licence
until death or December 31, 1991. The mean follow-up time was 21.3 years.
RESULTS. We found a statistically significant increased risk of prostate cancer with 401 cases
observed compared to 355 expected, with a standardized incidence ratio (SIR) of 1.13 (95%
confidence interval: 1.02–1.24). There were 7 cases among those born in 1935 or later, and the
SIR was 2.03 (0.82–4.19). For those born earlier than 1935 the SIR was 1.12 (1.01–1.24).
CONCLUSIONS. These findings of a statistically significant increased risk of prostate can-
cer, together with recent results from other studies, imply a relationship between agrochemi-
cals or other risk factors in the environment of farmers and prostate cancer. Prostate 34:100–
112, 1998. © 1998 Wiley-Liss, Inc.

KEY WORDS: risk evaluation; cohort study; farmers; lifestyle; pesticide exposure; cad-
mium exposure

INTRODUCTION The most consistent findings regarding occupations

Prostate cancer is the most common cancer among
men in many Western countries including Sweden,
and the fourth most common type of cancer among
men in the world. In 1985, approximately 300,000 men
in the world were diagnosed with prostate cancer [1]
and the incidence has increased considerably in most
countries during the last decade [2]. The annual world
standardized age-adjusted incidence rate per 100,000
varies from 0.8 in Quidong, China to 102 in blacks in
Atlanta, Georgia [2,3]. Scandinavians have a higher
incidence than men in Southern Europe, with a rate
comparable to that of white men in the U.S. [1]. Dif-
ferences in diagnostic methods and availability of
medical care contribute to the difference between de-
veloping and industrialized countries [4–6]. The aver-
age annual increase in Sweden from 1975–1994 was
approximately 1.7%, and 5,748 new cases were diag-
nosed in 1994. The age-standardized incidence ad-
justed to the world population was 61.8 [7]. Despite
the high incidence of this disease, its major causes are
still unclear [8,9].
at high risk involve farmers, cadmium workers, and
rubber workers [10]. As early as 1931, Henry et al. [11]
found an excess risk in some agricultural occupations,
and a number of subsequent studies have indicated
that men engaged in agriculture may be at higher risk
of prostate cancer [10,12,13]. However, some studies
could not confirm this hypothesis [14–16]. Previously
we did not find excess risk of prostate cancer among
Swedish farmers [17] or pesticide applicators [18].
The use of agricultural chemicals, especially pesti-
cides, has increased rapidly since the 1940s, and some
are suspected of being carcinogenic [12]. Exposure to
pesticides has been associated with increased risk of
prostate cancer in farmers.
Cadmium and cadmium compounds, which occur
as impurities in fertilizers and are used as active in-
gredients in some pesticides, are associated with pros-
*Correspondence to: J. Dich, Department of Cancer Epidemiology,
Institution of Oncology-Pathology, Radiumhemmet, Karolinska
University Hospital, S-171 76 Stockholm, Sweden.
Received 17 May 1996; Accepted 27 November 1996

© 1998 Wiley-Liss, Inc.

