Dermal Exposure Associated with Occupational End Use of Pesticides and the Role of Protective Measures

Abstract

Occupational end users of pesticides may experience bodily absorption of the pesticide products they use, risking possible health effects. The purpose of this paper is to provide a guide for researchers, practitioners, and policy makers working in the field of agricultural health or other areas where occupational end use of pesticides and exposure issues are of interest.
This paper characterizes the health effects of pesticide exposure, jobs associated with pesticide use, pesticide-related tasks, absorption of pesticides through the skin, and the use of personal protective equipment (PPE) for reducing exposure.
Although international and national efforts to reduce pesticide exposure through regulatory means should continue, it is difficult in the agricultural sector to implement engineering or system controls. It is clear that use of PPE does reduce dermal pesticide exposure but compliance among the majority of occupationally exposed pesticide end users appears to be poor. More research is needed on higher-order controls to reduce pesticide exposure and to understand the reasons for poor compliance with PPE and identify effective training methods.

Full text

Review Article
Dermal Exposure Associated with Occupational End Use of Pesticides
and the Role of Protective Measures
Ewan MacFarlane
1
,
*
, Renee Carey
2
, Tessa Keegel
1
,
3
, Sonia El-Zaemay
4
, Lin Fritschi
2
1
Monash Centre for Occupational and Environmental Health, School of Public Health and Preventive Medicine, Monash University, Melbourne, Australia
2
Western Australian Institute for Medical Research, University of Western Australia, Perth, Australia
3
McCaughey Centre, University of Melbourne, Melbourne, Australia
4
School of Population Health, University of Western Australia, Perth, Australia
article info
Article history:
Received 20 March 2013
Received in revised form
29 July 2013
Accepted 31 July 2013
Keywords:
agricultural workers’diseases
occupational exposure
pesticides
protective clothing
skin absorption
abstract
Background: Occupational end users of pesticides may experience bodily absorption of the pesticide
products they use, risking possible health effects. The purpose of this paper is to provide a guide for
researchers, practitioners, and policy makers working in the field of agricultural health or other areas
where occupational end use of pesticides and exposure issues are of interest.
Methods: This paper characterizes the health effects of pesticide exposure, jobs associated with pesticide
use, pesticide-related tasks, absorption of pesticides through the skin, and the use of personal protective
equipment (PPE) for reducing exposure.
Conclusions: Although international and national efforts to reduce pesticide exposure through regulatory
means should continue, it is difficult in the agricultural sector to implement engineering or system
controls. It is clear that use of PPE does reduce dermal pesticide exposure but compliance among the
majority of occupationally exposed pesticide end users appears to be poor. More research is needed on
higher-order controls to reduce pesticide exposure and to understand the reasons for poor compliance
with PPE and identify effective training methods.
Ó2013, Occupational Safety and Health Research Institute. Published by Elsevier. All rights reserved.
1. Introduction
According to the United States Environmental Protection Agency
(EPA), pesticides are defined as substances used to prevent, destroy,
repel, or mitigate any pest ranging frominsects, animals, and weeds
to microorganisms [1]. Occupational end users of pesticides may
experience bodily absorption of the pesticide products they use and
this puts them at risk of possible health effects associated with
pesticide exposure.
The purpose of this paper is to provide a guide for researchers
and practitioners working in the field of agricultural health or other
areas where occupational end use of pesticides and exposure issues
are of interest. Dermal exposure is an important issue for pesticide
applicators [2,3], and the aim of this paper is to describe and
characterize dermal exposure to pesticides among pesticide end
users, and protective measures that mitigate exposure.
2. Health effects of pesticide exposure
Chemical pesticides consist of an active ingredient, the actual
poison, and a variety of additives, which improve the efficacy of its
application and action. Pesticides can be classified or grouped ac-
cording to the target organisms (e.g., insecticides, fungicides, and
herbicides), chemical structure of the compound (e.g., organo-
chlorine, organophosphorus, phenoxy acid herbicides, urea, and
pyrethroids) [4,5], or type of health hazard involved [6].
Health effects resulting from pesticide exposure vary according
to the individual pesticide involved and may be the result of
exposure via the dermal, oral, or inhalational routes, however,
dermal exposure is the most relevant route of exposure for pesti-
cide applicators [2,3]. Health effects may be classified as acute or
chronic, based on the period it takes for symptoms of toxicity to
develop.
*Corresponding author. MonCOEH, School of Public Health and Preventive Medicine, Monash University, The Alfred Hospital, Commercial Road, Melbourne 3004,
Australia.
E-mail address: Ewan.MacFarlane@monash.edu (E. MacFarlane).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0)
which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Contents lists available at ScienceDirect
Safety and Health at Work
journal homepage: www.e-shaw.org
2093-7911/$ esee front matter Ó2013, Occupational Safety and Health Research Institute. Published by Elsevier. All rights reserved.
http://dx.doi.org/10.1016/j.shaw.2013.07.004
Safety and Health at Work 4 (2013) 136e141

Acute toxicity is normally the result of a single exposure and the
symptoms are seen within a comparatively short time of exposure,
usually within hours or days. Liquid formulations are generally
more hazardous than solid state products because it is more diffi-
cult for a solid to pass through the skin or mucous membrane [7].
Acute health effects may include irritation of skin or eyes or res-
piratory irritation.
