Occupational health risk of farmers exposed to pesticides in agricultural activities

Occupational health risk of farmers exposed to pesticides in agricultural activities

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Current Opinion in

Environmental Science & Health

Occupational health risk of farmers exposed to pesticides in agricultural activities Venugopal Dhananjayan and Beerappa Ravichandran Abstract

Farmers are routinely exposed to various types of agrochemicals, but there is no evidence about adverse effects posed by these chemicals on human health. Studies from all over the world have shown negative health effects of commonly used pesticides in the agricultural occupation. Correlation between occupational exposure to pesticides and development of a wide variety of diseases ranging from respiratory effects to various types of cancer has been identified. Although the published information does not include all variables that can assist in exposure risk assessment, the real risk associated with pesticide exposure is well established. It is more than obvious that the agricultural community needs the implementation of a new agricultural concept regarding food production, which is safer for farmers, farm-workers, and the environment. This review paper summarizes the most recent findings describing the association between occupational exposure to pesticides and related health effects on farmers and farm-workers regularly involved in agricultural activities. Addresses Industrial Hygiene & Toxicology Division, Regional Occupational Health Centre (Southern), Indian Council of Medical Research, Poojanahalli Road, Kannamangalo Post, Devanahalli TK, Bangalore 562110, India Corresponding author: Dhananjayan, Venugopal (dhananjayan_v@ yahoo.com)

Current Opinion in Environmental Science & Health 2018, 4:31–37 This review comes from a themed issue on Pesticides in agriculture: environmental and health effects Edited by Christos A. Damalas For a complete overview see the Issue and the Editorial

https://doi.org/10.1016/j.coesh.2018.07.005 2468-5844/© 2018 Elsevier B.V. All rights reserved.

Keywords Occupational health, Pesticide exposure, Health effects, Farmers.

Introduction Various type of exposure during work activities may affect the health conditions of farmers in agricultural practices, despite the use of personal protective equipment (PPE). Adverse effects associated with occupational exposure have been observed in a large number of studies [1,2]. All these effects may involve www.sciencedirect.com

biomolecular alterations, resulting in the development of specific diseases [3,4]. Although all components included in pesticides seem to be non toxic to humans, several studies have demonstrated that chronic exposure to pesticides may be a serious risk factor for the development of chronic diseases [5,6]. Exposure of farmers to pesticides can be through multiple pathways, including consumption of contaminated food, residing close to agricultural fields, and agricultural occupation. The risk of exposure will vary based on the type of pesticide, the duration and route of exposure, and the health status of each individual. The numerous negative health effects that have been associated with pesticides are dermatological, gastrointestinal, neurological, carcinogenic, respiratory, and reproductive effects. Also, accidental or intentional exposure to pesticides may result in death [7]. In addition, pesticide residues have been detected in human breast milk samples, while there are concerns about prenatal exposure and health effects on children [8]. Rural workers, farmers, and farm-workers are considered as a major risk group that receives the greatest exposure to pesticides by transporting, mixing, loading, and applying pesticides. Many workers are not aware of the risks associated with the use of pesticides, whereas the lack of training and equipment for safely handling pesticides increases health risk [9]. However, detailed understanding of pesticide exposure among farm-workers is essential for drawing firm conclusions about potential health effects. On this ground, this review paper summarizes health risks associated with occupational exposure to pesticides among farmers and farm-workers regularly involved in agricultural activities. The paper aims at highlighting the health risk associated with agricultural activities, focusing on the major health effects and recent findings regarding health effects that have been associated with exposure to common classes of chemical pesticides.

Methodology This review paper was based on a non-systematic methodological approach to explore the available literature published between January 2016 and March 2018. Articles that showed occupational exposure of farmers to pesticides in common agricultural activities were identified through online electronic databases (e.g., PubMed, Science Direct, Web of Science, and other web sources). The search keywords were occupational exposure, agricultural pesticides, farmers and farmCurrent Opinion in Environmental Science & Health 2018, 4:31–37

32 Pesticides in agriculture: environmental and health effects

workers, health effect of pesticides, occupational diseases. A preliminary total of 309 related published articles were selected from the literature, excluding duplicates. The references of those publications were checked for additional recent articles in relevant international journals to compile adequate information for discussion. The publications that are closely related to this review paper are discussed.

Results and discussion This review combined published results of various health effects of farm-workers exposed to pesticides in agricultural activities. Figure 1 illustrates the different activities of farmers and farm-workers exposed to pesticides during and after pesticide applications in the field. The published information was categorized based on the nature of health risk and presented in Figure 2. The majority of the publications (41%) were related to neurological disorders, followed by other health risks (14%), cancer (13%), poisoning (8%), respiratory problems (7%), reproductive disruption and genotoxicity (6% each), and chronic kidney diseases (5%).

