Rev Environ Health 2015; 30(1): 65–79

Suratman Suratman*, John William Edwards and Kateryna Babina

Organophosphate pesticides exposure among

farmworkers: pathways and risk of adverse
health effects
Abstract: Organophosphate (OP) compounds are the DOI 10.1515/reveh-2014-0072
most widely used pesticides with more than 100 OP com- Received November 7, 2014; accepted February 9, 2015
pounds in use around the world. The high-intensity use
of OP pesticides contributes to morbidity and mortal-
ity in farmworkers and their families through acute or
chronic pesticides-related illnesses. Many factors con- Introduction
tributing to adverse health effects have been investigated
by ­ researchers to determine pathways of OP-pesticide Pesticide use significantly increases from year to year, par-
exposure among farmers in developed and developing ticularly in developing countries. Pesticides are beneficial
countries. Factors like wind/agricultural pesticide drift, for food production, improving crop yields and the effi-
mixing and spraying pesticides, use of personal protec- ciency of food production processes, reducing the cost of
tive equipment (PPE), knowledge, perceptions, washing food, and providing high-quality produce for consumers.
hands, taking a shower, wearing contaminated clothes, Approximately 40% of food production around the world
eating, drinking, smoking, and hot weather are common is lost every year due to weeds, pests, and diseases. Crop
in both groups of countries. Factors including low socio- losses would be doubled if farmworkers did not apply pes-
economic status areas, workplace conditions, duration of ticides to crops. In addition, the safe domestic use of pesti-
exposure, pesticide safety training, frequency of applying cides also has some benefits for controlling pests relevant
pesticides, spraying against the wind, and reuse of pes- to public health and infrastructure (termites, roaches,
ticide containers for storage are specific contributors in ants, rats, and other pests).
developing countries, whereas housing conditions, social Organophosphates (OP) are among the most widely
contextual factors, and mechanical equipment were spe- used agricultural chemicals. More than 100 OP com-
cific pathways in developed countries. This paper com- pounds are known and have been used in most countries
pares existing research in environmental and behavioural around the world.
exposure modifying factors and biological monitoring Agricultural workers compose the population at
between developing and developed countries. The main most risk of exposure to OP pesticides. The aim of this
objective of this review is to explore the current depth of paper is to review exposure pathways prior to the design
understanding of exposure pathways and factors increas- of a study to assess ways to reduce OP exposure. The
ing the risk of exposure potentially leading to adverse novelty of this review article is a comparison of envi-
health effects specific to each group of countries. ronmental and behavioural factors, including biological
monitoring between developing and developed coun-
Keywords: biological monitoring; developed and devel- tries based on previous studies to determine specific
oping countries; farmworkers; occupational exposure; pathways of OP-pesticides exposure and factors affect-
organophosphate pesticides exposure. ing the risk of increased exposure leading to adverse
health effects.
*Corresponding author: Suratman Suratman, Health and
Environment Group, School of the Environment, Flinders
University, SA 5042, Australia, Phone: +61 434148451,
E-mail: [email protected]; and School of Public Health,
Faculty of Health Sciences, Jenderal Soedirman University, Kampus
A brief history of OP compounds
Karangwangkal, Purwokerto 53122, Indonesia
John William Edwards and Kateryna Babina: Health and
OP compounds have been used for a long time to protect
Environment Group, School of the Environment, Faculty of Science crops from insect attacks. De Clermont and Moschnine
and Engineering, Flinders University, Adelaide, SA, Australia discovered tetraethyl pyrophosphate (TEPP) as the first

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66 Suratman et al.: Organophosphate pesticides exposure among farmworkers

