Non-cancer health effects of pesticides

Systematic review and implications for family doctors

M. Sanborn, MD CCFP FCFP

Assistant Clinical Professor in the Department of Family Medicine at McMaster University in Hamilton, Ont

K.J. Kerr, MD DIP ENV HEALTH

Lecturer in the Department of Family and Community Medicine at the University of Toronto in Ontario

L.H. Sanin, MD MPH ScD

Professor in the Department of Public Health Sciences at the Universidad Autonoma de Chihuahua in Mexico

D.C. Cole, MD MSc FRCPC

Associate Professor of Medicine in the Department of Public Health Sciences at the University of Toronto

K.L. Bassil, MSc

Doctoral candidate in the Department of Public Health Sciences at the University of Toronto

C. Vakil, MD CCFP FCFP

Author information ► Copyright and License information ►

This article has been cited by other articles in PMC.

Abstract
Pesticides include all classes of chemicals used to kill or repel insects, fungi, vegetation, and
rodents.1,2 It is well accepted that acute poisonings cause health effects, such as seizures,
rashes, and gastrointestinal illness.1–4 Chronic effects, such as cancer and adverse
reproductive outcomes, have also been studied extensively, and the results have been
interpreted in various ways as evidence that pesticides aresafe or area cause for concern
because they can be detrimental to human health. Bylaw debates across Canada have focused
public attention on the cosmetic (non-commercial crop) uses of pesticides and the attendant
potential risks of chronic low-level exposure.

Family physicians need evidence-based information on the health effects of pesticides to

guide their advice to patients and their involvement in community decisions to restrict use of
pesticides. A systematic review by the Ontario College of Family Physicians’ Environmental
Health Committee was done as a basis for informing family physicians’ approach to
disseminating information on pesticides to patients and communities.5

This article reports on a systematic review of articles published between 1992 and 2003 on 4
non-cancer chronic health effects thought to be associated with exposure to pesticides:
dermatologic, neurologic, reproductive, and genotoxic effects. Cardiovascular, respiratory,
and learning disability outcomes were not included in the review because of resource
constraints. Findings on pesticides and cancer outcomes are reported in another article.6

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DATA SOURCES

Primary peer-reviewed studies were located using PreMedline, MEDLINE, and LILACS
(Spanish- and Portuguese-language articles) databases. All searches included the key MeSH
heading “pesticides” combined with the MeSH heading for the health effects under study.
Reviewers systematically scanned the references of all articles for additional relevant studies.

Study selection

The 3 criteria for inclusion in the assessment were being peer reviewed, being a study of
human health effects related to pesticide exposure, and being published between 1992 and
2003. A systematic review done in 1993 had covered pesticide health effect studies up to
1991.7 A total of 150 studies were retrieved by the search for the 4 categories of health effects
(Table 1). Two independent reviewers each filled out 5-page Data Extraction Forms for each
study. A 7-point Likert-type Global Methodological Quality Assessment Scale was used to
assess all papers; 26 papers scored <4 out of 7 and were excluded.

Table 1
Summary of studies reviewed

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SYNTHESIS

Dermatologic effects

Skin is the primary route of exposure to pesticides for sprayers, handlers, and people using
repellants. Excluding acute poisonings, contact dermatitis is thought to be the most common
health effect of pesticides, through either irritant or allergic mechanisms.8 Along with eye
injuries, it is the health effect most likely to be seen in the office2 and might be the only
indicator of exposure.

In the 10 studies reviewed9–18 (none from Canada), it was difficult to assess the prevalence of
skin disorders attributable to pesticides. In agricultural workers with contact dermatitis,
sensitization to both plant material and pesticides was documented,9,16 but most study designs
did not allow attribution of rashes specifically to pesticide exposure. One study that used a
biomarker for pesticide exposure found a dose-response relationship between dermatitis and
years of fungicide exposure or poor application practices13; 61% of pesticide-exposed
agricultural workers and 31% of controls had dermatitis (P < .001).13 Pet groomers who gave
more than 75 pyrethrin flea treatments per year had more rashes (odds ratio [OR] 2.04, 95%
confidence interval [CI] 1.02 to 4.09) and more eye symptoms (OR 4.75, 95% CI 1.14 to
18.23) than those who gave fewer treatments.10

Neurotoxicity

Long-term effects of pesticides on the nervous system include cognitive and psychomotor
dysfunction, and neurodegenerative and neurodevelopmental effects. Pesticide poisonings
result in well-described acute and chronic neurotoxic syndromes.19 Chronic effects from low
or moderate exposures have been less well documented.

