Occupational Exposure to Mixed Pesticides in Northern West Bengal Tea Gardens: Impact on Acetylcholinesterase Inhibition, Oxidative Stress, and Antioxidant Markers Among Female Tea Pluckers
Authors
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Department of Physiology, Serampore College, Hooghly - 712201, West Bengal ,IN
Ananya Bose -
Department of Physiology, Kalka Dental College, Meerut - 250006, Uttar Pradesh ,INSudipta Kundu
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Department of Medical Laboratory Technology, School of Allied Health Sciences, Swami Vivekananda University, Bara Kanthalia - 700121, West Bengal ,INOly Banerjee
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Department of Physiology, Serampore College, Hooghly - 712201, West Bengal ,INSiddhartha Singh
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Department of Physiology, Serampore College, 9 William Carey Road, Hooghly-712201, West Bengal. ,INAnindita Banerjee
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Department of Pathology, Bhatpara State General Hospital, Jagatdal - 743125, West Bengal ,INRanajit Mandal
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Department of Physiology, Serampore College, Hooghly - 712201, West Bengal ,INBithin Kumar Maji
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Department of Physiology, Serampore College, Hooghly - 712201, West Bengal ,INSandip Mukherjee
DOI:
https://doi.org/10.18311/jeoh/2024/43442Keywords:
Acetylcholinesterase, Antioxidant Enzyme, Female Tea Plucker, Oxidative Stress, Occupational Exposure, PesticideAbstract
Due to the potential health impacts of pesticides, biomonitoring of pesticide exposure is currently a subject of significant public interest. The purpose of the present research was to evaluate the levels of oxidative stress in female tea pluckers who are vulnerable to being exposed to a combination of pesticides in the northern part of West Bengal, India. Data were collected from 82 permanent female tea pluckers of two tea gardens in Jalpaiguri district and 68 women from the general population not directly exposed to the pesticides but living in the same geographical area. Acetylcholinesterase (AChE), Catalase (CAT), reduced glutathione (GSH), and Superoxide Dismutase (SOD) activity were measured, and levels of Lipid Peroxidation (LPO) and Nitric Oxide (NO) were determined in plasma. The student’s t-test analyzed the disparity between the exposed and non-exposed groups. Correlation coefficient analysis was conducted to determine the relationship between AChE and biomarkers of oxidative stress. Compared to the control group plasma AChE activity was significantly decreased (17.42%) among female tea pluckers (p≤0.001). In comparison to the control group, female tea pluckers showed a significant increase in LPO and NO levels as markers of oxidative stress, as well as a significant decrease in GSH levels. Enzymatic antioxidants SOD and CAT were significantly reduced in the exposed group. Significant correlations were observed between AChE and biomarkers of oxidative stress. In conclusion, the alterations in different biochemical parameters indicate that female tea pluckers were occupationally exposed to mixed pesticides (containing organophosphates) in tea gardens. It is therefore imperative to highlight the usage of personal protective equipment by the pluckers and environmentally friendly pesticide alternatives in the tea gardens. Additional research is recommended to connect our results with the negative health impacts seen in chronic pesticide exposure, in which oxidative damage is believed to be a key factor.
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Copyright (c) 2024 Ananya Bose, Sudipta Kundu, Oly Banerjee, Siddhartha Singh, Ranajit Mandal, Bithin Kumar Maji, Anindita Banerjee, Sandip Mukherjee
This work is licensed under a Creative Commons Attribution 4.0 International License.
Accepted 2024-06-21
Published 2024-08-26
References
Rastogi SK, Satyanarayan PV, Ravishankar D, Tripathi S. A study on oxidative stress and antioxidant status of agricultural workers exposed to organophosphorus insecticides during spraying. Indian J Occup Environ Med. 2009; 13(3):131-4. https://doi.org/10.4103/00195278.58916 PMID: 20442831; PMCID: PMC2862445.
Wafa T, Nadia K, Amel N, Ikbal C, Insaf T, Asma K, Hedi MA, Mohamed H. Oxidative stress, haematological and biochemical alterations in farmers exposed to pesticides. J Environ Sci Health B. 2013; 48(12):1058-69. https://doi.org /10.1080/03601234.2013.824285 PMID: 24007483.
Gilden RC, Huffling K, Sattler B. Pesticides and health risks. J Obstet Gynecol Neonatal Nurs. 2010; 39(1):103-10. https://doi.org/10.1111/j.1552-6909.2009.01092.x PMID: 20409108.
Simoniello MF, Kleinsorge EC, Scagnetti JA, Mastandrea C, Grigolato RA, Paonessa AM, Carballo MA. Biomarkers of cellular reaction to pesticide exposure in a rural population. Biomarkers. 2010; 15(1):52-60. https://doi.org/10.3109/13547500903276378 PMID: 19811113.
