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Visual disturbances with cholinesterasedepletion due to exposure ofagricultural pesticides among farmworkersMohammad Fareed a , Chandrasekharan Nair Kesavachandran a

, Manoj Kumar Pathak a , Vipin Bihari a , Mohammed Kuddus b &Anup Kumar Srivastava aa Epidemiology Division, CSIR – Indian Institute of ToxicologyResearch (CSIR-IITR), Lucknow, Uttar Pradesh, Indiab Department of Biotechnology, Integral University, Lucknow,Uttar Pradesh, India

Accepted author version posted online: 07 Aug 2012. Version ofrecord first published: 31 Aug 2012

To cite this article: Mohammad Fareed, Chandrasekharan Nair Kesavachandran, Manoj KumarPathak, Vipin Bihari, Mohammed Kuddus & Anup Kumar Srivastava (2012): Visual disturbanceswith cholinesterase depletion due to exposure of agricultural pesticides among farm workers,Toxicological & Environmental Chemistry, DOI:10.1080/02772248.2012.718780

To link to this article: http://dx.doi.org/10.1080/02772248.2012.718780

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Toxicological & Environmental Chemistry2012, 1–9, iFirst

Visual disturbances with cholinesterase depletion due to exposure

of agricultural pesticides among farm workers

Mohammad Fareeda, Chandrasekharan Nair Kesavachandrana,Manoj Kumar Pathaka, Vipin Biharia, Mohammed Kuddusb andAnup Kumar Srivastavaa*

aEpidemiology Division, CSIR – Indian Institute of Toxicology Research (CSIR-IITR),Lucknow, Uttar Pradesh, India; bDepartment of Biotechnology, Integral University, Lucknow,Uttar Pradesh, India

(Received 16 February 2012; final version received 30 July 2012)

In this study, risk assessment for visual disturbances among farm workersspraying agricultural pesticides in farms have been assessed. A cross-sectionalstudy for the assessment of visual disturbances was undertaken using question-naire survey and clinical examination among agricultural workers exposedto pesticides. Two hundred and thirty nine pesticide sprayers participated in thestudy. The study was compared to 110 controls not occupationally exposed topesticides with similar socio-economic status. The prevalence of ocular morbiditywas found to be 40% among pesticide sprayers which was significantly higher(p5 0.01) as compared to controls. The symptoms among morbid subjectswere found to be blurred vision, lacrimation, pain in eyes, red swollen eyes, andirritation of eyes. Exposure wise assessment of ocular symptoms among pesticidesprayers illustrates that exposure time elevates the ocular problems amongsprayers. The cholinesterase activity was found to be significantly depleted(p5 0.01) among pesticide sprayers as compared to controls which show theexposure of organophosphate pesticides among them. The visual disturbancesobserved among pesticide sprayers clearly exhibit that eyes get exposed bypesticides during spraying operations in agriculture and eventually get affectedleading to ocular illness.

Keywords: ocular illness; pesticide exposure; cholinesterase depletion; unsafework practices

Introduction

Eyes are exposed to external environment and thereby exposed to environmentalcontaminants. During agricultural operations, eyes of the farm workers get the pesticidesexposure while spraying if proper preventive steps are lacking. As a result, these chemicalsare absorbed through the eye tissue and enter the blood circulation. Exposure ofunprotected eyes to pesticides results in the absorption in ocular tissue and potential oculartoxicity (Jaga and Dharmani 2006). Aerial spraying of pesticides into the environmentover farms increases the risk of ocular exposure in workers on the ground (Ciesielski et al.1994). Case reports have implicated organochlorines and carbamates in ocular toxicity(Morse, Baker, and Kimbrough 1979; Taylor, Selhorst, and Houff 1978), and animal

*Corresponding author. Email: srianup1@yahoo.co.in

ISSN 0277–2248 print/ISSN 1029–0486 online

� 2012 Taylor & Francis

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studies have implicated two fungicides, thiram, and benomyl, in retinal degeneration(Hellman and Laryea 1990; Maita, Tsuda, and Shirasu 1991). Long-term ocular exposureto pesticides may produce chronic effects in the eyes. Pesticide exposure may worsenocular health, considering age-related visual problems, diabetic retinopathy, cataract,glaucoma, retinal detachment, and eye trauma (Jaga and Dharmani 2006). Beyond thedescription of eye symptoms, there is an understanding that pesticides may produce toxiceffects on various components of the eye. These include effects on the conjunctiva, cornea,iris, lens, retina, and the optic nerve, including visual neural pathways extending from thebrain (Jaga and Dharmani 2006). The ocular toxicity includes reduction of acuity, myopia,astigmatism, constriction of the visual field, disorders of intra and extra ocular eye musclesand discoloration and degeneration of the retina and optic nerve (Boyes et al. 1999).