Our systematic review began with 4 relevant studies, including a metanalysis on Parkinson
disease (PD) and pesticide exposure20; 41 primary studies21–62 were of adequate quality. Most
studies analyzed covariates that might affect nervous system function. Differentiating
between the effects of chronic or cumulative exposure and current intense exposure can be
difficult. Unfortunately for many exposed populations (eg, Ecuadorian farm families29,30),
mixed past poisoning, cumulative exposure, and current work and home exposures are
overlaid.

Maternal, in-utero, and early childhood exposures are likely all involved in producing
neurodevelopmental effects in preschool children in pervasive exposure situations, such as
Mexican valley agriculture.40 Only 2 studies of effects including children were
found,40,42 despite considerable concern about the effects of pesticide exposure on sensitive
populations, such as inner-city children.4

Most studies documented mixed pesticide exposures. Cross-sectional studies often included
exposure biomarkers, such as herbicide or alkyl phosphates in urine or acetylcholinesterase
levels in blood. Some studies were exceptional in documenting specific exposures, for
example, fumigants.28

General neurotoxic morbidity. General malaise and mild cognitive dysfunction might be the
earliest neurotoxic responses to pesticide exposure.62 Most studies using validated
questionnaires and performance tests found an increased prevalence of symptoms or mood
changes, as well as alterations in neurobehavioural performance and cognitive function.

Studies of the mental and emotional effects of pesticides found associations for current minor
psychiatric morbidity,27 depression,55 suicide among Canadian farmers,49 and death from
mental disorders,60particularly neurotic disorders in women. Keifer et al42 found substantially
higher rates of mental and emotional symptoms in residents (including adolescents) exposed
to spray-plane drift compared with those not exposed.

Associations between previous pesticide poisonings, particularly from organophosphates and

carbamates, and decreases in current neurobehavioural function were most consistently
positive. Those with greater exposures (eg, termiticide applicators31 or farmers handling
concentrates50) also showed more consistent decreases in function. Together, these studies
provide important evidence of the subclinical effects of pesticides on the nervous system.
These effects might become clinically manifest in a few cases.
Neurodegenerative disease

Most of these studies examined mixed occupational exposures. Some focused on herbicides.
Health outcomes varied from PD on clinical examination through adjusted incidence of
hospitalization for PD to deaths from PD. All found positive associations between exposure
and PD. Combined with the earlier meta-analysis,20 the results of 15 out of 26 studies were
positive for associations between pesticide exposure and PD. These data provide remarkably
consistent evidence of a relationship between PD and past exposure to pesticides on the job
(OR 1.8 to 2.5).

Evidence of other neurodegenerative effects of pesticides is also accumulating. Of 2 studies

on Alzheimer disease, 138 found no association and 124 found an association in men. A study
on amyotrophic lateral sclerosis46 found consistently elevated adjusted ORs associated with
pesticide exposure in both men and women.

Reproductive outcomes

Six distinct groups of reproductive outcomes were chosen for study: birth defects,
fecundability, fertility, altered growth, fetal death, and mixed outcomes.
Birth defects

Fifteen studies from 9 countries63–77 examined associations between pesticides and birth
defects. The studies consistently showed increased risk with pesticide exposure. Specific
defects included limb reductions,64,67,73 urogenital anomalies,68,73,75 central nervous system
defects,68,73 orofacial clefts,74 heart defects,66,67 and eye anomalies.77 The rate of any birth
defect was also increased by parental exposure to pesticides.66–71,74,76 In many studies, there
were multiple exposures. Two studies identified specific pesticides: glyphosate64 and the
pyridil derivatives.69
Time to pregnancy

Eight studies from 6 countries78–85 analyzed associations between pesticide exposure and time
to pregnancy. Data on pesticide exposures and outcome were collected retrospectively by
self-report. Five studies showed positive associations, and 3 showed no association between
pesticide exposure and time to pregnancy. All 3 papers showing no association collected
exposure and outcome information from men only.79–81
Fertility

Fertility refers to the ability to become pregnant in 1 year and includes male and female
factors, such as semen quality and infertility. Twelve studies from 7 countries were
reviewed.86–99 Results were mixed; several studies found no associations between pesticide
exposure and sperm abnormalities. One study found an association between organophosphate
metabolites and sperm sex aneuploidies94; another study found an association between
erectile dysfunction and pesticide exposure.95 One study found an increased risk of infertility
among women who worked with herbicides in the 2 years before attempted conception.98
Altered growth