Dutta S, Bahadur M. Effect of pesticide exposure on the cholinesterase activity of the occupationally exposed tea garden workers of the northern part of West Bengal, India. Biomarkers. 2019; 24(4):317-24. https://doi.org/10.1080/13 54750X.2018.1556342 PMID: 30512980.
Sule RO, Condon L, Gomes AV. A common feature of pesticides: Oxidative stress-the role of oxidative stress in pesticide-induced toxicity. Oxid Med Cell Longev. 2022; 2022:5563759. https://doi.org/10.1155/2022/5563759 PMID: 35096268; PMCID: PMC8791758.
Sivaram B. Productivity improvement and labour relations in the tea industry in South Asia. ILO Publications; 1996.
Kausar A, Giri S, Roy P, Giri A. Changes in buccal micronucleus cytome parameters associated with smokeless tobacco and pesticide exposure among female tea garden workers of Assam, India. Int J Hyg Environ Health. 2014; 217(2-3):169-75. https://doi.org/ 10.1016/j.ijheh.2013.04.007 PMID: 23706883.
Altuntas I, Delibas N, Demirci M, Kilinc I, Tamer N. The effects of methidathion on lipid peroxidation and some liver enzymes: role of vitamins E and C. Arch Toxicol. 2002; 76(8):470-3. https://doi.org/10.1007/s00204-002-0359-1 PMID: 12185416.
Cataño HC, Carranza E, Huamaní C, Hernández AF. Plasma cholinesterase levels and health symptoms in Peruvian farm workers exposed to organophosphate pesticides. Arch Environ Contam Toxicol. 2008; 55(1):153-9. https://doi.org/10.1007/s00244-007-9095-0 PMID: 18157496.
Kapka-Skrzypczak L, Sawicki K, Czajka M, Turski WA, Kruszewski M. Cholinesterase activity in blood and pesticide presence in sweat as biomarkers of children’s environmental exposure to crop protection chemicals. Ann Agric Environ Med. 2015; 22(3):478-82. https://doi.org/10.5604/12321966.1167718 PMID: 26403119.
Dhananjayan V, Ravichandran B, Anitha N, Rajmohan HR. Assessment of acetylcholinesterase and butyrylcholinesterase activities in the blood plasma of agriculture workers. Indian J Occup Environ Med. 2012; 16(3):127-30. https://doi.org/10.4103/0019-5278.111755 PMID: 23776322; PMCID: PMC3683181.
Ranjbar A, Solhi H, Mashayekhi FJ, Susanabdi A, Rezaie A, Abdollahi M. Oxidative stress in acute human poisoning with organophosphorus insecticides; a case-control study. Environ Toxicol Pharmacol. 2005; 20(1):88-91. https://doi.org/10.1016/j.etap.2004.10.007 PMID: 21783573.
Shadnia S, Azizi E, Hosseini R, Khoei S, Fouladdel S, Pajoumand A, Jalali N, Abdollahi M. Evaluation of oxidative stress and genotoxicity in organophosphorus insecticide formulators. Hum Exp Toxicol. 2005; 24(9):439-45. https:// doi.org/10.1191/0960327105ht549oa PMID: 16235732.
Ogut S, Gultekin F, Kisioglu AN, Kucukoner E. Oxidative stress in the blood of farm workers following intensive pesticide exposure. Toxicol Ind Health. 2011; 27(9):8205. https://doi.org/10.1177/0748233711399311 PMID: 21450927.
Banerjee BD, Seth V, Bhattacharya A, Pasha ST, Chakraborty AK. Biochemical effects of some pesticides on lipid peroxidation and free-radical scavengers. Toxicol Lett. 1999; 107(1-3):33-47. https://doi.org/10.1016/S03784274(99)00029-6 PMID: 10414779.
Pearson JN, Patel M. The role of oxidative stress in organophosphate and nerve agent toxicity. Ann N Y Acad Sci. 2016; 1378(1):17-24. https://doi.org/10.1111/ nyas.13115 PMID: 27371936; PMCID: PMC5063722.
Vanova N, Pejchal J, Herman D, Dlabkova A, Jun D. Oxidative stress in organophosphate poisoning: role of standard antidotal therapy. J Appl Toxicol. 2018; 38(8):105870. https://doi.org/10.1002/jat.3605 PMID: 29516527.
Bentley ME, Griffiths PL. The burden of anaemia among women in India. Eur J Clin Nutr. 2003; 57(1):52-60. https:// doi.org/10.1038/sj.ejcn.1601504 PMID: 12548297.
Kapeleka JA, Sauli E, Sadik O, Ndakidemi PA. Biomonitoring of Acetylcholinesterase (AChE) activity among smallholder horticultural farmers occupationally exposed to mixtures of pesticides in Tanzania. J Environ Public Health. 2019; 2019:3084501. https://doi.org/10.1155/2019/3084501 PMID: 31611921; PMCID: PMC6755286.