OP cholinesterase inhibitor in 1854 (1–3). From 1934 to Chlorpyrifos has a short biological half-life, approxi-
1944, Schrader developed parathion, paraxon, tabun, mately 18 h in plasma and 62 h in fat tissue (13). However,
sarin, and soman as nerve agents (1–3). Parathion was due to their very wide use, chlorpyrifos metabolites are
developed and introduced to the market for the first time commonly found in human tissue (fat tissue). Excretion
in 1943 and is still being used on a wide scale today (4, 5). of chlorpyrifos occurs mainly through urine. Chlorpyri-
After World War II, the use of OP pesticides in agricul- fos oxon is the active metabolite that causes toxic effects.
ture and public health rose significantly (6). Most people The oral LD50 of chlorpyrifos in rats ranges between 82–
used OP pesticides to control pests from the 1950s to the 270 mg/kg (13).
1960s. The Cyanamid Company introduced malathion in OP poisoning occurs when OP compounds enter a
1950 (1, 5). In 1952, dichlorvos, trichlorfon and diazinon human body through the dermal, gastrointestinal, or res-
were developed (7). Meanwhile, another nerve agent, VX, piratory system. The principle mechanism of action of
was developed in 1958 (1). From 1961, VX was mass-pro- OP pesticides is ChE inhibition. Acetylcholine (ACh) is an
duced to be among the chemical warfare agents used by excitatory neurotransmitter. ChE breaks down ACh into
the military (1). In the late 1950s, OP use rose dramatically choline and acetic acid in the synaptic cleft and thus pre-
in agriculture and horticulture (8). vents over-stimulating post-synaptic nerves, muscles, and
exocrine glands. (17, 18).
OP inhibits ChE activity by occupying and block-
Pesticide forms ing the location where the ACh attaches to the ChE. As a
result, excessive amounts of ACh accumulate at the skel-
Most OP are used as insecticides, with a few used as a etal neuromuscular junction and synapses and cause
fungicides, herbicides, or rodenticides. This group of over-stimulation of post-synaptic nerves, muscles, and
pesticides is available in powder, liquid concentrate, or exocrine glands (17).
granules. All forms are susceptible to hydrolysis and oxi- Specific cholinesterases, known as red-blood cell
dation. Moisture and sunlight play important roles in the Acetylcholinesterase (RBC-ChE), are in the nerve gan-
environmental transformation process (9, 10). Degrada- glion synapses and erythrocytes, whereas non-specific
tion of these compounds in the environment is fast. For cholinesterases, known as butyrylcholinesterase (BuChE)
example, malathion, chlorpyrifos, and diazinon degrade or plasma cholinesterase (PChE), are found mainly in
rapidly, with half-lives, respectively, ranging from 1 to 5 plasma and the liver (18).
days, from about 2 to 14 days, and from 16 to 103 days at
25°C (9, 11–13).
Exposure to OPs in humans can occur via ingestion,
inhalation, and dermal absorption. Uptake through the
Intrinsic factors increasing suscep-
skin may be significant because of the lipophilic nature tibility to OP effects
of these compounds. Biotransformation of OPs occurs
through three main reactions, namely, oxidation, trans- Two intrinsic factors that can increase susceptibility to OP
ferase reaction, and hydrolysis (14). Toxic effects of OPs pesticides are ChE and paraoxonase (PON1) (19) activity
occur through inhibiting acetylcholinesterase (AChE) levels.
(generally known as cholinesterase (ChE)) enzyme activ-
ity, inhibiting neuropathy target esterase (NTE), and
releasing the alkyl groups attached to the phosphorous ChE
atom and the alkylation of macromolecules, including
RNA and DNA (9, 14). ChE is the target enzyme of OP in the central and periph-
Chlorpyrifos [O,O-diethyl O-(3,5,6-trichloro- eral nervous systems. Lower ChE activity increases
2-pyridinyl)-phosphorothionate] is one of the most widely susceptibility to OP exposure (20). A study by Benmoyal-
used OP pesticides (15, 16). Chlorpyrifos can enter the Segal et al. (21) showed that Parkinson’s disease (PD)
body through the gastrointestinal tract, skin, or inha- patients who were exposed to OP insecticides had lower
lation (15, 16). Chlorpyrifos experiences bio-activation AChE activity than non-exposed PD patients (21). Another
to chlorpyrifos oxon in the liver through cytochrome study among OP-exposed agricultural pesticide han-
P-450-mediated desulfurisation and then undergoes dlers in Washington State recruited during the period of
hydrolysis to 3,5,6-diethylphosphate and trichloro-2-pyri- the 2006 and 2007 spray seasons (22) revealed that all of
dinol (TCP) (13). the research participants had significantly lower BuChE

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 Suratman et al.: Organophosphate pesticides exposure among farmworkers 67