Haematological and biochemical changes

Assessment of greenhouse workers exposed to pesticides revealed increased levels of erythrocytes, leukocytes, platelets, and haemoglobin, but decreased levels of erythrocyte acetylcholinesterase and glucose, creatinine, total cholesterol, triglyceride, and alkaline phosphatase relative to controls [3]. Exposure to pesticides was significantly correlated with reduction in pseudocholinesterase (PChE) activity, induced hematotoxicity, oxidative stress, and genotoxicity in greenhouse workers [10]. Nassar et al. [4] evaluated the effects of pesticides on blood indices as well as on thyroid and reproductive hormones among adult male volunteers. The study of Pressuti et al. [11] observed significant increases in multiple myeloma risk with the use of carbaryl, captan and DDT. Increased risk of death due to non-Hodgkin lymphoma (NHL) was observed among young farmworkers exposed to agrochemicals in southern Brazil [7]. Riaz et al. [12] determined the correlation between pesticide exposure, physical health and susceptibility towards tuberculosis along with alterations in haematological indices and liver enzymes in pesticide operators in Punjab, India. Prenatal exposure to organochlorine pesticides (OCPs) was marginally associated with decreases in neutrophil counts [13]. Parks et al. [14] suggested possible association of systemic lupus erythematosus (SLE), an autoimmune disease, with

Figure 1

Farmers and farm-workers exposed to pesticides (Ravichandran et al., unpublished pictures). Current Opinion in Environmental Science & Health 2018, 4:31–37

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Occupational health risk of farmers Dhananjayan and Ravichandran

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Figure 2

Health effects of farmers associated with occupational exposure to pesticides (based on literature between 2016 and 2018).

exposure to solvents, residential, and agricultural pesticides, heavy metals, and air pollution. Respiratory diseases

Certain studies have recommended that increased awareness of respiratory risks and improved monitoring of agricultural environments are necessary for limiting pulmonary health risks to exposed populations [15]. Farmers in rice fields were found to have the highest prevalence of allergies, nasal congestion, wheezing, and acute symptoms after pesticide use [16]. PPE is an approach for reducing respiratory exposures in agricultural settings, with education for correct use of respirator and evaluation for tolerance of respirator being important parameters [17]. Common symptoms of pesticide exposure are asthma attacks, shortness of breathing [18,19]. Agricultural industries are also associated with numerous lung diseases, including chronic obstructive pulmonary disease, asthma, and hypersensitivity pneumonitis [20]. Children in close proximity to farms showed adversely affected respiratory health [21] and urinary metabolites of pesticides were associated with decreased lung function [22]. Exposure to contaminants in agricultural activities leads to inflammation and lung function changes [23]. A large scale cross sectional study comprising different farming systems observed increased risk of adverse respiratory health effects among farm-workers exposed to pesticides [24].

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Neurological diseases

The World Health Organization (WHO) recommended the neurobehavioral core test battery (NCTB) to assess neurobehavioral functioning of exposed populations. Scores on the Profile of Mood States (POMS) in poisoned group were higher for anger-hostility, depression-dejection, tension-anxiety and lower for vigoractivity compared with controls. These findings provide important preliminary epidemiological evidence regarding the association between occupational exposure to pesticides and neurobehavioral functioning in Chinese farm-workers [25]. A review by Sa´nchez-Santed et al. [26] highlighted the main neurological and cognitive deficits and the experimental and epidemiological relationships between pesticide exposure and Alzheimer’s, Parkinson’s, and Amyotrophic Lateral Sclerosis (ALS) diseases. Numerous studies have demonstrated relationships between pesticide exposure and neurodegenerative and neurodevelopment disorders [27] and sleep apnea [28]. Farmers’ exposure to agrochemicals is linked with both acute and chronic neurotoxicity [29]. Although certain studies found no relationship between organophospharous pesticides (OPs) exposure and neuropsychological performance, several studies suggested association between chronic occupational exposure to OPs and neuropsychological effects [30] and interrelation of glycemic status and neuropsychiatric disturbances [31]. The major concerns related to OPs exposure are delayed effects following high exposure Current Opinion in Environmental Science & Health 2018, 4:31–37

34 Pesticides in agriculture: environmental and health effects

levels as well as the impact of low exposure levels during the lifespan, which are suggested to be a risk factor for nervous system chronic disease [26]. However, there is no consensus about the specific cognitive skills affected. Reproductive disorders