Chronic effects may include neurological and mental health
effects, mutagenic or reproductive effects, endocrine effects, and
cancer. For chronic effects, the level of evidence on which a deter-
mination of toxicity is made is often poor. Although acute effects
are relatively easy to demonstrate in animal experiments, or are
seen after poisonings, the chronic effects of pesticides are more
difficult to study. Toxicological studies can provide information
regarding mechanisms and effects in animals, but epidemiological
studies of exposure in humans are needed in order to establish
causation. However, many epidemiological studies combine expo-
sure to all pesticide groups together, resulting in a dilution of effect,
because it is not plausible that such a diverse collection of chem-
icals would have the same effect. By contrast, studies examining
individual pesticide groups may not provide sufficient study power
for definitive statements. Most studies categorize pesticide expo-
sure as a dichotomous variable (exposure or no exposure) with no
evidence on level or frequency [8]. As well as the misclassification
of exposure, there can be misclassification of outcome, such as
when all cancers are grouped together rather than examining the
risk of cancer at specific sites [9].
3. Occupational pesticide users ejobs associated with
pesticide use
Occupational end users of pesticides include workers who are
involved in the application of pesticides or who re-enter treated
areas shortly after pesticide application. Such workers are mostly
classifiable as (1) agricultural workers, (2) structural/urban pest
controllers, or (3) municipal, public utilities, parks and gardens
workers, and foresters. Each of these groups has distinctive pesti-
cide exposure profiles due to differences in the context and purpose
of pesticide use.
Agricultural workers are one of the major groups of pesticide-
exposed workers. The types of pesticide, frequency of use, and
application method vary according to the farm type and the com-
modities being grown. Although agricultural activity accounts for
the majority of occupational pesticide use [10,11], farm pesticide
use is generally an intermittent, seasonal task and only one of the
wide range of tasks undertaken by farm workers [10,12]. Conse-
quently, the exposure frequency and total exposure time among
most farm workers are typically lower than for pesticide applicators
in other industries [13]. Dedicated agricultural pesticide applicators
have more frequent exposure than farm operators but may have
fewer years of pesticide use [14]. Many of the published cohort
studies of pesticide exposure and health effects have focused spe-
cifically on agricultural workers who are licensed pesticide users
(e.g., [15e19]). However, there is evidence suggesting that pesticide
exposure may not be universal among farm workers, and a large
proportion of workers in the farming sector may not be exposed to
pesticides directly [20,21].
Dedicated nonagricultural pest control operators (structural or
urban pest controllers) comprise a comparatively small fraction of
the pesticide-exposed workforce, however, their exposure pattern
is systematically different from that of agricultural pesticide ap-
plicators [22].These nonagricultural pest controllers are exposed
on a more regular basis because the application of pesticides is a
central task of their job [23,24]. Another important difference is
that nonagricultural pest controllers’work is predominantly
associated with built environments and applying pesticides in-
doors, including restricted spaces [25].
Other occupational pesticide users include turf workers, such as
greenkeepers and other sports facilities caretakers, ornamental
gardeners, and park workers who may use weedicides, fungicides,
and insecticides to maintain turf and gardens [26]. Herbicide use is
characteristic of workers involved in maintenance of public infra-
structure and in particular clearance of vegetation from linear
infrastructure corridors such as roads, railway lines, and overhead
electrical distribution lines (line clearance) [26]. Line clearance and
other vegetation control tasks using herbicides may also be com-
mon among forestry workers [27].
4. Pesticide-related work tasks
The principal route of exposure with end use of pesticides is
through skin contact [3]. Respiratory entry appears to be more
limited, likely due to low vapor pressures of many pesticides
[28,29].
Assessing exposure to pesticides in real-life situations is diffi-
cult. It is seldom possible to assess pesticide exposure by direct
biological measurement in large epidemiological studies, so pesti-
cide exposure has often been assessed using surrogates of expo-
sure, such as self-reported questionnaire data, leading to imprecise
exposure assessment [13,29]. Exposure estimates based on indi-
vidual-use records have been shown to result in substantial dose
misclassification [30e32].
In general, pesticide end use involves the following basic
sequential stages: (1) mixing and loading, (2) application, and (3)
clean-up. Although exposure levels may vary widely between in-
dividual operators, mixing and loading are the tasks associated with
the greatest intensity of exposure. It is during the mixing/loading
phase that workers are exposed to concentrated product and when
high exposure events (e.g., spills) are most likely [3,28]. However,
because pesticide application is typically a longer duration task than
mixing and loading, total contamination incurred while applying
pesticide may exceed mixing and loading [29]. There is also evidence
that equipment cleaning at the end of the task may also be an
important source of exposure, at least in some workers [29].
The amount of pesticide deposited on the operator’s skin de-
pends on the type of application equipment used [3,10,29]. Hand
spraying with wide-area spray nozzles is associated with greater
operator exposure than narrowly focused spray nozzles [31]. When
pesticides are applied using tractors, spraying equipment mounted
directly on the tractor is associated with a higher degree operator
exposure than when the sprayequipment is attached to a trailer [3].
Due to differences in individual work habits, the distribution of
pesticide deposition on different parts of the operator’s body is also
subject to variation [3]. Several studies of body surface contami-
nation in agricultural applicators show that the hands and forearms
are the part of the worker’s body subject to the greatest pesticide
contamination during preparation and application of pesticides
[3,13,29]. However, the thighs, forearms, chest, and back may also
be subject to significant contamination [3,13].
Cleaning of pesticide application equipment may also be a
source of operator exposure. Equipment cleaning is an important
farm pesticide task, and time devoted to cleaning may be a sub-
stantial proportion of the mix/load/apply/clean-up sequence [3,29].
In a study of workers’whole-body dermal contamination, Baldi
et al [29] demonstrated that equipment cleaning may contribute
appreciably to workers’cumulative daily dermal exposure and, as
with other pesticide tasks, considerable variation was observed
between workers.