activity during the OP spray season compared to presea- Some studies have demonstrated the existence of OP
son levels (n = 163; p < 0.001). in the environment. Simcox et al. (29) measured OP com-
pounds (azinphosmethyl, chlorpyrifos, parathion, and
phosmet) in household dust and soil samples collected
Paraoxonase (PON1) from children’s play areas near operating apple and pear
orchards. The samples were extracted and analysed by
Paraoxonase (PON1) is a polymorphic enzyme synthe- gas chromatography/mass selection detective. As many
sized in the liver and transported, along with a high-den- as 62% of household dust samples contained these four
sity lipoprotein, in plasma that plays an important role OP compounds, and 66.7% of the farm homes were found
in hydrolysing the active metabolites of OP compounds to have at least one OP in quantities above 1000 ng/g.
like diazinon, chlorpyrifos, and parathion (23–25). Her- Another study by Gordon et al. (30) revealed that chlorpy-
nandez et al. (24) showed that long-term exposure to rifos and diazinon have been detected in all sample media
pesticides decreased PON1 – 909 G/C polymorphism (indoor and outdoor air, house dust, and foundation soil).
activity. Similarly, Ellison et al. (26) in Egypt demon- Chlorpyrifos were found in floor dust (88%), indoor air
strated that PON1 55 and PON1 192 genotypes had a sig- (65%), personal air (17%), yard soil (31%), foundation
nificant influence on PON1 activity among agricultural soil (48%), and outdoor air (ng/m3) (10%). Meanwhile,
workers exposed to chlorpyrifos. PON1 phenotype is an diazinon had been identified in floor dust (53%), indoor
important factor of susceptibility to OP toxicity. Among air (63%), yard soil (18%), foundation soil (37%), and
163 OP-exposed agricultural pesticide handlers in Wash- outdoor air (ng/m3) (21%).
ington State there was significant association between
lower levels of plasma PON1 activity and greater BuChE
inhibition (22). Costa et al. (25) found PON1 to be an Biological monitoring
important factor of OP-pesticide toxicity among rats and
mice, especially in the toxicity of diazinon and chlorpy- According to Berlin et al., biological monitoring means
rifos oxon. “the measurement and assessment of workplace agents
or their metabolites either in tissues, secreta, excreta,
expired air or any combination of these to evaluate

Monitoring of OP-pesticide exposure and health risk compared to appropriate refer-

ence” (31).
exposure The National Research Council classified biological
monitoring into three types as follows: [1] biological moni-
Agricultural workers are frequently occupationally toring of exposure (i.e., measuring the dose of pesticides
exposed to OP pesticides in occupational settings. absorbed by the human body and identifying its metabo-
Common methods to monitor exposure to OP pesticides lites in urine after exposure); [2] biological monitoring of
use data collected from environmental measurements effect (i.e., blood cholinesterase testing); and [3] biologi-
and/or in biological samples. cal monitoring of susceptibility (i.e., PON1 status) (32).
Biological monitoring has an important role in iden-
tifying any substances that accumulate in a human body
Environmental monitoring exposed to chemicals, especially pesticides, through
measurement of biomarkers in biological samples. Bio-
The aim of environmental monitoring is to measure haz- logical monitoring is the best method to analyse to what
ardous materials in environmental media, such as air, extent a farmworker has been exposed to pesticides due to
surfaces, household dust, water, food, and soil. It is par- multiple pathways by which exposure can occur (33, 34).
ticularly important when a single exposure route has been Table 1 presents some previous studies regarding
identified (27). According to Hoppin et al. (28), surface biological monitoring (AChE, PChE, PON1, metabolites)
sampling indoors can be measured using methods of of OP-pesticide exposure in developing (35–44) and
deposition pad samples, a wipe sampling technique, or developed countries (20–25, 45–54). Generally, some bio-
a vacuum technique. Air samples can be measured using markers (AChE, PChE, and metabolites) and symptoms of
high-volume samplers. Meanwhile, a duplicate plate OP-pesticide exposure have been investigated by research-
method is used to analyse OP-pesticide exposure in food ers in both groups of countries. However, researchers in
samples. developing countries have generally not measured PON1

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68 Suratman et al.: Organophosphate pesticides exposure among farmworkers

Table 1: Biological monitoring of OP-pesticide exposure studies in developing and developed countries.

Study sites References Biological monitoring related to risk factors

AChE PChE PON1 Metabolites Health effects Environmental Behavioural

factors factors

Developing Shomar et al. (35) – – – o – – o

countries Panuwet et al. (36) – – – X – – X
Afriyanto (37) X – – – – o X
Jintana et al. (38) X X – – – – X
Dasgupta et al. (39) X – – – ∧ – –
Cecchi et al. (40) X X – – – X o
Kashyap (41) X X – – o – o
Panuwet et al. (42) – – – X – – –
Phung et al. (43) – – – X – – –
Catano et al. (44) – X – – X – X

Developed Gonzalez et al. (20) X X X – – – –

countries Benmoyal-Segal et al. (21) X – X – – – –
Hofmann et al. (22) – X X – – – –
La Du et al. (23) – – o – – – –
Hernández et al. (24) – – ∧ – – – X
Costa et al. (25) – X X – – – –
Tromm et al. (45) X – – – X – –
Nomura et al. (46) – X – – – – –
Koch et al. (47) – – – X – – –
Bouvier et al. (48) – – – X – X –
Furlong et al. (49) – – X – – – –
Grandjean and Landrigan (50) – – – o o – –
Lopez-Granero et al. (51) X – – – X – –
Marsillach et al. (52) – o – – – – –
Rohlman et al. (53) o o – – o – o
Sanchez-Santed et al. (54) X – – – X – –