Ellman GL, Courtney KD, Andres V Jr, Featherstone RM. A new and rapid colourimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961; 7:88-95. https://doi.org/10.1016/0006-2952(61)90145-9 PMID: 13726518.
Chambers JE, Chambers HW. An investigation of acetylcholinesterase inhibition and ageing and choline acetyltransferase activity following high-level acute exposure to paraoxon. Pest Biochem Physiol. 1989; 33:12531. https://doi.org/10.1016/0048-3575(89)90003-5
Raso GM, Meli R, Gualillo O, Pacilio M, Di Carlo R. Prolactin induction of nitric oxide synthase in rat C6 glioma cells. J Neurochem. 1999; 73(6):2272-7. https://doi.org/10.1046/j.1471-4159.1999.0732272.x PMID: 10582584.
Wills ED. Evaluation of lipid peroxidation in lipids and biological membranes. In: Snell K, Mullock B, editors. Biochemical toxicology: a practical approach. Oxford: IRL Press; 1987. p. 127-52.
Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem. 1988; 34(3):497500. https://doi.org/10.1093/clinchem/34.3.497 PMID: 3349599.
Beers RF Jr, Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952; 195(1):133-40. https://doi.org/10.1016/ S0021-9258(19)50881-X PMID: 14938361.
Lakshmi Sundaram R, Vasanthi HR. Dalspinin isolated from Spermacoce hispida (Linn.) protects H9c2 cardiomyocytes from hypoxic injury by modulating oxidative stress and apoptosis. J Ethnopharmacol. 2019; 241:111962. https:// doi.org/10.1016/j.jep.2019.111962 PMID: 31121210.
Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. https://doi.org/10.1016/S00219258(19)52451-6 PMID: 14907713.
Cocco P, Satta G, Dubois S, Pili C, Pilleri M, Zucca M, et al. Lymphoma risk and occupational exposure to pesticides: results of the Epilymph study. Occup Environ Med. 2013; 70(2):91-8. https://doi.org/10.1136/oemed-2012-100845 PMID: 23117219.
Hagmar L, Strömberg U, Tinnerberg H, Mikoczy Z. The usefulness of cytogenetic biomarkers as intermediate endpoints in carcinogenesis. Int J Hyg Environ Health. 2001; 204(1):43-7. https://doi.org/10.1078/1438-463900071 PMID: 11725344.
Alavanja MC, Hoppin JA, Kamel F. Health effects of chronic pesticide exposure: cancer and neurotoxicity. Annu Rev Public Health. 2004; 25:155-97. https://doi.org/10.1146/ annurev.publhealth.25.101802.123020 PMID: 15015917.
Hanke W, Jurewicz J. The risk of adverse reproductive and developmental disorders due to occupational pesticide exposure: an overview of current epidemiological evidence. Int J Occup Med Environ Health. 2004; 17(2):223-43.
McCauley LA, Anger WK, Keifer M, Langley R, Robson MG, Rohlman D. Studying health outcomes in farmworker populations exposed to pesticides. Environ Health Perspect. 2006; 114(6):953-60. https://doi.org/10.1289/ehp.8526 PMID: 16760000. PMCID: PMC1480483.
Bishnu A, Chakrabarti K, Chakraborty A, Saha T. Pesticide residue level in tea ecosystems of Hill and Dooars regions of West Bengal, India. Environ Monit Assess. 2009; 149(14):457-64. https://doi.org/10.1007/s10661-008-0222-9 PMID: 18286381.
Singh S, Bhutia D, Sarkar S, Rai BK, Pal J, Bhattacharjee S, et al. Analyses of pesticide residues in water, sediment and fish tissue from river Deomoni flowing through the tea gardens of Terai Region of West Bengal, India. Int J Fish Aquat Stud. 2015; 3:17-23.
Vidyasagar J, Karunakar N, Reddy MS, Rajnarayana K, Surender T, Krishna DR. Oxidative stress and antioxidant status in acute organophosphorous insecticide poisoning. Indian J Pharmacol. 2004; 37:76-9.
Singh S, Kumar V, Thakur S, Banerjee BD, Chandna S, Rautela RS, et al. DNA damage and cholinesterase activity in occupational workers exposed to pesticides. Environ Toxicol Pharmacol. 2011; 31(2):278-85. https://doi.org/10.1016/j.etap.2010.11.005 PMID: 21787695.
Crane AL, Abdel Rasoul G, Ismail AA, Hendy O, Bonner MR, Lasarev MR, et al. Longitudinal assessment of chlorpyrifos exposure and effect biomarkers in adolescent Egyptian agricultural workers. J Expo Sci Environ Epidemiol. 2013; 23(4):356-62. https://doi.org/10.1038/ jes.2012.113 PMID: 23321857. PMCID: PMC3926695.