Organophosphate (OP) pesticides inhibit the action of Acetylcholinesterase (AChE),enzyme involved in the release of acetylcholine at the nerve endings (Yalemtsehayand Ejigu 2005), thus OP increases the cholinergic effects of acetylcholine in the body anddepolarization of neural transmission (Weiss, Amler, and Amler 2004). AChE activityin the red blood cells and butrylcholinesterase (BChE) activity in plasma have been usedto monitor the extent of OP and carbamate exposure (Rama and Jaga 1992; Yamanakaet al. 1993).

In the present study, we investigated the visual disturbances and cholinesterase levelsas a biomarker of OP pesticides exposure among farm workers who spray pesticidesby working in unsafe environment without following any preventive and hygienic workpractices. There is very much paucity of such kind of study which could reveal the oculartoxicity among pesticide sprayers who get the pesticide exposure occupationally.

Material and methods

Study design

This is a cross-sectional study for the visual disturbances leading to ocular illness relatedto agricultural pesticide exposure. The study was conducted at Malihabad region ofLucknow, India. The pesticide sprayers had experience of spraying in mango plantationfrom 1–30 years. Spraying operations last for 2–8 h per week per season on the treesof mango orchards from December to March every year (Kesavachandran, Rastogi, andMathur 2006). Mixing of chemicals with bare hands, leakages from tanks of pesticideduring spraying operations were found to be very common. Pesticide sprayers of mangoplantations were using pesticides like OPs (monocrotphos, dichlorvos, malathion,methyl parathion), organochlorines (endosulfan, thiodon), pyrethroids (cypermethrin),and carbamates (carbaryl).

Subjects

All the exposed subjects participated in this study were engaged in spraying of pesticidesincluding OP, organochlorine, carbamate, and pyrethroids without using any personalprotective equipment. Two hundred and thirty nine male pesticide sprayers participatedin the study. The study was compared to 110 healthy males having no previous or currentoccupational exposure to pesticides taken as control from near by area with same socio-economic status. On the basis of area of living, ethnicity both groups of subjects werealmost similar. The purpose of the study was explained to all the participants and theirconsent was obtained. Institutional Human Ethics Committee clearance was obtainedfor collecting the human blood samples and clinical investigations from subjects.

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Questionnaire

A preliminary questionnaire was designed to record the personal and occupationalinformation along with pesticide exposure and ocular health symptoms of the pesticidesprayers. Each pesticide sprayer was interviewed based on questionnaire like generalinformation about the name, age, smoking habit of individual pesticide sprayer; infor-mation about the exposure period of pesticide spraying in respect of years; informationabout the use of pesticide like the type of pesticide they spray, methods of spraying thepesticides, information about the work practices followed by them during sprayingthe pesticides such as whether they handle the pesticides with bare hands or measuringcup, whether they wear any protective equipment, whether they eat anything whilespraying, whether they take bath after spraying; ocular health information through clinicalexamination.

Clinical examination

Clinical examination for self reported ocular health symptoms was done by a medicaldoctor who was familiar with ocular illness and the symptoms were recorded in thequestionnaire for every individual. The self reported symptoms of each participant wererecorded in the questionnaire by medical doctor. Institutional Human Ethics Committeeclearance was obtained for collecting the blood samples and clinical investigations of thestudy subjects.

Blood sample collection

Approximately 3.0mL venous blood was collected in the heparinized, pesticide free glassvials as coded samples from both the control and sprayers. Samples were transported tothe laboratory of the Epidemiology Division of Indian Institute of Toxicology Research,Lucknow, India, in ice-cold condition immediately after the collection. The cholinesterasemeasurement was carried out on same day.

Cholinesterase measurement

Blood AChE and BChE activities as biomarkers of OP pesticide exposure were determinedby the method of Ellman et al. (1961) as modified by Chambers and Chambers (1989)by taking acetylthiocholine iodide and butyrylthiocholine iodide, respectively, as substrateand expressed as mmols hydrolyzed h�1L�1 blood (IUL�1).

Statistical analysis

The data was analyzed by using Software EPI-INFO version 6.04 d, Centre for DiseaseControl and Prevention (CDC), USA. The student’s t-test and chi-square test for trial wasused for statistical significance. The student’s t-test were used to compare the physicalcharacteristics namely age, height, and body weight between pesticide sprayers and controlsubjects (Table 1), comparison of ocular symptoms among pesticide sprayers and controlsubjects (Table 2), comparison of cholinesterase activity among pesticide sprayersand control subjects (Table 5). Chi-square test was used for the distribution of ocular

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symptoms among control and sprayers (Table 3) and for the exposure wise distributionof ocular symptoms among pesticide sprayers and control subjects (Table 4).