X = significant (p < 0.05) in bivariate analysis; XX = significant (p < 0.05) in multivariate analysis; o = factor was not statistically examined; ∧ = factor
was examined, no significant association; ∼ = factor was examined, no information regarding association test; – = factor was not investigated.

in their studies. This is completely different from devel- Acute cholinergic syndrome
oped countries, where most studies have investigated
PON1, and some of them have linked these biomarkers Acute cholinergic syndrome occurs due to high level expo-
with neuro-behavioural outcomes (Table 1). sure to OP compounds. It occurs soon after exposure to
OP and lasts for several days. Symptoms and signs occur
as the result of ChE inhibition. A failure of ChE hydrolysis

Clinical manifestations of OP results in excessive amounts of ACh (18, 55). Cholinergic

receptors are nicotinic, found at autonomic ganglia and
toxicity the neuromuscular junction, and muscarinic, found in
parasympathetic effector organs (18). Nicotinic and mus-
ACh is a neurotransmitter that acts at two main receptors, carinic are two types of cholinergic receptors that have a
namely, nicotinic and muscarinic. There are three types different anatomical locations, different functions, and
of clinical manifestations of OP toxicity: acute choliner- different clinical symptoms (Figure 1) (17).
gic syndrome, intermediate syndrome, and organophos- The percentage of normal RBC-ChE or PChE activ-
phate-induced delayed neuropathy (OPIDN). Marrs (18) ity required to produce acute clinical manifestation
indicates that acute cholinergic syndrome and intermedi- is as follows: normal if the activity is greater than or
ate syndrome are the result of inhibition of ChE, whereas equal to 75%, mild inhibition if the activity ranges from
OPIDN is associated with the inhibition of NTE. 30% to 74%, moderate inhibition if the activity ranges

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 Suratman et al.: Organophosphate pesticides exposure among farmworkers 69

Figure 1: Nicotinic and muscarinic effects of cholinesterase inhibitors.

Adapted from Heide (17).

from 10% to 29%, and severe inhibition if the activity syndrome” was introduced by Senanayake and K ­ aralliedde
is < 10% (56). in 1987. It appears between acute cholinergic syndrome and
Heide (17) grouped signs of OP poisoning based on OP-induced delayed polyneuropathy (OPIDN) (57–59).
types of cholinergic receptors (Table 2). An anatomical IMS (known as the nicotinic syndrome) occurs when
location of nicotinic and muscarinic receptor targets asso- the synaptic ChE is inhibited by at least 80% after acute
ciated with signs and symptoms of ChE inhibitors are pre- exposure (60). IMS only occurs in the event of severe poi-
sented in Figure 1. soning (60). Some clinical manifestations of IMS are weak-
ness of the respiratory system, neck, and proximal limb
muscles that occur approximately 16–120 h after expo-
Intermediate syndrome (IMS) sure and 7–75 h after the onset of acute pesticide poison-
ing symptoms (9, 61). However, ChE inhibition does not
Intermediate syndrome (IMS) develops 1–4 days after acute directly influence the occurrence of IMS. Muscle weakness
poisoning and lasts for 18 days. The term “intermediate may be affected by prolonging cholinergic stimulation (9).

Table 2: Signs of OP poisoning based on types of cholinergic receptors (17).

Type of receptor Location Signs Onset

Nicotinic a) Skeletal neuromuscular junction Mydriasis (pupillary dilation), tachycardia, Soon after OP exposure
b) Sympathetic and parasympathetic hypertension, weakness, fasciculations
nervous system
c) Autonomic ganglia
d) Central nervous system
Muscarinic a) Parasympathetic nervous system: Salivation, urination, lacrimation, Slower than nicotinic
– Cardiac conduction system defecation/diaphoresis, gastrointestinal receptor
– Exocrine glands pain, emesis, miosis (pupillary
– Smooth muscles constriction), bronchospasm, anxiety,
b) Sympathetic nervous system emotional lability, hallucinations,
– Sweat glands restlessness, confusion, depression,
c) Central nervous system headache, respiratory-depression, coma

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70 Suratman et al.: Organophosphate pesticides exposure among farmworkers