 Prostate Cancer in Pesticide Applicators 101

tate cancer in humans and animals [19–21]. No other TABLE I. Observed and Expected Number of Prostate
chemicals, groups, or mixtures predominant in occu- Cancer Cases Until December 31, 1991, SIR, and 95%
pational exposure, pesticides, or drugs have so far CI for SIR in the Cohort of Swedish
been associated with prostate cancer in humans or ani- Pesticide Applicators
mals [19,20,22].
The aim of the present study was to extend earlier Observed Expected SIR 95% CI
studies on Swedish pesticide applicators concerning Total 401.0 355.4 1.13 (1.02–1.24)
the risk of prostate cancer. We have, in addition, per- Year of license
formed subgroup analyses in year-of-birth (up to 1934, 1965–1966 299.0 260.8 1.15 (1.02–1.29)
and 1935 to present) and year-of-license (1965–1966, 1967–1976 102.0 94.7 1.08 (0.88–1.31)
and 1967–1976) groups and in the area of the country Year of birth
in which pesticide use is most prevalent (Malmöhus Up to 1934 394.0 352.0 1.12 (1.01–1.24)
County, Sweden). 1935 to present 7.0 3.4 2.03 (0.82–4.19)
Malmöhus
County 63.0 62.5 1.01 (0.77–1.29)
MATERIALS AND METHODS
The study cohort consisted of 20,025 men who held
a license for pesticide application issued between on approximately 400,000 person-years. The unique
1965–1976 and who had a complete personal identifi- personal identification number, issued to all Swedish
cation number. In the computerized record linkages, residents since 1947, was used as the matching vari-
the unique personal identification number was used able in the computerized record linkage. Notification
for matching purposes. The personal identification of all malignant and some benign tumors has been
number consisted of 10 digits: two each for year, compulsory for almost all physicians and pathologists
month, and day of birth, a three-digit serial number, since the Registry was established in 1958. Each case is
and a check digit. Only 18 of those with a license were thus in general reported from at least two different
excluded owing to incomplete identification. sources. The study included all registered cases of ma-
Since there is no information on individual expo- lignant prostatic tumors according to the modified
sure to pesticides in this cohort, a random sample of version of the seventh revision of the International
268 applicators was previously described with refer- Classification of Diseases [23].
ence to the use of pesticides with information on trade Expected number of cases in the cohort was based
name, number of application days in a year and num- on the annual incidence of prostate cancer in 5-year
ber of years, application method, the use of protective age groups in the male Swedish population. The stan-
clothing, tobacco habits, and occupational history dur- dardized incidence ratio (SIR) was calculated as the
ing the 1950s, 1960s, and 1970s [18]. Pesticides had ratio between the observed and expected number of
been used 1 day or more in 1950–1979 by 92% of the cases. The 95% confidence intervals (CI) for the SIR
pesticide applicators. The most common pesticides were calculated according to Byar’s approximation
were phenoxy acetic acid herbicides, organochlorine [24].
compounds (e.g., DDT, lindane, pentachlorophenols),
mercury, and organophosphorous compounds. Use RESULTS
was considerably more frequent in the south and very
scarce in the north. The use of protective clothing has, In the cohort, 401 cases of prostate cancer were
despite special training, been only slightly more fre- found compared to 355 expected (SIR 1.13, 95% con-
quent among pesticide applicators than among farm- fidence interval: 1.02–1.24) (Table I). For those born in
ers in general. 1935 or later the SIR was 2.03 (0.82–4.19) and for those
The division into year-of-birth groups was due to a born earlier than 1935, 1.12 (1.01–1.24).
higher use of pesticides and fertilizers among younger For applicators licenced in 1965–1966 the SIR was
applicators. Licenses for applying pesticides in agri- 1.15 (1.02–1.29), and in the subgroup licenced in 1967–
culture became compulsory in 1965 and a majority of 1976, 1.08 (0.88–1.31). We found no increased relative
the applicators who had their licenses issued in 1965 risk in the southern region, Malmöhus County, where
or 1966 have used pesticides to a greater extent in the the SIR was 1.01 (0.77–1.29).
1950s and 1960s compared to those who had their li-
censes issued in 1967–1976 [18]. DISCUSSION
The cohort was followed in the Swedish Cancer
Registry from date of license until December 31, 1991, The etiology of prostate cancer is still unclear and
or until death if prior to that date. The study is based the epidemiology is therefore of considerable interest,
102 Dich and Wiklund
mainly because of high and increasing incidence. Even
if the main contribution is earlier detection due to new
diagnostic tools, there seems to be an increased inci-
dence, presumably depending on environmental fac-
tors [25,26]. Studies on occupation and prostate cancer
have indicated that farmers may be at higher risk for