Results

Physical characteristics and educational status of pesticide sprayers and control subjectsis shown in Table 1. Age and height were not significantly different in both the groups,while body weight, body mass index (BMI), educational status and exposure period werestatistically found to be significant. Table 2 shows the comparison of exposed and control

Table 1. Physical characteristics and educational status of control and pesticidesprayers.

VariablesControl (n¼ 110)(Mean� SD)

Pesticide sprayers(n¼ 239) (Mean� SD)

Age (years) 35.5� 13.6 36.5� 1.4Height (cm) 167.0� 7.5 162.6� 0.6Body weight (kg) 63.4� 17.1 51.8� 0.8*BMI (kgm�2) 22.2� 4.4 19.3� 2.7*Educational statusIlliterate n (%) 0 (0) 51 (21)*Literate n (%) 110 (100) 188 (79)*Exposure (year) 0.0� 0.0 14.1� 10.5*

Note: *p5 0.05.

Table 3. Distribution of ocular symptoms among control and sprayers.

No. of ocular symptomsControl (N¼ 110)

n (%)Pesticide sprayers(N¼ 239) n (%)

0 or nil 103 (93.7) 144 (60.3)*1 6 (5.4) 50 (20.9)*2 1 (0.9) 27 (11.2)*3 0 (0) 10 (4.1)*4 0 (0) 7 (2.9)*5 0 (0) 1 (0.6)

Note: *p50.01.

Table 2. Overall ocular problems among control and exposed group.

Groups No. of subjectsSubjects having ocular

symptoms n (%)

Control 110 7 (6.3)Pesticide sprayers 239 95 (40)*

Note: *p50.01.

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groups having ocular symptoms. Only seven individuals (6.3%) reported ocular problemsin the control group, whereas there are many subjects in the exposed groups who reportedfor the ocular symptoms while spraying or after spraying the pesticides in the mangoplantations. The prevalence of the ocular symptoms was found to be 40% among pesticidesprayers. Table 3 shows the number of ocular symptoms among pesticide sprayers andcontrol. Pesticide sprayers reported ocular symptoms ranging from 1 to 6 in number whichwere blurred vision, watering of eyes, pain in eyes, itching and burning sensation in eyes,and swollen eyes. Some pesticide sprayers have only a single problem while some havemany and even some have all the six problems which are exhibited in the table. Table 4shows exposure wise distribution of ocular symptoms among pesticide sprayers andcontrol subjects which illustrates that exposure time elevates the ocular problems amongpesticide sprayers. Pesticide exposure was taken into consideration both as number ofyears and hours per day (years * hours per day), according to which four groups wereestablished, namely 511, 11–50, 51–100, 101 and above. It was seen that the group havingmost time of pesticide exposure exhibited most prevalence of ocular symptoms. Odd ratioalso shows regular increment pattern as exposure time increases, chi-square value forlinear trial was found to be 34.5 and p-value was found to be 0.001 which shows highlystatistical significance for increasing trend in prevalence of ocular symptoms observedwith increasing pesticide exposure.

The biomarkers of OP pesticides exposure namely, AChE and BChE activities in bloodamong pesticide sprayers were analyzed and the results shown in Table 5. Activities ofboth AChE and BChE among pesticide sprayers were found to be highly significantlydepleted (p5 0.01) as compared to control subjects.

Figure 1 shows the frequency distribution of ocular symptoms namely blurred vision,watering of eyes, pain in eyes, swollen eyes, and itching and burning sensation ineyes among pesticide sprayers. It was seen that maximum pesticide sprayers havereported for symptoms of blurred vision during the time of spraying and after the sprayingas well.

Table 4. Exposure wise distribution of ocular symptoms among pesticide sprayers and control.

Total pesticide exposureat work place (years� hours)

No. ofsprayers

No. of sprayers havingocular symptoms

Prevalence ofsymptoms (%)

Oddratio*

511 40 6 15.0 1.0011–50 83 22 26.5 2.1651–100 49 20 40.8 4.14101 and above 67 44 65.7 11.4

Notes: *Chi-square value for linear trial¼ 34.5.p-value¼ 0.001.

Table 5. Cholinesterase activity (IUL�1) in study subjects.

Cholinesterase activity (IUL�1) Control (n¼ 69) Pesticide sprayers (n¼ 163)

AChE mean� SD 570� 307 412� 239**Butyrylcholinesterase mean� SD 435� 218 271� 193**

Note: **p5 0.01.