Applying pesticides to livestock, particularly sheep dipping, is a
source of occupational pesticide exposure on livestock farms but
E. MacFarlane et al / Dermal Pesticide Exposure 137

there are relatively few published data about worker exposures
during this task. Published data from the UK suggest that like other
applicators, skin absorption is the main route of exposure during
sheep dipping and particularly associated with handling of con-
centrates, and to a lesser extent splashing with dilute dip as animals
pass through the bath. Inhalation does not appear to be an
important route of exposure [33]. Given that dip baths need to be
regularly topped up with concentrate, handling is frequent and the
potential for skin contamination among those workers who handle
the concentrate is high [33].
Unexpected events are also an important source of surface
contamination for applicators and the exposure levels associated
with these events can result in acute and long-term health effects
[34]. Such events include spills and splashes that may lead to high
personal exposure and can overwhelm usual protective measures.
In the Agricultural Health Study (USA) 14% of farmers licensed to
apply restricted pesticides reported ever having had such an
exposure event [34]. The unexpected problems that lead to high
exposure events are most common during mixing/loading and
application phases but may also occur during clean-up [29].
Although workers who prepare and apply pesticides have been
the main focus of research to date, workers re-entering sprayed
fields after pesticide treatment may also be exposed, sometimes to
a significant degree [20,35,36]. There is evidence that re-entry
workers may have pesticide absorption greater even than appli-
cators, possibly because safety training and use of personal pro-
tective equipment (PPE) are less and their duration of exposure
may be greater than that of applicators [20,36,37]. Re-entry
exposure is a particular problem if workers re-enter treated fields
very soon after pesticide application [28]. Field workers may also
be inadvertently exposed to spray drift from neighboring fields,
and overexposure events of this kind, each involving groups of
workers, have been documented [11,38]. An Australian field study
conducted in the early 1990s found 6% inhibition of erythrocyte
cholinesterase in workers re-entering cotton fields for weed
removal after aerial spraying [35]. Although the degree of cholin-
esterase inhibition was not associated with symptoms in this
study, the findings were statistically significant and demonstrate
the principle that re-entry workers are at risk of pesticide
absorption.
There is a lack of published data about pesticide exposure
among nonagricultural pest controllers. A survey of Australian
termite control operators showed that use and maintenance of
protective equipment was poor and the frequency of splashes and
spills was high. Hands and the lower part of the body received
most surface contamination and, although the wearing of appro-
priate gloves may protect the hands, the legs, and abdomen are
less protected by the standard clothing used [25]. In the same
study, cholinesterase inhibition monitoring indicated that these
workers did appear to have significant pesticide absorption [39].
There is a limited published literature on exposure in turf
pesticide applicators. As with other pesticide exposed workers,
skin deposition appears to be the most important route of expo-
sure. Although deposition on the hands remains important, there
is a consistency of evidence that in these workers the majority of
body surface deposition may occur on the lower body [40,41].
Therefore protective clothing in addition to gloves, particularly
covering the feet, legs, and abdomen, may be especially important
in this group [31,40,41].Type of spray nozzle may also be an
important factor modifying applicator exposure, with wide-angle
nozzles causing greater exposure to the operator [31,32]. Unlike
other occupational pesticide use situations, for lawn applicators
spraying appears to be the task associated with highest exposure
and mixing and loading may be less important sources of expo-
sure. This difference may have important implications for exposure
and risk assessment in this group [32]. Exposure in forestry
workers is complicated by additional factors unique to the forestry
work environment such as height of vegetation and terrain con-
ditions [27].
5. Absorption through the skin
Pesticides may be absorbed through the layers of the epidermis
into the body [42,43]. The rate of penetration of active and inert
pesticide agents varies according to a range of biological and
environmental factors. Rates of absorption for pesticides are
generally estimated through in vitro and in vivo human and animal
testing [44]. There have also been attempts to describe percuta-
neous absorption through the development of mathematical
models incorporating a range of variables obtained from in vitro
and in vivo tests, such as age, anatomical site, ambient temperature,
humidity, and pesticide concentration [44e46].
Pesticide formulations vary in ability to be absorbed through the
skin [47]. For example emulsifiable concentrates are more readily
absorbed than other formulations [48]. Presence of other material
on the skin, such as the active ingredient of sunscreen, may pro-
mote the penetration of agents through the skin [49,50] and ab-
sorption is affected by temperature and humidity [51].
Rates of absorption through the skin are different for different
parts of the body. Compared to the forearms, pesticides are
absorbed 12 times faster at the site of the genitals, four times faster
at the site of the head, and three times faster at the site of the trunk
[44e46]. Rates of absorption can also be affected by higher skin
temperature. Higher temperatures will also increase cutaneous
blood flow, leading to an amplified circulation of pesticides within
the body [44e46]. Further influencing factors include the number
of follicles, the thickness of the stratum corneum, the sebum
composition, and the distance of blood vessels to the surface of the
skin [52].
Another possible effect of pesticide contact with the skin is that
the agent may remain in the skin itself and can act as a reservoir for
release in the future [44]. Consideration of dermal absorption as
well as the potential reservoir function of the skin should be taken
into account when conducting risk assessments for individual
pesticides [44]. The circumstances of exposure may provide an
indication of the amount of pesticide absorbed [43].
6. Reducing exposure to pesticides
Following the hierarchy of control, the most obvious way to
reduce pesticide exposure is to ban pesticide use. There is a clear
role for governments in the approval of pesticides for use following
strict risk criteria, and in setting strict requirements for control of
their use, and for establishing programs to encourage the substi-
tution of less hazardous alternatives to replace more hazardous
pesticides. Although efforts have been made internationally to ban
the most hazardous pesticides, it is known that in many lower in-
come countries, banned products are widely used [53].