A prospective study conducted by De Bleecker et al. Table 3 presents 17 selected studies of OP-pesticide
(59) indicated that in a 19-patient cohort group, eight poisoning among agricultural workers in developing (37,
patients suffered from IMS, and six of them had relaps- 39, 69–78) and developed (74, 79–82) countries. The main
ing cholinergic signs like lacrimation, increased bronchial approaches used in the studies in developing countries
and salivary secretion, diarrhea, sweating, bradycardia, were cross-sectional (5 of 12; 41.7%), whereas the studies
and fasciculation that superimposed on IMS. in developed countries used literature approaches (2 of
Wananukul et al. (62), in a 2005 study in Thailand 5; 40.0%). Most of the studies shown in Table 3 indicate
of two cases of OP poisoning in which IMS developed, that the proportion of OP-pesticide poisoning in develop-
reported that in the first case, weakness of the neck, ing countries was higher than in developed countries. In
proximal limb muscles, and respiratory system developed developing countries, OP insecticides are mainly applied
on the 3rd day after ingestion, and the patient recovered in agriculture and are reported to produce adverse health
11 days after the poisoning. The second case developed effects (83). OP pesticides used in farming worldwide
bulbar palsy, proximal muscle and respiratory weakness also lead to an increase in morbidity and mortality rates
3 days after ingestion. around the world, largely due to an increase in acute pes-
ticide poisoning cases (74). Although data on worldwide
impacts are limited, the number of deaths due to pesti-
OPIDN cide poisoning in 2002 was estimated to be approximately
186,000, with 4,420,000 disability-adjusted life years (84).
OPIDN starts 1 or 2 weeks after poisoning and is, at least to In developing countries, the number of deaths caused by
some extent, persistent. OPIDN is one of the types of toxic- pesticide poisoning is higher than the mortality caused by
ity due to some OP insecticide compounds like tri-o-cresyl infectious diseases (85).
phosphate, O-ethyl-O-4-nitrophenyl phenylphosphono- In addition to acute poisonings, OP pesticides also
thionate), and O-(4-bromo-2,5-dichlorophenyl)-O-methyl cause chronic diseases like cancer, birth defects and
phenylphosphonothionate and can happen in many developmental toxicity, reproductive disorders, Parkin-
species including humans. Some clinical manifestations son’s disease, Alzheimer’s disease, amyotrophic lateral
of OPIDN are numbness, weakness of the arms and legs sclerosis (ALS), diabetes, cardiovascular diseases, chronic
followed by progressive and irreversible ataxia or paraly- nephropathies, chronic respiratory disease, etc. (86). In
sis that develops 2–3 weeks to months after acute exposure developed countries, a cohort study from 1993 to 1997 con-
to OP insecticides (61, 63–65). It occurs when neuropathy ducted by Kamel et al. (87) in the U.S. showed that preva-
target esterase (NTE) is inhibited in lymphocytes by neu- lent and incident cases of Parkinson’s disease associated
ropathic OPs within hours of exposure (66). Glynn (67) with pesticide exposure, respectively, were 83 of 79,557
defined NTE as ‘an integral membrane protein in vertebrate (0.10%) at enrolment and 78 of 55,931 (0.14%) at follow-
neurons’. Whole blood NTE is the ideal biomarker to detect up. Another prospective cohort among 57,284 U.S. certi-
OP compounds until 96 h after exposure, in relation with fied/licensed pesticide applicators and 32,333 spouses of
the occurrence of OPIDN (66). OPIDN occurs when NTE is private applicators revealed that 300 incidents of lung
inhibited by at least 55%–70% following an acute dose of cancers linked with OP-pesticide exposure (chlorpyrifos
organophosphate and no < 45% inhibition after repeated and diazinon) had been observed since enrolment in 1993
exposure (68). until December 2001 (88). Soetadji et al. (89) investigated
There is no association between inhibition of NTE and aortic (Ao) elasticity in Indonesia and showed that chil-
inhibition of ChE. Not all commercial insecticides (i.e., dren living in an OP-exposure area had higher Ao-stiffness
chlorpyrifos and dichlorvos) lead to OPIDN, unless they indexes (96%). Another study conducted by Suhartono
are ingested at near lethal doses (61). et al. (90) among 44 women of childbearing age (WCA)
as a case group and 44 WCA as a control group living in
agricultural areas found that the proportion of hypothy-
roidism due to OP exposure among the case group was
Epidemiological studies 43.2% (19 of 44), whereas the proportion of hypothyroid-
ism among the control group was only 20.0%.
Studies in and around the world have demonstrated that It appears from this review of the literature that, in
pesticide poisoning is a major public health problem. general, developed countries are more concerned with
Some studies have reported the occurrence of acute poi- long term effects of low exposures to insecticides, whereas
sonings from mild to severe due to OP exposure. developing countries remain more focused on acute

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 Table 3: Available epidemiological studies on OP-pesticide poisoning among agricultural workers in developed and developing countries.