prostate cancer. We have not found any excess risk of
prostate cancer among Swedish farmers in general
[17], but a statistically significant increased risk among
pesticide applicators in agriculture.
If exposure to agricultural chemicals can influence
prostate cancer risk, this should be seen among groups
who are more heavily exposed. Pesticide applicators
are shown to use more pesticides and hence are more
exposed than farmers in general. As many as 92% of
pesticide applicators have been exposed to pesticides,
compared to only 40% of farmers [17].
In two papers, studies on the risk of prostate cancer
among farmers have been reviewed. One summarizes
that of 24 studies on farming and prostate cancer, 17
showed an increased risk, of which 10 were statisti-
cally significant [12]. In the other review, of 29 recent
studies with 5 or more cases who had worked as farm-
ers or farm workers, the risk of prostate cancer was
found to be significantly elevated in 13 [27]. Some of
the studies, however, are identical in the reviews.
In Tables II and III, cohort and case-control studies
up to 1996 are presented and include published stud-
ies on farmers, pesticide applicators, and related oc-
cupations dealing with exposure to agricultural
chemicals and the association with prostate cancer.
More than 40 cohort studies have so far been pub-
lished (Table II). The results are inconclusive, but the
majority show statistically significant increased risk.
Excess risk of prostate cancer, among farmers, pesti-
cide applicators, and industrial workers exposed to
similar chemicals, was found in the majority of case-
control studies and several of them showed that the
risk was statistically significant (Table III). However,
some published case-control studies are not included
in Table III because the controls were chosen from
patients with other cancer diagnoses. This can lead to
biased results, since such controls may not reflect rep-
resentative exposures. Most of the studies deal with
risks related to farming. However, some cohort stud-
ies conducted on chemical workers and manufacturers
contain information on direct exposure to specified
chemicals.
Agricultural Chemicals
Exposure to agricultural chemicals, such as pesti-
cides and cadmium from fertilizers, has been associ-
ated with an increased risk of prostate cancer
[12,65,69,70]. An early study by Henry et al. in 1931
[11] found an increased incidence of prostate cancer
among farm bailiffs and foremen but not among agri-
cultural workers and farmers. Some chemicals, e.g.,
mercury and arsenical compounds, were used as pes-
ticides before 1931.
Knowledge of specific pesticide exposure and risk
of prostate cancer is very scarce.
In a Canadian study a statistical trend was found
between the number of acres sprayed with herbicides
and prostate cancer mortality [10]. Phenoxy acetic ac-
ids were the most commonly used herbicides.
A population-based case-control study of cancer
and occupation in Canada found a weak support for
10 years or more duration as farmers or horticultural-
ists or occupied in agriculture (Table III) and also with
use of pesticides [13].
In a recently conducted case-control study [66], the
odds ratio for farming was statistically significant.
Case-control studies conducted in Missouri [71]
found an excess risk of prostate cancer in farmers and
also in occupations with exposure to exhaust fumes,
solvents, or fuel oils. Farmers are often exposed to
these agents.
Four cohort studies [38,39,43,53] conducted on
manufacturers or chemical workers in plants manu-
facturing phenoxy acetic acid herbicides or chlorophe-
nols found an increased, but not statistically signifi-
cant, risk of prostate cancer. Four similar studies
[34,51,56,57] did not find any excess risk. Three of
these studies were, however, small.
There is a weak association between exposure to
agricultural chemicals such as pesticides and risk of
prostate cancer. This must, however, be interpreted
cautiously since in the environment of farmers and
pesticide applicators there are other potential carcino-
gens, e.g., exhaust fumes, solvents, or fuel oils, as well
as exposure to animals and indirectly to zoonotic vi-
ruses. No studies on experimental animals involving
pesticide exposure have, however, shown any signs of
tumors in the prostate [20].
Cadmium is one of the few chemicals connected
with increased prostate cancer risk both in humans
and animals [19,20]. An association between cadmium
exposure and prostate cancer was suggested in 1965
by Potts [72], and several studies recently reviewed
[70] support this result.
Pesticide applicators are to a minor extent exposed
to cadmium via use of fertilizers, fungicides, and in-
secticides [73–75]. Both the use and quality of fertiliz-
ers, however, are very different in various countries
[76].
One study found a significant increased risk of
prostate cancer in nitrate fertilizer workers [77]. Ni-
trate fertilizers contain less cadmium than other fertil-
izers, but other studies [47,55,78] could not find any
 Prostate Cancer in Pesticide Applicators 103