There is a paucity of research investigating the feasibility and
effectiveness of higher-order control measures for pesticide end
users and the inherent nature of the agricultural sector limits the
applicability of higher-order controls. Administrative controls other
than training, such as rotation of workers and other forms of
exposure time limitation, may be feasible in some contexts outside
agriculture. However, the noninstitutional nature of the agricul-
tural industry and large proportion of small businesses in this
sector are likely to limit the practicability of higher-level control
measures, such as engineering and barrier controls in many agri-
cultural workplaces. This is because higher-order control measures
generally rely on environmental modification, which is not as
Saf Health Work 2013;4:136e141138

feasible in the farm environment as it is in a factory or office. The
urban/structural pest control industry is also dominated by small
businesses [22] and workers in this sector characteristically work in
environments over which they do not have structural control.
Institutional level administrative controls may be feasible for pest
controllers employed by local government agencies and for pesti-
cide users in the public infrastructure sector, although these
comprise a minority of pesticide users [21].
Taking into consideration these issues, much of the re-
sponsibility falls to the individual worker to use PPE and use it
correctly. In the next sections we review the evidence regarding
effectiveness and compliance with PPE.
7. PPE for dermal pesticide exposure
Various types of PPE may be used to limit dermal exposure,
including gloves, long-sleeved clothing, chemical-resistant cover-
alls, boots, and hats. The PPE ultimately used is influenced by the
toxicity of the pesticide being used, the circumstances of exposure,
and the worker’s personal preferences, among other factors [54].At
a minimum, most pesticide products require the use of gloves and
boots [55], and as a general rule, more toxic pesticides require the
use of more PPE.
Different PPE types provide differing levels of protection against
dermal exposure. Gloves were found to provide the most effective
protection against pesticide exposure in Danish greenhouse
workers [56], whereas a study of US citrus farmers found dermal
exposure to be reduced by 27% by the use of gloves, 38% by the use
of coveralls, and 65% by the use of both gloves and coveralls [57].
The effectiveness of PPE also varies according to the protective
features of the PPE itself, the way in which the pesticide is applied,
and the way in which PPE is utilized by workers, such as correct
fitting and maintenance.
The ability of protective clothing to protect against exposure is
primarily influenced by fabric type, including thickness and weight
[58]. One study observed very little to no penetration through
fabrics thicker than 0.8 mm, regardless of other factors [54], with
workpants providing much greater protection than thinner work
shirts [59], In addition, although garments made of both barrier and
non-barrier fabrics have been shown to decrease dermal exposure
[60], greater protection is afforded by waterproof polypropylene
fabrics than by cotton garments [61]. For example, an Italian study
found penetration through cotton clothing to range from 11.2% to
26.8%, whereas penetration through synthetic material was <2.4%
[62], although a study of US citrus farmers found little difference
between synthetic materials and woven garments [63].
PPE effectiveness, in particular penetration of pesticides
through clothing, may be influenced by application method [64e
66], however, the literature is somewhat inconsistent concerning
this question. Stewart and colleagues [67], for example, found low-
pressure and backpack spraying to be associated with greater
penetration through clothing than high-pressure spraying, whereas
Machera and colleagues [68] found low-pressure backpack appli-
cation led to lower penetration than high-pressure hand lance
spraying.
The ways in which PPE is actually used is also an important
determinant of PPE effectiveness. Penetration resistance may be
affected by worker movements that increase the transfer of dusts
and/or liquids through fabric, as well as by sweating [63]. For
example, greater penetration has been observed through parts of a
polyethylene coverall where the movement of the worker is likely
to create friction [68]. In addition, the protective features of PPE are
dependent on proper use. For example, workers who roll their
sleeves up or remove their gloves are at increased risk of dermal
exposure [62].
8. PPE compliance
Evidence suggests that PPE use may be poor among pesticide
end users. An Australian study found that use of clothing that
provided basic skin covering when applying pesticides was far from
universal [69]. The majority of contamination is consistently found
on the hands, therefore, gloves are a key PPE item. In one French
observational study of vineyard workers, <5% of workers wore
gloves during pesticide tasks [3]. A US survey showed that self-
reported PPE usage varied widely between different pesticide
classes. Although gloves were the most commonly reported PPE
item for most pesticide classes and tasks, substantial proportions of
users never used gloves for pesticide tasks (15e55%), and only 25e
30% reported always using gloves for mixing and application [70].
In a study of French vineyard workers [71], 62% wore gloves during
mixing, only 10% wore gloves during application, and 41% wore
gloves during equipment cleaning. It was noted that skin contam-
ination of the hands was high even when gloves were worn, sug-
gesting that improper use, breakthrough permeation, or other
factors may reduce the potential effectiveness of PPE even when it
is used [71]. Use of inappropriate types of gloves has also been
noted as a frequent problem among applicators [70]. It is also
important to note that these published data have come from self-
reported surveys or observation of workers who have volunteered.
In both cases the reported or observed usage rates are likely to
overestimate actual use in general; either because of over-report-
ing, greater diligence under observation, or differential recruitment
of more safety conscious workers.
Few data about protective equipment use in animal pesticide
applicators has been published. In a UK study of sheep dippers,
waterproof boots and trousers were commonly worn but gloves
were used by only 30e50% of workers [33,72]. Australian data
suggest that compliance with personal protective clothing among
Australian sheep dippers may be similarly poor and is likely to be
inadequate to protect users from low-level exposure [73].