Organochlorine pesticides had been widely used in agriculture and disease prevention in the 1940s-1960s. Currently, OCPs are raising global concerns due to their associated prevalent contamination and adverse health effects, such as endocrine disruption. Several studies have explored the underlying association of OCPs with thyroid hormone (TH) status in adults and newborns [32]. An investigation on both cumulative and recent occupational exposure to agricultural pesticides showed a positive association of serum levels of OCPs and those of total triiodothyronine (T3), total thyroxine (T4), and negative but no significant changes in thyroidstimulating hormone (TSH) in male floricultural workers [33]. Alteration in thyroid function after longterm exposure to aldrin, pendimethalin and methyl bromide due to occupational exposure among male pesticide applicators was evaluated by Lerro et al. [34]. Waheed et al. [35] suggested that dust contaminated with pesticides engenders significant health risk particularly related to the nervous and endocrine system, not only for occupational farm-workers exposed to direct ingestion, but also for nearby residential community. Chronic diseases

End-stage renal disease was associated with pesticide exposure provided reassuring findings of significantly increased risks and positive exposure-response trends among pesticide applicators [2,36]. Currently, there is little literature available on the nephrotoxic effects of pesticides. Migrant farm-workers employed on pineapple, durian, and rambutan plantations in Thailand involved in spraying of pesticides showed increased risk of chemical exposure and developed acute or chronic illness from pesticide exposure [37]. The major concerns related to pesticide exposure are even low exposure levels during the lifespan leads to nervous system chronic diseases [26]. Over the past two decades, there has been an increase in chronic interstitial nephritis in agricultural communities. However, an understanding of a comprehensive approach with multicentre cooperation is essential for the development of public health programs to prevent this devastating epidemic [38,39]. Future research should be made with an assessment of lifetime exposures to specific pesticides with other major risk factors. Genotoxicity

High pesticide exposure and DNA methylation was observed among pesticide applicators [40,41]. Prevalence of GSTP1 and XRCC1 polymorphisms and DNA damage was assessed among population exposed to Current Opinion in Environmental Science & Health 2018, 4:31–37

pesticides. These risks may be affected by polymorphisms of genes for glutathione transferasedependent metabolism of pesticides and for DNA repair [42]. Although some studies have reported that the low level use of insecticides does not pose a risk to DNA in general [43], a long term exposure increased the prevalence of muscle weakness and numbness [44]. A recent study has shown oxidative stress as a marker of oxidative DNA damage and 8-isoPGF as a product of lipoprotein peroxidation [45]. A positive correlation between urine metabolites of pesticides and oxidative stress and DNA damage in farmers exposed to OCPs, OPs, carbamate and pyrethroid pesticides was observed [46e48]. Reactive oxygen species formed through pesticide exposures can overwhelm an organism’s antioxidant capabilities resulting in oxidative stress linked with many chronic diseases [45]. A significant reduction of superoxide dismutase (SOD) and catalase (CAT) activities was reported among farmworkers occupationally exposed to pesticides [48]. A few studies have shown increase in frequency of chromosomal aberration (CA) and micronucleus (MN) among exposed group [27,49,50] and its relation with various confounding factors [49]. Farm-workers during intensive spraying season and acute exposure, showed consistent increases in MN frequency [27,50]. Even short-term exposure to pesticides created chromosome translocations and a decreased level of pesticide-induced genotoxicity was associated with proper use of PPE [51]. Pesticide exposed and tobacco smoking subjects showed significant effects on absolute telomere length compared with the non-exposed group and the telomere length indicated biomarker of occupational exposure [52]. Nevertheless, prospective and longitudinal studies aiming on genetic polymorphisms and associated health effects are needed to further delineate the influence of agricultural exposure in farmers. Cancer

In the developed world, occupational exposure to pesticides is a leading cause of cancer. Several studies have reported associations between specific pesticides and bladder cancer risk [53], lung cancer [20], and laryngeal cancer [34], skin melanoma and multiple myeloma [54] and increased risks among non smokers [55]. A possible association existed between the development of prostate cancer and pesticide exposure in agricultural occupations [40]. A decreased incidence for tobaccorelated cancers and an increased incidence of prostate cancers, skin melanoma, and multiple myeloma were also observed. Specific subgroups had a higher level of cancer incidence related to occupational status and pesticide use [54]. Further studies regarding this occupational exposure of farmers are required to determine the causes of the increased risk of this cancer,

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Occupational health risk of farmers Dhananjayan and Ravichandran

particularly in regions where there is intense agricultural activity and where pesticides are extensively used.

* of special interest 1.

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Nassar AMK, Salim YM, Malhat FM: Assessment of pesticide residues in human blood and effects of occupational exposure on hematological and hormonal qualities. Pakistan J Biol Sci 2016, 19:95–105.