TABLE II. Cohort Studies of Exposure to Pesticides and Prostate Cancer Risks in Farmers, Pesticide Applicators, and
Related Occupations†

No. of
Exposure exposed SMR/PMR/SIR
Reference Country Study population assessment cases (95% CI) Comments

Alavanja et U.S. 1,495 white male extension Extension agents 46 1.50** (1.13–1.99) PMR
al., 1988 agents from the U.S. Potential exposure
[28] Department of Agriculture to pesticides
(USDA) mortality file,
deceased 1970–1979,
compared to the white male
population
Alavanja et U.S. 1,411 forest and soil Forest and soil 40 1.6*** (1.2–2.2) PMR
al., 1989 conservationists in the conservationists Pesticides not
[29] USDA mortality file, specified
deceased 1970–1979,
compared to the U.S. white
population
Alavanja et U.S. 22,938 white male workers Workers in flour 37 1.00 (0.70–1.38) SMR
al., 1990 who were enrolled in the life mills and other Fumigation of
[30] insurance program of the grain industries 18 0.97 (0.57–1.53) pesticides
American Federation of
Grain Millers followed up
1955–1985 compared to the
U.S. white male population
Alberghini et Italy 4,580 male pesticide Pesticide 10 0.59 (0.28–1.09) SMR
al., 1991 applicators, identified from applicators National reference
[31] the local agricultural Fungicides and
inspectorate offices, followed organochlorine
1974–1987 compared to the insecticides the
general population most used
pesticides in the
examined area
Blair et al., U.S. Farmers from 22 different Farmers 7,753 1.08 (1.06–1.11) Metaanalysis
1992 [32] studies mortality study;
15/22 studies,
showed RR >1.0
Blair et al., U.S. 119,648 white males, 11,446 Farmers 3,765 1.18 (1.14–1.22) PMR
1993 [33] nonwhite males from 564 1.14 (1.05–1.24) White males
mortality records from 23 Nonwhite males
states, 1984–1988, compared
to decendents with neither
an occupational code of
farmer nor an industry code
of agricultural products
Bond et al., U.S. 878 chemical workers Chemical 1 1.04 (0.01–5.76) SMR
1988 [34] identified from 1945–1982 workers Small study
census lists compared to U.S. potentially
white men and to other male exposed to
employees not exposed to 2,4-D
2,4-D
Buesching U.S. 71 white male farmers Farmers >5 1.95 SMR
and (Illinois) identified from death
Wollstadt, certificates with cancer,
1984 [35] 1973–1980, compared to total
white male population in the
county
104 Dich and Wiklund

TABLE II. Cohort Studies of Exposure to Pesticides and Prostate Cancer Risks in Farmers, Pesticide Applicators, and
Related Occupations†—Continued

No. of
Exposure exposed SMR/PMR/SIR
Reference Country Study population assessment cases (95% CI) Comments

Burmeister, U.S. 6,402 white male farmers Farmers 1,138 1.10** (1.04–1.17) PMR
1981 [36] (Iowa) according to job 1.41** (1.33–1.49) SMR
classifications by the
Department of Labor
deceased due to cancer,
1971–1978, compared to 1960
and 1970 censuses, male
nonfarmers
Burmeister, U.S. White male farmers identified Farmers 1.24 PMR
1990 [37] (Iowa) from death certificate tapes, Mainly exposed to
1979–1986 insecticides; the
number of the
study population
is not given
Cantor and U.S. 9,677 aerial pesticide Aerial pesticide 5 1.36 (0.44–3.17) SMR
Booze, applicators and flight applicators,
1991 [16] instructors compared to U.S. flight 2 0.57 (0.06–2.07)
white male population instructors
Coggon et U.S. 5,754 manufacturers and Manufacturers 18 1.33 (0.79–2.11) SMR
al., 1986 applicators of phenoxy acetic and pesticide No differences after
[38] acid herbicides employed applicators 10 years latency
1947–1975, identified from mainly exposed period, white
personnel records traced to to MCPA farmers only
the end of 1983 compared to
the national population
Cook et al., U.S. 2,189 manufacturers of Manufacturers of 6 1.88 (0.69–4.08) SMR
1986 [39] phenoxy acetic acid phenoxy acetic
herbicides 1940–1979, acid herbicides
identified from department and
census lists and personnel chlorophenols
records compared to
decendents in aggregated
rural areas of England and
Wales, 1968–1978
Delzell and U.S. 9,245 white and 3,508 Farmers PMR
Grufferman, (N.C.) nonwhite male farmers age
1985 [40] 15 years or more deceased ù65 years: 211 1.1 (0.9–1.3) White males
1976–1978 identified from <65 years: 22 1.6 (1.0–2.5)
the N.C. Department of
Human Resources computer >65 years: 126 0.9 (0.8–1.1) Nonwhite males
files of death certificates, <65 years: 21 1.3 (0.8–2.2)
compared to other male N.C.
residents, who died during
the same period
Faustini et Italy 1,701 farmers or farm workers Farmers or farm 8 0.91 (0.39–1.79) SMR
al., 1993 age 30 years or more workers
[41] registered in the 1971 census
or on their arrival, with
same occupation in 1988 or
at their date of death,
followed 1972–1988,
compared to the general
population
 Prostate Cancer in Pesticide Applicators 105