Particular pesticide products have specific PPE requirements and
compliance with such requirements has been shown to vary. A study
of the use of restricted pesticides by US dairy farmers, for example,
found that <50% of users fully complied with PPE requirements for 12
of the 15 pesticides studied [74]. Higher toxicity pesticides with more
burdensome PPE requirements were generally associated with the
lowest compliance, with highest compliance demonstrated for those
pesticides requiring the use of gloves only. In addition, for nine of the
pesticides, the majority of applicators reported wearing no PPE dur-
ing application. Another study involving 554 US farm workers found
that less than half of the respondents reported wearing protective
clothing [75], whereas an observational study of US orchard farmers
found coveralls to be worn by a minority of workers involved in
mixing and applying pesticides [76].
Studies have found correlations between the extent of worker
training and compliance with PPE requirements. For example,
Australian farmers who received formal farm chemical training
were more likely to report the use of skin protective equipment
(including gloves, clothing, and boots) when mixing and applying
pesticides [69]. Similar relationships have been found in the US [75]
and UK [77].Afinal point to note is that the use of protective
clothing may also confer a false sense of security on workers and
may lead to behavior that can result in increased exposure [78].
9. Methods to increase PPE usage
By their nature, pesticide tasks are generally undertaken in the
field or in other environments and contexts that are not amenable
to the sorts of institutional or organizational-level controls that
may be possible, for example, in a factory workforce. Therefore PPE,
E. MacFarlane et al / Dermal Pesticide Exposure 139

specifically protective clothing, remains a key control measure for
managing dermal exposure. Use of PPE in the farm workplace is
governed mainly by voluntary behavior [79], and recent research
suggests that factors influencing the use of personal protective
measures include availability of PPE in the workplace, perceived
control, previous adverse health consequences of pesticide expo-
sure, and having had specific safety training [55,75,77,79,80].
Evidence for the effectiveness of safety training in the promo-
tion of personal protection is contradictory [70], and it is likely that
local factors including the quality and content of safety training and
the receptivity of the audience may vary in different local contexts.
A US dairy farmer study found that an educational session
regarding the hazards associated with pesticides increased the use
of PPE, although it did not lead to complete compliance with PPE
requirements [80]. Thus, even with training in the use of and risks
surrounding pesticides, some pesticide workers may still neglect to
abide fully by recommendations for PPE [77]. Compounding this is
the fact that not all workers receive training, with the literature
indicating that approximately half of all pesticide users may not
have had training in pesticide safety [69,77,81]. Reynolds et al [70]
also found that use of PPE, including gloves, was more likely when
odorous agrochemicals were used, irrespective of the toxicity of the
product, and suggested the addition of odorant to the more toxic
pesticides may be an effective intervention strategy.
One likely reason for the lack of PPE worn by workers is thermal
comfort. As the protection afforded by protective clothing in-
creases, the breathability of the fabric is generally decreased,
meaning it is less comfortable for use in warm conditions [54].
Therefore, although pesticide workers may appreciate the protec-
tive benefits of PPE, they may avoid using it because of physical
discomfort [58]. Pesticide workers may also view the use of PPE as
cumbersome and unnecessary [81], with farmers who consider
themselves too busy to use PPE during pesticide application less
likely to actually use it [74]. Inclination to use PPE has been shown
to be related to the training that pesticide users receive [69], sug-
gesting that if workers are not aware of the risks, they may be less
likely to view PPE as important.
Use of PPE is also dependent on its availability in the workplace
[75] and although employers are legally required to provide PPE to
their workers [82], compliance is not guaranteed. A US study found
that only 41.8% of farm workers were provided with PPE [75],
whereas another reported estimates ranging from 35.3% to 84.6%
for the provision of different types of PPE, with long-sleeved shirts,
gloves, and boots most frequently being provided [83]. Lack of
availability may be a particular issue for migrant and minority
workers [81], with 36.8% of Hispanic workers being provided with
PPE, compared to 83.3% of white workers [75].
10. Discussion
Use of pesticides is widespread in several different industries
and exposure presents a significant health risk to workers involved
in the end use of pesticides. The majority of pesticide absorbed into
the body comes from dermal exposure, and PPE in the form of
appropriate gloves and clothes has been shown to reduce absorp-
tion. However, compliance among the majority of occupationally
exposed pesticide end users appears to be poor. The reasons for
poor compliance are not clear and, although training appears
promising, there is poor understanding of the delivery modes,
content, and teaching methods that are most effective.
Conflicts of interest
The authors’have no conflicts of interest to report.
References
[1] Environmental Protection Agency (USA). Pesticide industry sales and usage:
1998 and 1999 market estimates. Washington DC: USEPA; 2002.
[2] van Hemmen JJ, Brouwer DH. Assessment of dermal exposure to chemicals. Sci
Total Environ 1995;168:131e41.
[3] Lebailly P, Bouchart V, Baldi I, Lecluse Y, Heutte N, Gislard A, Malas J-P.
Exposure to pesticides in open-field farming in France. Ann Occup Hyg
2009;53:69e81.
[4] Benavides FG, Benach J, Muntaner C, Delclos GL, Catot N, Amable M. Associ-
ations between temporary employment and occupational injury: what are the
mechanisms? Occup Environ Med 2006;63:416e21.
[5] Alavanja MC, Hoppin JA, Kamel F. Health effects of chronic pesticide exposure:
cancer and neurotoxicity. Annu Rev Public Health 2004;25:155e97.
[6] World Health Organization. The WHO recommended classification of pesti-
cides by hazard and guidelines to classification 2009. Geneva (Switzerland):
World Health Organisation; 2010.
[7] Reifenrath WG. Enhanced skin absorption and fly toxicity of permethrin in
emulsion formulation. Bull Environ Contam Toxicol 2007;78:299e303.