References Type of study Population Key findings

Developing Zhang et al. (69) Cross-sectional 910 pesticide applicators from two villages in Approximately 80 people or 8.8% of the 910 pesticide applicators
countries southern China suffered from acute work-related pesticide poisoning. Most
poisoning cases were due to insecticide exposure (92.5%).
Kishi et al. (70) Prospective cohort 204 farmworkers in Tegal and Brebes Regency, Of OP-pesticide sprayers, 21% exhibited at least four symptoms
Central Java, Indonesia like neurobehavioral, gastrointestinal, and respiratory symptoms
related to OP-pesticide exposure.
Murali et al. (71) Retrospective All patients hospitalised with acute poisoning A total of 2884 patients (1918 men) suffered from acute pesticide
during the period of 1990–2004 (15 years) at poisoning during the period of 1990–2004. OP pesticides were
Nehru Hospital of the Postgraduate Institute of the most common agents (35.1%).
Medical Education and Research in Chandigarh
He (72) Retrospective 52,287 cases of acute pesticide poisoning 6281 deaths. 17.8% of total cases were due to occupational
reported from 27 provinces of China in 1993 pesticide poisoning, and 78% of total cases of pesticides
poisoning were due to OP compounds.
Rustia et al. (73) Cross-sectional 56 pesticide applicators at Campang Village, 71.4% of 56 participants suffered from mild OP poisoning, and
Gisting Sub District, Tanggamus Regency, 28.6% of 56 farmworkers suffered from moderate OP poisoning.
Lampung Province, Indonesia
Dasgupta et al. (39) Survey 190 farmworkers in the Mekong Delta, Vietnam All 190 farmworkers had some symptoms after mixing and
spraying OP pesticides. These symptoms consisted of skin
irritation (66%), headache (61%), dizziness (49%), eye irritation
(56%), and shortness of breath (44%).

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Jeyaratnam (74) Literature Cases of acute pesticide poisonings based on Proportion of total acute poisonings due to pesticides in
hospital data in Indonesia and Brazil in 1980s Indonesia and Brazil in 1980s, respectively, was 28.0% and
16.0%.
Faria et al. (75) Cross-sectional 2400 tobacco farmers in southern Brazil Prevalence of minor psychiatric disorders (MPD) due to

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OP-pesticide exposure was 12%. Tobacco farmworkers using OP
pesticides had 50% more risk of MPD than those not exposed to
OP.
Peshin et al. (76) Retrospective 4929 calls of pesticide poisoning were recorded 40.61% of pesticide poisoning cases associated with agricultural
during 13-year period (1999–2012) by the pesticides. OP pesticides ranked first (9.79%) in agricultural
National Poisons Information Centre, All India pesticides group that caused poisoning.

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Institute of Medical Sciences, New Delhi, India
Rajashekhara et al. (77) Cross-sectional 76 OP-poisoned patients who were admitted to 25% of 76 patients were agricultural workers. Most of them
Jawaharlal Nehru Medical College suffered from congested conjunctiva (87%), pinpoint pupil (83%),
lacrimation (80%), vomiting (78%), non-reactive pupil (75%),
respiratory distress (60%), and abdominal pain (37%).
Kir et al. (78) Retrospective 10,720 autopsied by Ankara Branch of Council 70 cases of 10,720 were attributed to fatal pesticide poisoning.
Suratman et al.: Organophosphate pesticides exposure among farmworkers

of Forensic Medicine in Turkey Most of them (63%) were due to OP insecticides.

Afriyanto et al. (37) Cross-sectional 50 chili farmers in Candi Village, Bandungan 13 of 50 participants or 26% suffered from severe OP-pesticide
Sub District, Semarang Regency, Indonesia poisoning.
71
 (Table 3: Continued)
72

References Type of study Population Key findings

Developed Beseler and Stallones (79) Cohort study 872 farmworkers in Colorado, USA 6.0% of 872 respondents on baseline data suffered from
countries pesticide poisoning.
Das et al. (80) Survey 138 farmworkers were selected from nine cities 27.6% of 138 respondents had health problems related to
in the USA chemicals, including pesticides.
Lee et al. (81) Retrospective 2945 cases from 1998 to 2006 related to 92% of agricultural workers suffered from low-severity illness.
agricultural pesticide drift from 11 states in The annual incidence was between 1.39 and 5.32 per million
the US. Data were obtained from the National persons over the 9-year period. 45% of cases were due to soil
Institute for Occupational Safety and Health’s applications with fumigants. Meanwhile, 24% of cases were due
Sentinel Event Notification System for to aerial applications.
Occupational Risk – Pesticides Program and the
California Department of Pesticide Regulation.
Zilker (82) Literature OP poisoning data for Germany between 1975 Approximately 200 OP-poisoning cases happen in Germany every
and 1996 year. The poison centre in Munich reported that 482 cases of OP
compounds poisoning have occurred from 1975 to 1996. Twenty
OP compounds contributed to these cases. The highest incidence
was due to parathion (287 cases), oxydemeton-methyl (90
cases), and dimethoate (22 cases). OP compounds were the most
commonly used OP in Germany.
Jeyaratnam (74) Literature Cases of acute pesticide poisonings based on Proportion of total acute poisonings due to pesticides in UK,

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hospital data in the UK, Australia, Canada, and Australia, Canada, and the U.S. In 1980s. respectively, was 5.0%,
the US in 1980s 3.0%, 2.4%, and 0.8%.