TABLE II. —Continued

No. of
Exposure exposed SMR/PMR/SIR
Reference Country Study population assessment cases (95% CI) Comments

Figá- Italy 2,310 pesticide applicators who Pesticide SMR

Talamanca obtained licence 1973–1979 applicators 6 0.89 (0.33–1.93) Provincial basis
et al., 1993 followed up to 1988 or to 1.00 (0.37–2.17) National basis
[42] time of death if earlier, Exposure to
compared to provincial and pesticides, but
national mortality rates not specified
Fingerhut et U.S. 5,172 workers at 12 plants, Manufacturing of 17 1.22 (0.71–1.95) SMR
al., 1991 with 1,520 workers in a chlorinated 9 1.52 (0.70–2.90)
[43] subcohort with ù1 year compounds
exposure to TCDD, at least with potential
20 years of latency: vital contamination
status determined 1987 from by TCDD
records of the Social Security
Administration or from the
National Death Index
Firth et al., New 26,207 cancer cases from New Woodworkers, 54 1.43 (1.07–1.86) SIR
1996 [44] Zealand Zealand cancer registry protective 22 1.96 (1.23–2.97) No report on
1972–1984, compared to service workers significance in
population of men in full- or farmers or
part-time employment age pesticide
15–64 years, 1981 census, as applicators
standard
Gallagher et Canada 28,032 male farmers age 20 Farming 764 1.13*** (1.05–1.22) PMR
al., 1984 (British years or more deceased
[45] Columbia) 1950–1978 identified in the
Division of Vital Statistics;
age-standardized
proportional mortality ratios
(PMRs) were calculated for
160 causes of deaths
Gallagher et Canada 2,328 farm workers age 20 Farming 40 1.09 (0.80–1.49) PMR
al., 1984 (British years or more deceased
[46] Colombia) 1950–1978, identified in the
Division of Vital Statistics;
PMRs calculated as above
Gunnarsdóttir Iceland 5,922 male farmers registered Farming 39 0.71 (0.53–0.93) SIR
and at the Farmer’s Pension
Rafnsson, Fund 1977–1983, compared
1991 [47] to Icelandic men
Kato et al., Japan 17,164 male cancers including Farming 82 1.40** (1.11–1.74) SPR
1990 [48] 1,557 agricultural workers
age 30 years or more,
registered 1979–1987,
compared to the general
population of Aichi
Prefecture
Kristensen et Norway 136,463 males occupied in Farming 277 0.96 (0.85–1.08) SIR
al., 1996 agriculture identified from
[49] the agricultural and
horticultural censuses
1969–1989 compared to the
general Norwegian
population
Orchards, greenhouses Horticulture 33 1.45 (1.01–2.09) RR
106 Dich and Wiklund

TABLE II. Cohort Studies of Exposure to Pesticides and Prostate Cancer Risks in Farmers, Pesticide Applicators, and
Related Occupations†—Continued

No. of
Exposure exposed SMR/PMR/SIR
Reference Country Study population assessment cases (95% CI) Comments