[8] Wirdefeldt K, Adami HO, Cole P, Trichopoulos D, Mandel J. Epidemiology and
etiology of Parkinson’s disease: a review of the evidence. Eur J Epidemiol
2011;26(Suppl 1):S1e58.
[9] Boffetta P, Mundt KA, Adami HO, Cole P, Mandel JS. TCDD and cancer: a critical
review of epidemiologic studies. Crit Rev Toxicol 2011;41:622e36.
[10] Curwin B, Hein M, Sanderson W, Barr DB, Heederik D, Reynolds SJ, Ward EM,
Alavanja MC. Urinary and hand wipe pesticide levels among farmers and
nonfarmers in Iowa. J Expo Sci Environ Epidemiol 2005;15:500e8.
[11] Calvert GM, Karnik J, Mehler L, Beckman J, Morrissey B, Sievert J, Barrett R,
Lackovic M, Mabee L, Schwartz A, Mitchell Y, Moraga-McHaley S. Acute
pesticide poisoning among agricultural workers in the United States, 1998-
2005. Am J Ind Med 2008;51:883e98.
[12] van Drooge HL, Groeneveld CN, Schipper HJ. Data on application frequency of
pesticide for risk assessment purposes. Ann Occup Hyg 2001;45(Suppl 1):
S95e101.
[13] Arbuckle TE, Burnett R, Cole D, Teschke K, Dosemeci M, Bancej C, Zhang J.
Predictors of herbicide exposure in farm applicators. Int Arch Occup Environ
Health 2002;75:406e14.
[14] Alavanja MC, Sandler DP, McDonnell CJ, Lynch CF, Pennybacker M, Zahm SH,
Mage DT, Steen WC, Wintersteen W, Blair A. Characteristics of pesticide use in
a pesticide applicator cohort: the Agricultural Health Study. Environ Res
1999;80:172e9.
[15] Blair A, Sandler DP, Tarone R, Lubin J, Thomas K, Hoppin JA, Samanic C, Coble J,
Kamel F, Knott C, Dosemeci M, Zahm SH, Lynch CF, Rothman N, Alavanja MC.
Mortality among participants in the agricultural health study. Ann Epidemiol
2005;15:279e85.
[16] Fleming LE, Bean JA, Rudolph M, Hamilton K. Mortality in a cohort of licensed
pesticide applicators in Florida. Occup Environ Med 1999;56:14e21.
[17] Sperati A, Rapiti E, Settimi L, Quercia A, Terenzoni B, Forastiere F. Mortality
among male licensed pesticide users and their wives. Am J Ind Med 1999;36:
142e6.
[18] Blair A, Sandler D, Thomas K, Hoppin JA, Kamel K, Coble J, Lee WJ, Rusiecki J,
Knott C, Dosemeci D, LynchCF Lubin J, Alavanja M. Disease and injury among
participantsin the Agricultural Health Study. J Agric Saf Health 2005;11:141e50.
[19] Bonner MR, Lee WJ, Sandler DP, Hoppin JA, Dosemeci M, Alavanja MC.
Occupational exposure to carbofuran and the incidence of cancer in the
Agricultural Health Study. Environ Health Perspect 2005;113:285e9.
[20] Coronado GD, Thompson B, Strong L, Griffith WC, Islas I. Agricultural task and
exposure to organophosphate pesticides among farmworkers. Environ Health
Perspect 2004;112:142e7.
[21] MacFarlane E, Glass D, Fritschi L. Is farm-related job title an adequate surro-
gate for pesticide exposure in occupational cancer epidemiology? Occup En-
viron Med 2009;66:497e501.
[22] MacFarlane E, Benke G, Goddard D, Sim M. Urban pest control operators in
Australia. Occup Environ Med 2007;64:422e7.
[23] Wang HH, MacMahon B. Mortality of pesticide applicators. J Occup Med
1979;21:741e4.
[24] MacFarlane E, Benke G, Del Monaco A, Sim MR. Cancer incidence and mor-
tality in a historical cohort of Australian pest control workers. Occup Environ
Med 2009;66:818e23.
[25] Cattani M, Cena K, Edwards J, Pisaniello D. Potential dermal and inhalation
exposure to chlorpyrifos in Australian pesticide workers. Ann Occup Hyg
2001;45:299e308.
[26] MacFarlane E, Benke G, Del Monaco A, Sim MR. Causes of death and incidence
of cancer in a cohort of Australian pesticide-exposed workers. Ann Epidemiol
2010;20:273e80.
[27] Green LM. A cohort mortality study of forestry workers exposed to phenoxy
acid herbicides. Br J Ind Med 1991;48:234e8.
[28] Burns C, Mahlburg W, Dutra JPJ. Pesticide exposure among farm workers.
Environ Res 2007;105:285e8.
[29] Baldi I, Lebailly P, Jean S, Rougetet L, Dulaurent S, Marquet P. Pesticide
contamination of workers in vineyards in France. J Expo Sci Environ Epidemiol
2006;16:115e24.
[30] Harris SA, Corey PN, Sass-Kortsak AM, Purdham JT. The development of a new
method to estimate total daily dose of pesticides in professional turf
Saf Health Work 2013;4:136e141140

applicators following multiple and varied exposures in occupational settings.
Int Arch Occup Environ Health 2001;74:345e58.
[31] Harris SA, Sass-Kortsak AM, Corey PN, Purdham JT. Development of models to
predict dose of pesticides in professional turf applicators. J Expos Anal Environ
Epidemiol 2002;12:130e44.
[32] Harris SA, Sass-Kortsak AM, Corey PN, Purdham JT. Pesticide exposures in
professional turf applicators, job titles, and tasks performed: implications of
exposure measurement error for epidemiologic study design and interpre-
tation of results. Am J Ind Med 2005;48:205e16.