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 Suratman et al.: Organophosphate pesticides exposure among farmworkers 73

effects and high level exposures. This may reflect the

Social contextual
availability and use of these agents in different countries

X = significant (p < 0.05) in bivariate analysis; XX = significant (p < 0.05) in multivariate analysis; o = Factor was not statistically examined; ∧ = Factor was examined, no significant association;
and may also be a consequence of the awareness of chemi-
factors
cal risks and the presence of environmental and consumer
lobby groups in developed countries. Further research is
–
–

–
–

–
–
–
X

X
o
o
necessary to establish the contribution of these factors to
conditions
Workplace

XX pesticide exposures.
–

–
–
–
–
–
–
–
o

o
Pathways of OP-pesticide exposure
Wind/agricultural

among agricultural workers

pesticide drift

This aim of this review is a better understanding of how

farmworkers are exposed to OP pesticides and how such
–
–
–
–

–
–

–
–
–
X

X
o

exposures can be reduced. The potential risk factors that

Poor areas

were frequently included in pathways of OP-pesticide

exposure in developing and developed countries were
modifiable environmental and behavioural factors. These
XX
–

–
–

–
–
–
–
–
–
–
–

factors were the most influential factors contributing to

Table 4: Environmental risk factors and pesticide exposure risk factor studies in developing and developed countries.

A greater number of adults

and farmworker in a house

good health (91).

The potential environmental risk factors or modifi-
able determinants for OP-pesticide exposure among agri-
cultural workers based on previous studies in developing
(37, 69, 92, 93) and developed (81, 94–100) countries are
∼ = factor was examined, no information regarding association test; – = factor was not investigated.

presented in Table 4. There are some differences between

developing and developed countries regarding environ-
–
–
–
–

–
–
–
–
–
–
o

mental factors most commonly relating to OP-pesticide

exposures. Generally, hot weather and wind/agricultural
conditions
Housing

pesticide drift appear to be significant factors of higher

exposure levels in both country groups. However, other
–
–
–
–

–
–
X

X
X
o

factors, namely, poor areas (69) and workplace condi-

Environmental related factors

tions (93), provided large contributions to OP-pesticide

Humidity

exposure in developing countries. Meanwhile, housing

conditions (96, 98, 99) and social contextual factors (96,
–
–

–
–
–
–
–
–
–
–
o

98) were very significant in developed countries (Table 4).

Hot weather

The other group of exposure modifying factors was

human behavioural risk factors, which also significantly
contributed to OP-pesticide exposure among agricultural
XX
–

–
–
–
–
–
X
o

workers based on previous studies in developing (35–38,

69, 70, 92, 93, 101–107) and developed (96, 100, 108–113)
Quackenbush et al. (94)

countries. The summary of these studies is presented in

Ward and Tanner (98)
Keller-Olaman (96)

Flocks et al. (100)

Table 5. Generally, both developing and developed coun-

Blanco et al. (93)

Arcury et al. (99)

Zhang et al. (69)

Early et al. (95)

Issa et al. (92)

Litchfield (97)

tries were similar in terms of behavioural factors con-

Afriyanto (37)

Lee et al. (81)

References

tributing to OP-pesticide exposure. These factors were

as follows: mixing pesticides, spraying pesticides, use
of PPE, knowledge, perceptions, washing hands, show-
ering, wearing contaminated clothes, eating, drinking,
Study sites

Developing

Developed

and smoking. However, each group of countries also had

countries

countries

specific behavioural risk factors significantly associated

with the exposures. Duration of exposure (37, 70, 104,

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 74

Table 5: Behavioural risk factors and pesticide exposure risk factor studies in developing and developed countries.