Low birth weight, prematurity, and intrauterine growth restriction are not only important
determinants of health during the first year of life, but also of chronic diseases of
adulthood.100 Ten studies, mainly from Europe and North America,76,77,101–108 examined
pesticide effects on fetal growth. Seven of these showed positive associations between
agricultural pesticide exposure and altered fetal growth. Two pesticides implicated in the
positive studies were pyrethroids and chlorpyrifos, the latter a commonly used ant-killer now
being phased out because of health effects.
Fetal death

Fetal death includes spontaneous abortion, fetal death, stillbirth, and neonatal death. Results
were consistent across several study designs; 9 of 11 studies64,76,77,109–116 found positive
associations with pesticide exposure. The Ontario Farm Study results suggested critical
windows when pesticide exposure is most harmful. Preconception exposure was associated
with early first-trimester abortions, and post-conception exposure was associated with late
spontaneous abortions.110 In a study from the Philippines,76 risk of spontaneous abortion was 6
times higher in farming households with heavy pesticide use than it was among those using
integrated pest management (which results in reduced pesticide use).
Other reproductive outcomes

Seven studies examined other reproductive outcomes, such as sex ratio, placental quality, and
developmental delay after in-utero exposure.64,107,117–121 A Mexican study115found higher rates
of placental infarction in rural women exposed to organophosphate insecticides; exposure
was biomarker-documented with depressed red blood cell cholinesterase levels. Results on
altered sex ratios were inconsistent.64,114

Genotoxicity

Genotoxicity is the ability of a pesticide to cause intracellular genetic damage. In all reported
studies, it was measured as percent chromosome aberrations per 100 peripheral blood
lymphocytes. Increased frequency of chromosome aberrations was a predictor of increased
cancer rates in a large prospective cohort study (n = 5271) with follow-up for 13 to 23
years.122 Similar studies of associations with reproductive outcomes have not been done.

Important confounders are exposures that cause genetic damage: smoking, alcohol
consumption, diet, caffeine intake, radiation, and mutagenic drugs. The latter are important
since drugs such as methotrexate are now used widely for rheumatoid arthritis and Crohn
disease. Few studies measured all confounders; most excluded smokers and subjects who had
x-rays or took mutagenic drugs during the previous year.
Positive associations between pesticide exposure and elevated percent chromosome
aberrations were found in 11 of 14 studies.123–136 Two studies showing no association had
taken blood samples during low-exposure seasons.128,129 Two studies pointed to synthetic
pyrethrins134 and organophosphates135 as highly genotoxic. Aggregate results from all 14
studies are shown in Figure 1; pesticide exposure doubled the frequency of chromosome
aberrations. In clinical practice, these aberrations could present as spontaneous abortion, birth
defects, sperm abnormalities, or cancer risk.

Figure 1
Percent of chromosome aberrations for 500 control and 529 pesticide exposed subjects in 14
genotoxicity studies compared with the general population

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DISCUSSION

For the 4 non-cancer effects reviewed, the strongest evidence of association with pesticide
exposure was found for neurologic abnomalities, 4 out of 6 reproductive outcomes, and
genotoxicity effects (Table 1).

The most striking feature of the results of this systematic review is the consistency of
evidence showing that pesticide exposure increases the risk of 3 non-cancer health effects:
neurologic, reproductive, and genotoxic effects. The results are consistent with those of other
reviews published before20 and since137,138 this review was completed. Results of dermatologic
studies are less consistent and of poorer quality and indicate the need for a primary care
prevalence study of pesticide-related skin conditions.

Assessment of exposure remains a key problem that is being addressed in newer studies by
enhanced biomonitoring. For example, a cohort of children now being followed
longitudinally had cord-blood levels of several pesticides measured at birth139 and by maternal
air and blood sampling during pregnancy.140The role of genetics in the ability to metabolize
pesticides, which varies widely among ethnic groups,141 is being incorporated into more study
designs41,124,142 and should refine our knowledge and explain some inconsistencies in the
international literature.

Limitations

The major limitation of studies of the health effects of pesticides is their inability to
demonstrate cause-effect relationships. Study subjects cannot be deliberately exposed to
potentially harmful toxins, and few exposure-reduction options are tested in randomized
controlled trials. The evidence generated by well-constructed clinical and epidemiologic
observational studies is the highest level of evidence we can ethically obtain.
The studies reviewed have methodologic problems, such as exposure misclassification and
inadequate exposure assessment (causing mixed results) and recall bias (in retrospective case-
control studies). Unpublished literature on health effects that was not accessed would be
useful to determine whether there is a publication bias toward positive studies. The effect of
unpublished positive or negative studies generated by chemical industry–funded research also
cannot be assessed. Many good-quality studies were found in the review, however, and taken
together, the results provide sufficient cause for family doctors to educate patients and to act
to prevent unnecessary pesticide exposure.