[33] Buchanan D, Pilkington A, Sewell C, Tannahill S, Kidd M, Cherrie B, Hurley J.
Estimation of cumulative exposure to organophosphate sheep dips in a study
of chronic neurological health eVects among United Kingdom sheep dippers.
Occup Environ Med 2001;58:694e701.
[34] Alavanja MC, Sprince NL, Oliver E, Whitten P, Lynch CF, Gillette PP, Logsden-
Sacket N, Zwerling C. Nested case-control analysis of high pesticide expo-
sure events from the Agricultural Health Study. Am J Ind Med 2001; 39:
557e63.
[35] Clarke L, Churches T. Pesticide exposure in cotton chippers in the Gwydir
Valley 1991-92. Moree (Australia): Australian Centre for Agricultural Health
and Safety; 1992.
[36] Strong LL, Thompson B, Coronado GD, Griffith WC, Vigoren EM, Islas I. Health
symptoms and exposure to organophosphate pesticides in farmworkers. Am J
Ind Med 2004;46:599e606.
[37] Ward MH, Prince JR, Stewart PA, Zahm SH. Determining the probability of
pesticide exposures among migrant farmworkers: results from a feasibility
study. Am J Ind Med 2001;40:538e53.
[38] O’Malley M, Barry T, Ibarra M, Verder-Carlos M, Mehler L. Illnesses related to
shank application of metam-sodium, Arvin, California, July 2002. J Agromed
2005;10:27e42.
[39] Dyer SSM, Cattani MM, Pisaniello DDL, Williams FFM, Edwards JJW. Peripheral
cholinesterase inhibition by occupational chlorpyrifos exposure in Australian
termiticide applicators. Toxicology 2001;169:177e85.
[40] Slocum AC, Shern LC. Spray deposition patterns during simulated work ac-
tivities by lawn care specialists. J Environ Sci Health B 1991;26:259e78.
[41] Cowell JE, Lottman CM, Manning MJ. Assessment of lawn care worker expo-
sure to dithiopyr. Arch Environ Contam Toxicol 1991;21:195e201.
[42] Pesticides Liden C. In: Johansen JD, Frosch PJ, Lepoittevin J-P, editors. Contact
dermatitis. Berlin (Germany): Springer; 2010. p. 927e36.
[43] Routt Reigart J, Roberts JR. Recognition and management of pesticide poi-
sonings. Washington DC: US Environmental Protection Agency; 1999.
[44] Kielhorn J, Melching-Kollmuss S, Mangelsdorf I. Dermal Absorption. Geneva
(Switzerland): United Nations Environment Programme, the International
Labour Organization & the World Health Organization; 2006.
[45] Wester RC, Maibach HI, Bucks DA, Aufrere MB. In vivo percutaneous absorp-
tion of paraquat from hand, leg, and forearm of humans. J Toxicol Environ
Health 1984;14:759e62.
[46] Poet TS. Assessing dermal absorption. Toxicol Sci 2000;58:1e2.
[47] Carrico RM, Coty MB, Goss LK, Lajoie AS. Changing health care worker
behavior in relation to respiratory disease transmission with a novel training
approach that uses biosimulation. Am J Infect Control 2007;35:14e9.
[48] Lamm F. Small businesses and OH&S advisors. Saf Sci 1997;25:153e61.
[49] Graveling R, Sanchez-Jimenez A, Lewis C, Groat S. Protecting respiratory
health: what should be the constituents of an effective RPE programme? Ann
Occup Hyg 2011;55:230e8.
[50] Heron RJL. Worker education in the primary prevention of occupational
dermatoses. Occup Med 1997;47:407e10.
[51] Cherrie JW, Semple S, Christopher Y, Saleem A, Hughson GW, Philips A. How
important is inadvertent ingestion of hazardous substances at work? Ann
Occup Hyg 2006;50:693e704.
[52] Gardner D, Carlopio J, Fonteyn PN, Cross JA. Mechanical equipment injuries in
small manufacturing businesses. Knowledge, behavioural, and management
issues. Int J Occup Saf Ergon 1999;5:59e71.
[53] Al-Haj MA, Awadh NA, Ali AA. Survey of Pesticides used in Qat
cultivation in Dhale’and Yafe’and their Adverse Effects. J Nat Appl Sci 2005;9:
103e10.
[54] Lee S, Obendorf SK. Statistical model of pesticide penetration through woven
work clothing fabrics. Arch Environ Contam Toxicol 2005;49:266e73.
[55] Perry MJ, Marbella A, Layde PM. Association of pesticide safety knowledge
with beliefs and intentions among farm pesticide applicators. J Occup Environ
Med 2000;42:187e93.
[56] Lander GH, Hinke K. Indoor application of anti-cholinesterase agents and the
influence of personal protection on uptake. Arch Environ Contam Toxicol
1992;22:163e6.
[57] Nigg HN, Stamper JH, Queen RM. Dicofol exposure to Florida citrus applica-
tors: effects of protective clothing. Arch Environ Contam Toxicol 1986;15:
121e34.
[58] Obendorf SK, Csiszar E, Maneefuangfoo D, Borsa J. Kinetic transport of pesti-
cide from contaminated fabric through a model skin. Arch Environ Contam
Toxicol 2003;45:283e8.
[59] Fenske RA, Hamburger SJ, Guyton CL. Occupational exposure to fosetyl-Al
fungicide during spraying of ornamentals in greenhouses. Arch Environ
Contam Toxicol 1987;16:615e21.