Study sites References Behavioural related factors

Mixing Load­ Spray­ Touched Riding Duration Use of Know­ Percep­ Pesticide Wash­ Taking a Wearing Re-entry Eating, Illite­ Frequ­ Spraying Reuse of
pesti­ ing ing sprayed on of expo- PPE ledge tions safety ing shower contami­ into a drinking, or racy ency of against pesti­cide
cides pesti­ pesti­ crops equip- sure training hands nated farm area smoking apply­ the wind contai­
cides cides ment clothes after ing ners for
pesticide pesti­ sto­rage
spraying cides

Developing Ribeiro et al. (101) o o o – – – o – – o o o – o – – – –

Countries Shomar et al. (35) o – o – – – o o – – – – – – – – – –
Dosemeci (102) ∼ – ∼ – – – – – – – ∼ – – – – – – –
Lein et al. (103) ∧ – ∧ – – – X – – – – – – – ∧ – – –
Mancini et al. (104) X o o – – X – – – – – – – – – XX – – –
Panuwet et al. (36) – – – – – – X – – – – – – – – – ∧ – –
Zhang et al. (69) – – ∧ – – – XX – – XX – ∧ – – XX – – ∧ –
Jintana et al. (38) X – – – – ∧ X – – – – ∧ ∧ – ∧ – – – –
Oluwole and Cheke (105) o – o – – – o – – o – – o – – o – – –

Authenticated
Lu (106) o o o – – X – – – – – – X ∧ – – – – X
Afriyanto (37) – – X – – X X X X – X X – – – – – X –
Issa et al. (92) ∧ – o – o o – – – – – – – – X – ∧ – –
Kishi et al. (70) o o X – – X X – – – – – X – o – XX – X

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Suratman et al.: Organophosphate pesticides exposure among farmworkers

Recena et al. (107) – – – – – ∧ ∧ o o – X ∧ ∧ – ∧ – – ∧ o

Blanco et al. (93) – – XX – – – ∼ – – – ∼ – – – – – – ∼ –

Developed Hines et al. (108) X – X – X – XX – – – – – – – – – – – –

countries Stallones et al. (109) ∧ ∧ ∧ – X – – – – – – – – – – – – – –
Strong et al. (110) – – – – – – o X o o o o – – – – – –
Arcury et al. (111) – – – – – – X X X – X X X – – – – – –

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Johnstone (112) ∧ ∧ – – – ∧ ∧ o – – X – – – ∧ – – – –
Bradman et al. (113) – – – – – ∧ X – – – – – o – o – – – –
Keller-Olaman (96) – – – – – – – – X – – – – – X – – – –
Flocks et al. (100) – – – – – – – o – – – – – – – – – – –

X = significant (p < 0.05) in bivariate analysis; XX = significant (p < 0.05) in multivariate analysis; o = factor was not statistically examined; ∧ = factor was examined, no significant association;
∼ = factor was examined, no information regarding association test; – = factor was not investigated.
 Suratman et al.: Organophosphate pesticides exposure among farmworkers 75

106), pesticide safety training (69), frequency of pesticide approach was very common in developed countries.
application (70), spraying against the wind (37), and reuse There was an absence of integrated studies regarding
of pesticide containers for storage (70, 106) were very sig- OP exposure, risk factors, and outcomes.
nificant factors in developing countries. Riding on equip- 7. Finally, improving knowledge about the adverse effect
ment (108, 109) was reported to be a significant factor in of pesticides and knowledge about self-protection
developed countries (Table 5). from pesticide exposure has the potential to make a
significant impact on improving pesticide handling,
storage, and application.
Conclusion
Despite research exploring the risk factors of pesticide
Farmers, market gardeners, pesticide applicators, mixers, exposure and its impact on farmers’ health, we still do not
loaders, flaggers, and their families have been badly know much about the specific pathways that may increase
affected by pesticide exposure. Morbidity and mortality pesticide exposure for farmers in developing and devel-
rates due to pesticide exposure have risen dramatically oped countries. Particularly concerning, there is a clear
since the first use of pesticides thousands of years ago. paucity of relevant research in Indonesia and Australia.
The number of studies exploring the impact of pesticide At this point, we can conclude that well-designed quasi-
exposure on the health of farmers is increasing. Evalua- experimental studies are needed to highlight the benefits
tion of the existing literature revealed the following: of providing pesticide safety training for preventing and
1. Scientific research examining factors contributing to reducing pesticide exposure among farmworkers.
OP-pesticide exposure among farmworkers by com-
paring developed countries and developing countries Acknowledgments: The authors are grateful to the Direc-
remains limited. In general, results indicate that the torate General of Higher Education (DIKTI) of the Republic
data were only partially analysed. of Indonesia for providing scholarships in the Ph.D. Pro-
2. Few studies have looked at biological monitoring like gram at the School of the Environment, Flinders Univer-
levels of cholinesterase in blood, types of metabolites sity, South Australia, Australia.
in urine samples, and adverse health effects due to
pesticide exposure associated with risk factors. Most Conflict of interest: The authors declare that they have no
studies looked only at risk factors of pesticide expo- conflicts of interest to report.
sure without direct biomarker measurements.
3. Environmental and behavioural risk factors like hot
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