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Gangemi S, Gofita E, Costa C, Teodoro M, Briguglio G, Nikitovic D, Tzanakakis G, Tsatsakis AM, Wilks MF, Spandidos DA, Fenga C: Occupational and environmental exposure to pesticides and cytokine pathways in chronic diseases (Review). Int J Mol Med 2016, 38:1012–1020.

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Cremonese C, Piccoli C, Pasqualotto F, Clapauch R, Koifman RJ, Koifman S, Freire C: Occupational exposure to pesticides, reproductive hormone levels and sperm quality in young Brazilian men. Reprod Toxicol 2017, 67:174–185.

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Boccolini PM, Boccolini CS, Chrisman JR, Koifman RJ, Meyer A: Non-Hodgkin lymphoma among Brazilian agricultural workers: a death certificate case-control study. Arch Environ Occup Health 2017, 72:139–144.

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Gunier RB, Kang A, Hammond SK, Reinier K, Lea CS, Chang JS, Does M, Scelo G, Kirsch J, Crouse V, Cooper R, Quinlan P, Metayer C: A task-based assessment of parental occupational exposure to pesticides and childhood acute lymphoblastic leukemia. Environ Res 2017, 156:57–62.

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Other health effects

There are many other health risks associated with exposure of farmers to pesticides. Pesticide poisoning among farmers was correlated with their poverty and poor education [46]. Bakhsh et al. [19] evaluated negative effects of pesticides on health of women cotton pickers. Our recent study showed that women workers exposed to pesticides in tea plantation suffered from various health effects (Dhananjayan et al., unpublished). The common health risks reported involved headache, eye irritation, flue/fever, skin infection/rash, dryness of throat, nausea and vomiting, dizziness, abdominal pain, sleeplessness, and other respiratory disorders. Specific agricultural pesticides showed increased frequency of rheumatoid arthritis in women [14,18]. Many of these findings emphasize the requirement of a detailed study that will address instances of pesticide use and the occurrence of health effects.

Conclusion In spite of many barriers in studying associations between health effects and pesticide exposure in farmers and farm-workers, adverse health consequences have been associated with pesticide exposure in these populations. Since most studies were limited to particular provinces, the available evidence cannot be interpreted as providing an accurate picture of the health status of the farm-workers throughout the world. However, based on the available health risk factors covered by occupational health research, the unsafe use of pesticides can causes several health effects to humans. Farmers should have more knowledge about alternatives to pesticides, color code classifications of pesticides, and negative side effects of pesticide exposure. Although many studies admitted several limitations considering the study power, design, and risk of selection bias, a large number of studies exists on the possible risk of pesticide exposure in human diseases. Nevertheless, more studies are warranted to identify the prevalence and related risk factors of these disorders among farmers and farm-workers.

Conflict of interest statement

35

10. Ahmadi A, Shadboorestan A: Oxidative stress and cancer; the role of hesperidin, a citrus natural bioflavonoid, as a cancer chemoprotective agent. Nutr Cancer 2016, 68:29–39. 11. Presutti R, Harris SA, Kachuri L, Spinelli JJ, Pahwa M, Blair A, Zahm SH, Cantor KP, Weisenburger DD, Pahwa P, McLaughlin JR, Dosman JA, Freeman LB: Pesticide exposures and the risk of multiple myeloma in men: an analysis of the North American Pooled Project. Int J Cancer 2016, 139: 1703–1714. 12. Riaz S, Manzoor F, Mahmood N, Shahid S: Molecular detection of M. tuberculosis and M. bovis and hematological and biochemical analyses in agricultural sprayers exposed to pesticides: a cross-sectional study in Punjab, Pakistan during 2014–2016. J Expo Sci Environ Epidemiol 2017, 27: 434–443.

Acknowledgments

13. Oulhote Y, Shamim Z, Kielsen K, Weihe P, Grandjean P, Ryder LP, Heilmann C: Children’s white blood cell counts in relation to developmental exposures to methylmercury and persistent organic pollutants. Reprod Toxicol 2017, 68: 207–214.

We are thankful to the Director, National Institute of Occupational Health, Ahmedabad for his continuous support for research. We are also grateful to Dr. Christos A. Damalas, Guest Editor of this special issue, who offered an invitation for contribution and made comments on the manuscript. Authors are thankful to the staff of ROHCS, Bangalore for their support during the manuscript preparation.

14. Parks CG, Hoppin JA, De Roos AJ, Costenbader KH, Alavanja MC, Sandler DP: Rheumatoid arthritis in agricultural health study spouses: associations with pesticides and other farm exposures. Environ Health Perspect 2016, 124: 1728–1734.

Nothing declared.

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