[60] Coffman CW, Stone J, Slocum AC, Landers AJ, Schwab CV, Olsen LG, Lee S. Use
of engineering controls and personal protective equipment by certified
pesticide applicators. J Agric Saf Health 2009;15:311e26.
[61] Aprea C, Terenzoni B, De Angelis V, Sciarra G, Lunghini L, Borzacchi G,
Vasconi D, Fani D, Quercia A, Salvan A, Settimi L. Evaluation of skin and res-
piratory doses and urinary excretion of alkylphosphates in workers exposed
to dimethoate during treatment of olive trees. Arch Environ Contam Toxicol
2004;48:127e34.
[62] Vitali M, Protano C, Del Monte A, Ensabella F, Guidotti M. Operative modalities
and exposure to pesticides during open field treatments among a group of
agricultural subcontractors. Arch Environ Contam Toxicol 2009;57:193e202.
[63] Fenske RA, Birnbaum SG, Methner MM, Lu C, Nigg HN. Fluorescent tracer
evaluation of chemical protective clothing during pesticide applications in
central Florida citrus groves. J Agric Saf Health 2002;8:319e31.
[64] Keifer MC. Effectiveness of interventions in reducing pesticide overexposure
and poisonings. Am J Prev Med 2000;18:80e9.
[65] Driver J, Ross J, Mihlan G, Lunchick C, Landenberger B. Derivation of single
layer clothing penetration factors from the pesticide handlers exposure
database. Regul Toxicol Pharmacol 2007;49:125e37.
[66] Nigg HN, Stamper JH, Easter E, DeJonge JO. Protection afforded greenhouse
pesticide applicators by coveralls: a field test. Arch Environ Contam Toxicol
1993;25:529e33.
[67] Stewart PA, Fears T, Kross B, Ogilvie L, Blair A. Exposure of farmers to phosmet,
a swine insecticide. Scand J Work Environ Health 1999;25:33e8.
[68] Machera K, Goumenou M, Kapetanakis E, Kalamarakis A, Glass CR. Determi-
nation of potential dermal and inhalation operator exposure to malathion in
greenhouses with the whole body dosimetry method. Ann Occup Hyg
2003;47:61e70.
[69] MacFarlane E, Chapman A, Benke G, Meaklim J, Sim M, McNeil J. Training and
other predictors of personal protective equipment use in Australian grain
farmers using pesticides. Occup Environ Med 2008;65:141e6.
[70] Reynolds SJ, Tadevosyan A, Fuortes L, Merchant JA, Stromquist AM,
Burmeister LF, Taylor C, Kelly KM. Keokuk County rural health study: self-
reported use of agricultural chemicals and protective equipment.
J Agromedicine 2007;12:45e55.
[71] Baldi I, Brochard P, Mohammed-Brahim B, Rolland P, Salamon R. Retrospective
estimation of methods of pesticide occupational exposure. Rev Epidemiol
Sante Publique 1999;47:165e74.
[72] Pilkington A, Buchanan D, Jamal GA, Gillham R, Hansen S, Kidd M, Hurley J,
Soutar C. An epidemiological study of the relations between exposure to
organophosphate pesticides and indices of chronic peripheral neuropathy and
neuropsychological abnormalities in sheep farmers and dippers. Occup En-
viron Med 2001;58:702e10.
[73] National Registration Authority for Agricultural and Veterinary Chemicals
Expert Panel. The relevance to sheep husbandry practices in Australia of the
UK Institute of Occupational Medicine (IOM) Report: ‘Epidemiological study of
the relationship between exposure to organophosphate pesticides and indices
of chronic peripheral neuropathy, and neuropsychological abnormalities in
sheep farmers and dippers’. Canberra (Australia): National Registration Au-
thority for Agricultural and Veterinary Chemicals; 2000.
[74] Perry MJ, Marbella A, Layde PM. Compliance with required pesticide-specific
protective equipment use. Am J Ind Med 2002;41:70e3.
[75] Strong LL, Thompson B, Koepsell TD, Meischke H. Factors associated with
pesticide safety practices in farmworkers. Am J Ind Med 2008;51:69e81.
[76] Hines CJ, Deddens JA, Coble J, Alavanja MC. Fungicide application practices
and personal protective equipment use among orchard farmers in the agri-
cultural health study. J Agric Saf Health 2007;13:205e23.
[77] Avory G, Coggon D. Determinants of safe behaviour in farmers when working
with pesticides. Occup Med (Lond) 1994;44:236e8.
[78] Eakin JM. Leaving it up to the workers: sociological perspective on the
management of health and safety in small workplaces. Int J Health Serv
1992;22:689e704.
[79] Lichtenberg E, Zimmerman R. Adverse health experiences, environmental
attitudes, and pesticide usage behavior of farm operators. Risk Anal 1999;19:
283e94.
[80] Perry MJ, Layde PM. Farm pesticides: outcomes of a randomized controlled
intervention to reduce risks. Am J Prev Med 2003;24:310e5.
[81] Gomes J, Lloyd OL, Revitt DM. The influence of personal protection, environ-
mental hygiene and exposure to pesticides on the health of immigrant farm
workers in a desert country. Int Arch Occup Environ Health 1999;72:40e5.
[82] Stone J, Padgitt S, Wintersteen W, Shelley M, Chisholm S. Iowa greenhouse
applicators perceptions and use of personal protective equipment. J Environ
Health 1994;57:16e22.
[83] Cameron L, Lalich N, Bauer S, Booker V, Bogue HO, Samuels S, Steege AL.
Occupational health survey of farm workers by camp health aides. J Agric Saf
Health 2006;12:139e53.
E. MacFarlane et al / Dermal Pesticide Exposure 141