Levi et al., Switzerland 4,461 deceased cancer cases in Occupational, 26 0.79 (0.52–1.16) PMR
1988 [50] (Vaud) agricultural occupations mainly farming
registered in the Vaud
Cancer Registry 1977–1984,
compared to cause-specific
expected numbers based on
the proportional cancer
mortality experience of the
whole data set
Lynge, 1985 Denmark 3,390 manufacturers of Occupational 1 0.55 RR
[51] phenoxy acetic acid manufacturing Small study
herbicides followed up pesticides
1947–1982 in the Danish
Cancer Registry, compared
to the general Danish
population
Morrison et Canada 1,148 farmers age 45 years or Farmers, 127 2.23** (1.30–3.84) RR
al., 1993 more, deceased 1971–1987 herbicide P < 0.01 for farmers
[10] identified in central farm spraying spraying more
registers compared to death than 250 acres
records for all Canadians age with herbicides;
45–69 years otherwise, no
relation
d:o age 45 years or more 20 1.19 (0.98–1.45) Herbicide spraying
>250 acres vs. 0
acres
Morrison et Canada 169,222 fruit and vegetable Farmers SMR
al., 1995 farmers age 35 years or more 16 1.12 (0.64–1.82) >10 acres in
[52] at some point in the potatoes
follow-up period in the 19 1.28 (0.77–2.00) >10 acres in
Canadian Mortality Database vegetables
1971–1987, compared to 6 0.91 (0.33–1.97) >10 acres in
death records for all berries
Canadians 86 1.01 (0.81–1.25) 25 or more fruit
trees
Ott et al. U.S. 2,187 manufacturers of 2,4,5-T Occupational 8 1.90 (0.82–3.75) SMR
1987 [53] and chlorophenols identified manufacturing
from company records and of 2,4,5-T and
Social Security chlorophenols
Administration deceased
1940–1982, compared to all
U.S. white male deaths
Pearce and New Agricultural workers Farming 1.61 (1.12–2.25) RR
Reif, 1990 Zealand Numbers of study
[54] population or
disease incidence
are not given
Rafnsson Iceland 5,923 farmers registered with Farming 8 0.86 (0.37–1.69) SMR
and the Farmers’ Pension Fund
Gunnarsdóttir, until 1984; death certificate
1989 [55] from the Statistical Bureau of
Iceland compared to all
Icelandic males of the same
age
 Prostate Cancer in Pesticide Applicators 107

TABLE II.—Continued

No. of
Exposure exposed SMR/PMR/SIR
Reference Country Study population assessment cases (95% CI) Comments

Ramlow et U.S. 770 workers, a subcohort of a Pentachloro- SMR

al., 1996 larger Dow Company cohort phenol Small study
[56] potentially exposed exposure,
1940–1989 or from date of 1940–1989 3 0.79 (0.16–2.31) 0 year latency
employment compared to 3 0.86 (0.18–2.50) 15 years latency
the U.S. white male
population
Riihimäki et Finland 1,926 pesticide applicators Phenoxy acetic 2 1.82 RR
al., 1982 from the personnel records acid herbicides Small study
[57] of the four main Finnish
employers involved in
chemical brushwood control
exposed at least 2 weeks
during 1955–1971 and
followed up 1972–1980 for
mortality and 1972–1978 for
cancer morbidity
Ronco et al., Denmark, Denmark: a cohort of farmers Farming SIR
1992 [58] Italy 15–74 years old, identified Denmark: 399 0.89 (0.80–0.98)
from the 1970 census farmers, farm 63 0.76 (0.58–0.97)
workers
Italy: a cohort of farmers 18–74 Italy: MOR
years old, identified from the farmers, farm 10 0.9
1981 census workers 2 0.53
Both compared to the
general populations
Saftlas et al., U.S. 35,972 white male farmers or Farming 1,016 1.22* (0.83–0.89) PMR
1987 [59] (Wisconsin) farm laborers age 18 years or
more from mortality records
1968–1976, compared to U.S.
white male and Wisconsin
white male nonfarmers
Farmers born 1905–1958 30 1.12 (0.76–1.59) Herbicides
29 1.08 (0.72–1.55) Insecticides
33 1.31 (0.90–1.84) Fertilizers
50 1.39 (1.03–1.83) Dairy products
Stark et al., U.S. 18,811 farmers and operators Farmers, 41 0.92 (0.66–1.25) SMR
1987 [14] (N.Y. age 18 years or more pesticide
state) identified through member applicators
lists of the N.Y. State Farm
Bureau, deceased 1973–1984,
compared to the U.S. census
population age 25 years or
more who resided in N.Y.
State
Stubbs et al., U.S. 7,504 white farm owners, 7,404 Farmers, farm 202 1.22** (1.06–1.40) PCMR
1984 [60] (California) white farm workers workers 1.10
deceased 1978–1979,
identified through death
certificates from the
California Department of
Health Services’ Center for
Health Statistics compared to
death certificates of the
general population on
California
108 Dich and Wiklund