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Discussion

Present study is a report for the ocular illness among the pesticide applicators of India who

get the exposure during and after pesticide spraying operations in agriculture. These farm

workers spray pesticides with bare eyes having no safety spectacles; eventually eyes of

these pesticide sprayers get exposed. We recorded the ocular morbidity symptoms namely

near vision, far vision, blurred vision, watering of eyes, pain in eyes, and swollen eyes

among pesticide sprayers which were found to be very much prevailed as compared

to control showing the risk of toxic effects due to pesticide exposure on eyes. However,

there are very limited similar kinds of studies, but certain earlier studies show some

agreement with our study. The most commonly described effects of pesticides on eyes are;

irritation, burning sensation, itchiness, blurring of vision, and watering of eyes (Bradberry,

Proudfoot, and Vale 2004; Gomes et al. 1998; Lu 2005; Strong et al. 2004). Blurring

of vision and burning sensation are known symptoms of OP poisoning from systemic

exposure as a result of inhalation, ingestion, or dermal contact (Echobichon 1996;

Schenker, Albertson, and Saiki 1992; Sullivan and Blose 1992). Applicators, who used

certain methods to apply fungicides were at greater risk of retinal degeneration than

those who used other methods (Kamel et al. 2000). These studies show some similarity

with our study suggesting that the use of personal protective equipment might help

to reduce risk of pesticide exposure among pesticide sprayers.OP and pyrethoid pesticides used by the pesticide sprayers in the present study were

neurotoxic in nature, so the AChE and BChE activities were found to be significantly

depleted in the pesticide exposed group than that of control group. It is a well-accepted

fact that AChE and BChE are biomarkers for OP pesticide exposure, so it could be

considered that the inhibited activities of AChE and BChE are due to OP pesticide

exposure among the pesticide sprayers. Exposure to large doses of OP is required for

significant AChE inhibition to occur and hence it is more appropriately used as an

indicator of toxicity at higher levels (He 1999). All the pesticide sprayers recruited in this

Figure 1. Frequency distribution of ocular symptoms among pesticide sprayers.

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study showed significant depletion in the activities of AChE and BChE among whichsome (40%) have ocular illness which ascertains that all the sprayers having ocularproblems are exposed to OP and carbamate pesticides.

The ocular symptoms reported were mostly during the spraying. The prevalenceof ocular illness among pesticide sprayers was found to be 40% whereas among controlgroup, 6.3% subjects reported for any eye problem as all the control subjects were healthyand not occupationally exposed to pesticides. There are many pesticide sprayers who haveonly single ocular complaint but some of them have two or more and even few of themhave all the six ocular complaints included in our study. We have correlated the exposureduration of pesticides considering both years and hours per day spraying with theprevalence of ocular symptoms and found a regular increment pattern in prevalenceof ocular symptoms which illustrates that exposure duration causes more exposure ofpesticides to eyes which eventually results in more risk of ocular toxicity due to pesticides.We found the maximum number of cases reported for blurred vision among farm workers,which may lead to loss of vision and visual impairment. Watering of eyes, pain in eyes, andswollen eyes were prominently reported during the spraying operations.

There is existence of many risks of ocular diseases due to exposure of pesticides.Pesticides may produce toxic effects on various components of the eye. A previous casereport (Mckeag, Maini, and Taylor 2002) illustrates that a farm worker exposed to theherbicide, paraquat, developed injury to the cornea, with damage to the epithelium in theacute phase of the eye injury. Exposure to pesticides may increase the risk of retinaldegeneration. Studies in Japan have linked OP exposure to Saku disease, which involvesretinal degeneration and other adverse ocular effects (Dementi 1994; Ishikawa 1973).A cross-sectional study of fenthion pesticide exposure in India found macular degener-ation in 19% of the workers, compared to 3% of controls (Misra, Baker, and Kimbrough1985). These studies show the ocular diseases due to exposure of different pesticides usedin agriculture. Pesticide sprayers in the present study were working at a very high riskof ocular toxicity as they get exposed to agricultural pesticides regularly. The eyes of thesepesticide sprayers get direct exposure of pesticides while spraying. During sprayingoperations these pesticide sprayers never follow any hygienic work practices due to theirunawareness of ocular toxicity due to pesticides. Sometimes, during spraying they rub theireyes from fingers of their unwashed hands when they feel itching in their eyes. The effectof pesticide toxicity in the eyes may be worse than imagined, starting with mild visualproblems, conditions could progress to more severe visual impairment, or possibly a totalloss of vision (Jaga and Dharmani 2006).

However, in present study any specific eye examination test was not performed amongthe study subjects, which is the limitation of this study, but the self reported symptomsfor visual disturbances are due to pesticide exposure because most of the subjectscomplained these symptoms during pesticide spraying operations. It could not be deniedthat if these symptoms persist continuously, then it may lead to some serious oculardisease. It is suggestive that safe precautionary methods of pesticide spraying operationsin agriculture should be applied for the prevention of eyes from pesticide exposure.

Acknowledgments

Mohammad Fareed acknowledges Council of Scientific and Industrial Research, India for providinghim Senior Research Fellowship. Mr. Neeraj Mathur is acknowledged for his assistance in statisticalanalysis involved in this study. The financial support by Uttar Pradesh Council of Science &Technology, India (CST/SERPD/D-860) for the project is hereby acknowledged.

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