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CONCLUSION

This systematic review provides clear evidence that pesticide exposure increases risk to
human health across a range of exposure situations and vulnerable populations. Public
support for restrictions on pesticide use is growing; 71% of respondents supported
provincewide restrictions in a recent Ontario poll.143 The Canadian Association of Physicians
for the Environment144 and national pediatric and public health groups in Canada and the
United States145–8 have expressed concern about health effects from cosmetic use of pesticides
and recommended that physicians participate in reduction efforts.

Family doctors have a dual role in reducing pesticide exposures. First, during individual
encounters, we can educate patients about pesticide health effects,149 monitor through
exposure histories150 and laboratory tests,151 and advise when we believe the level of exposure
poses a health threat. We should encourage harm reduction through use of protective
equipment when pesticide exposure is necessary. Advice about use of protective equipment is
an important and neglected area of family practice,152 although it is an effective intervention
for reducing pesticide exposure.133,153 Then, in our role as public and community health
advocates, we need to educate the public about the health effects of pesticide use. We need to
reinforce community efforts to reduce cosmetic use of pesticides that can disproportionally
affect children, pregnant women, and elderly people.

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Practice tips based on the review

1. Advise patients to avoid pesticide exposure during critical reproductive periods. This
includes occupational, indoor, lawn, and garden exposure to pesticides.
 For women, the critical period for early spontaneous abortion is before
pregnancy, and for late spontaneous abortion, the first trimester.
 For men, the critical period is the 3 months of spermatogenesis before
conception.
2. Take a pesticide-exposure history from patients who have adverse reproductive
events, such as intrauterine growth restriction, prematurity, inability to conceive in 1
year, or birth defects.
  Birth defects are associated with both maternal and paternal exposure to
pesticides before conception and during the first trimester.
 Most exposures are work related, but transposition of the great vessels is
increased with household exposure.
3. Screen patients with a history of exposure to pesticides for neurologic conditions
(which can be subtle).
 Occupationally exposed adults are at increased risk of neurologic symptoms,
including neurobehavioural changes and Parkinson disease.
4. Use biomonitoring as an effective tool to reduce exposure. Biomonitoring for recent
(within 3 months) organophosphate insecticide exposure is done by ordering red
blood cell cholinesterase tests.2 The test is covered by the Ontario Health Insurance
Plan; in other provinces, it costs $25 to $100, but might be covered for exposed
workers.

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Notes
EDITOR’S KEY POINTS

 Due to the unethical nature of cause-effect studies on pesticide exposure, the growing
body of literature on pesticide health effects cannot be used to establish a cause-effect
relationship between the use of pesticides and non-cancer health effects.
 However, there is consistent evidence in the literature that pesticide exposure does
increase the risk of 3 non-cancer health effects (neurologic, reproductive, and
genotoxic).

POINTS DE REPÈRE DU RÉDACTEUR

 En raison de la nature non éthique des études de type cause-effets sur l’exposition aux
pesticides, on ne peut utiliser les données de plus en plus nombreuses de la littérature
dans ce domaine pour éta-blir une relation de cause à effet entre l’utilisation des
pesticides et les effets sur la santé autres que les cancers.
 Il existe toutefois dans la littérature des preuves abondantes confirmant que
l’exposition aux pesticides augmente le risque de développer trois effets nocifs autres
que cancéreux: effets sur le système nerveux, sur la reproduction et génotoxicité.

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Footnotes
This article has been peer reviewed.

Competing interests

The systematic review was completed with funding from the Laidlaw Foundation and the Ontario College of
Family Physicians. Dr Sanborn, Dr Kerr, and Dr Vakil received honoraria from the Ontario College of
Family Physicians for working on this article. Dr Cole has received funding from the International
Development Research Centre and the Canadian Institutes for Health Research around pesticides but not
for this review. Although Ms Bassil currently works in the Environmental Protection Office at Toronto Public
Health in Ontario, she was not employed there while working on the systematic review. Dr Vakil has
received teaching honoraria from the Ontario College of Family Physicians and the International Joint
Commission Health Professional Task Force.

Contributors

Dr Sanborn, Dr Kerr, Dr Sanin, Dr Cole, Ms Bassil, and Dr Vakil contributed to concept and design of
the study, data analysis and interpretation, and preparing the article for submission.

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