TABLE II. Cohort Studies of Exposure to Pesticides and Prostate Cancer Risks in Farmers, Pesticide Applicators, and
Related Occupations†—Continued

No. of
Exposure exposed SMR/PMR/SIR
Reference Country Study population assessment cases (95% CI) Comments

Torchio et Italy 23,401 pesticide applicators Pesticide 66 0.96 (0.74–1.22) SMR

al., 1994 including 2,683 deaths applicators
[61] 1970–1986, identified in records
of hospital discharges of the
region and from death
certificates compared to regional
and provincial populations
Une et al., U.S. 2,820 farmers and farm workers Farmers, farm PMR
1987 [62] (South age 35–84 years, deceased workers
Carolina) 1983–1984, identified in the White males 54 1.57** (1.18–2.05)
South Carolina Department of Nonwhite 60 0.86 (0.66–1.11)
Health and Environmental males
Control computer file of death
certificates
Wigle et al., Canada 69,513 male farmers age 35 years Farmers 441 0.96 (0.87–1.05) SMR
1990 [15] (Saskat- or more identified in the 1971 Overall
chewan) Census of Agriculture and mortality and
corresponding Census of also the risk
Population, deceased 1971–1985, cancer deaths
compared to the mortality among
records of Census Population Saskatchewian
farmers are 20–
25% lower than
for all
Saskatchewian
men
Wiklund, Sweden 19,490 primary tumours diagnosed Farmers 3,890 0.95 (0.91–0.99) O/E
1983 [63] 1961–1973 among agricultural
workers identified in the
Swedish Cancer-Environment
Registry compared to the
national population
Wiklund et Sweden 20,025 pesticide applicators Pesticide 90 0.99 (0.80–1.22) SIR
al., 1989 followed up in the Swedish applicators
[18] Cancer Registry from date of
licence until death or 1982,
compared to agricultural
workers
Wiklund and Sweden 140,208 male farmers followed up Farmers 3,987 0.93 (0.90–0.96) SIR
Dich, 1995 in the Swedish Cancer
[17] Environment Registry from 1971
until death or 1987, compared
to all Swedish men
Williams et U.S. 7,518 cancer incidence cases Farmers 37 1.52 (1.07–2.10) Relative odds
al., 1977 including farmers identified
[64] from the Third National Cancer
Survey Interview Study in a
random 10% sample of all
incident invasive tumors
occurring in 3 years in eight
areas compared to total
occupations (census
comparisons)

†
MOR, mortality odds ratio; O/E, observed/expected; OR, odds ratio; PCMR, proportionate cancer mortality ratio; PMR, proportion-
ate mortality ratio; RR, relative risk; SIR, standardized incidence ratio; SMR, standardized mortality ratio; SPR, standardized propor-
tional ratio; TCDD, 2,3,7,8-tetrachlorodibenzo-p-dioxin.
*Significant excess risk, P < 0.05.
**Significant excess risk, P < 0.01.
***Significant excess risk, P < 0.001.
 Prostate Cancer in Pesticide Applicators 109

TABLE III. Case-Control Studies Relating Prostate Cancer Risks and Pesticide Exposure or
Exposure to Similar Chemicals†

Cases of Exposure OR
Reference Country prostate cancer Controls assessment (95% CI) Comments

Alavanja U.S. 204 agricultural 832 controls, Extension agents 1.02 (0.69–1.49) No trend due to
et al., 1988 extension agents other causes years worked
[28] from the U.S. than cancer as agents, P
Department of value for
Agriculture trend 0.485
(USDA) mortality linear
file, deceased
1970–1979
Alavanja U.S. 40 forest and soil 160 other Forest 1.5 Pesticides not
et al., 1989 conservationists causes than conservationists 1.0 specified, P
[29] from the USDA, cancer Soil value for
deceased 1970–1979 conservationists linear trend,
0.05 and 0.26
Aronson Canada 449 histological cases, 553 other Pesticide applicators, Data on
et al., (Montreal) confirmed from causes than partially adjusted 1.60 (0.91–2.81) cadmium
1996 [13] hospitals 1979–1985 cancer Fully adjusted 1.09 (0.57–2.08) compounds in
this survey
too scarce to
provide a
meaningful
analysis
Checkoway U.S. 40 cases age 50 64 with Farmers 75% of cases
et al., 1987 years or more benign compared to
[65] diagnosed at the prostatic 38% of controls
North Carolina hyperplasi reported farming
Memorial Hospital, work as occupation
1984–1985
Dosemeci U.S. 228 African-American 3,093 other Farmers 1.39 (1.2–1.6)
et al., farmers from 21 causes of 1.40 (1.3–1.5)
1994 [66] states, 891 cases death
from three 13,620
southeastern states, controls, d:o
farm-related
occupations; death
certificates for
1984–1991
Franceschi et Italy 42 farmers below age 119 Farmers 0.9 (0.6–1.4) Multisite study
al., 1993 80 from hospitals, nonfarmers
[67] collected 1985–1991 with other
causes of
death
Le Marchand U.S. (Hawaii) 454 cases from the 899 other Farmers 1.2 (0.7–2.0)
et al., 1991 Hawaii Tumor causes of
[68] Registry 1981–1983 death
(27 were farmers)

†
Studies using controls with other cancer diagnoses are not included. OR, odds ratio.
*Significant excess risk, P < 0.05.
**Significant excess risk, P < 0.01.
***Significant excess risk, P < 0.001.

association between the use of fertilizers and the risk
of prostate cancer.
Hormonal Factors
Androgens, e.g., testosterone, can influence the risk
of prostate cancer. High serum levels of testosterone
among young blacks might be associated with an el-
evated risk of prostate cancer [79]. African-Americans,
who have the highest reported risk of prostate cancer
in the world, also have 10–15% higher concentrations
of circulating testosterone than their white counter-
parts [79]. The prostate is also sensitive to estrogens
[80–82], and there is some evidence that certain pesti-
110 Dich and Wiklund
cides, e.g., organochlorine compounds such as DDT,
may cause weak estrogenic activity. Both in vivo and
in vitro studies confirm that TCDD and related com-
pounds exhibit a broad spectrum of antiestrogenic ef-
fects [83,84]. The consequences, if any, on prostate can-
cer remain unclear.
Other Factors
Dietary factors, alcohol, smoking habits, low physi-
cal activity, and genetic factors have been suggested
by several authors to influence the risk of prostate
cancer [68,85–91]. Farming households have on aver-
age considerably lower expenditures on alcohol
[17,92]. Pesticide applicators and farmers smoke con-
siderably less than the general Swedish population
[18,91]. However, it is not possible to draw any con-
clusions with respect to how these factors have influ-
enced the results.
CONCLUSIONS
Several incidence and mortality studies have found
an association between farming and prostate cancer,
and in this study an increased risk among pesticide
applicators was found. Pesticide applicators are more
exposed to pesticides than farmers in general. The in-
creasing incidence of prostate cancer worldwide, how-
ever, calls for intensified research on etiological factors
and studies on exposure in groups with elevated in-
cidence of prostate cancer.
ACKNOWLEDGMENTS
The financial support of the Cancer Society of
Stockholm is greatly appreciated.
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