García-García CR, Parrón T, Requena M, Alarcón R, Tsatsakis AM, Hernández AF. Occupational pesticide exposure and adverse health effects at the clinical, haematological and biochemical levels. Life Sci. 2016; 145:274-83. https://doi.org/10.1016/j.lfs.2015.10.013 PMID: 26475762.
Jeong JY, Kim M, Park SH, Kim B, Oh SI, Kim E, et al. Residual level, histology, and blood biochemistry of tebuconazole: A repeated dose 28-day oral toxicity study in pigs. Food Sci Anim Resour. 2022; 42(4):712-22. https:// doi.org/10.5851/kosfa.2022.e31 PMID: 35855269. PMCID: PMC9289805.
Kori RK, Singh MK, Jain AK, Yadav RS. Neurochemical and behavioural dysfunctions in pesticide exposed farm workers: A clinical outcome. Indian J Clin Biochem. 2018; 33(4):372-81. https://doi.org/10.1007/s12291-018-0791-5 PMID: 30319182. PMCID: PMC6170243.
Ahmadi N, Mandegary A, Jamshidzadeh A, MohammadiSardoo M, Mohammadi-Sardo M, Salari E, et al. Haematological abnormality, oxidative stress, and genotoxicity induction in the greenhouse pesticide sprayers; investigating the role of NQO1 gene polymorphism. Toxics. 2018; 6(1):13. https://doi.org/10.3390/toxics6010013 PMID: 29414880. PMCID: PMC5874786.
Abdollahi M, Mostafalou S, Pournourmohammadi S, Shadnia S. Oxidative stress and cholinesterase inhibition in saliva and plasma of rats following subchronic exposure to malathion. Comp Biochem Physiol C Toxicol Pharmacol. 2004; 137(1):29-34. https://doi.org/10.1016/j.cca.2003.11.002 PMID: 14984701.
Muniz JF, McCauley L, Scherer J, Lasarev M, Koshy M, Kow YW, et al. Biomarkers of oxidative stress and DNA damage in agricultural workers: a pilot study. Toxicol Appl Pharmacol. 2008; 227(1):97-107. https://doi.org/10.1016/j.taap.2007.10.027 PMID: 18086483.
Oncu M, Gultekin F, Karaöz E, Altuntas I, Delibas N. Nephrotoxicity in rats induced by chlorpryfos-ethyl and ameliorating effects of antioxidants. Hum Exp Toxicol. 2002; 21(4):223-30. https://doi.org/10.1191/0960327102ht225oa PMID: 12099624.
Bagchi D, Bagchi M, Hassoun EA, Stohs SJ. In vitro and in vivo generation of reactive oxygen species, DNA damage and lactate dehydrogenase leakage by selected pesticides. Toxicology. 1995; 104(1-3):129-40. https://doi.org/10.1016/0300-483X(95)03156-A PMID: 8560491.
Maiti PK, Kar A, Gupta P, Chaurasia SS. Loss of membrane integrity and inhibition of type-I iodothyronine 5’-mono deiodinase activity by fenvalerate in the female mouse. Biochem Biophys Res Commun. 1995; 214(3):905-9. https://doi.org/10.1006/bbrc.1995.2372 PMID: 7575562.
Prakasam A, Sethupathy S, Lalitha S. Plasma and RBCs antioxidant status in occupational male pesticide sprayers. Clin Chim Acta. 2001; 310(2):107-12. https://doi.org/10.1016/S0009-8981(01)00487-9 PMID: 11498075.
López O, Hernández AF, Rodrigo L, Gil F, Pena G, Serrano JL, et al. Changes in antioxidant enzymes in humans with long-term exposure to pesticides. Toxicol Lett. 2007; 171(3):146-53. https://doi.org/10.1016/j.toxlet.2007.05.004 PMID: 17590542.
Lefaki M, Papaevgeniou N, Chondrogianni N. Redox regulation of proteasome function. Redox Biol. 2017; 13:452-8. https://doi.org/10.1016/j.redox.2017.07.005 PMID: 28715730; PMCID: PMC5512181.
Zhang J, Wang X, Vikash V, Ye Q, Wu D, Liu Y, et al. ROS and ROS-mediated cellular signalling. Oxid Med Cell Longev. 2016; 2016:4350965. https://doi.org/10.1155/2016/4350965 PMID: 26998193; PMCID: PMC4779832.
Tian H, Zhang B, Di J, Jiang G, Chen F, Li H, et al. Keap1: one stone kills three birds Nrf2, IKKβ and Bcl-2/Bcl-xL. Cancer Lett. 2012; 325(1):26-34. https://doi.org/10.1016/j.canlet.2012.06.007 PMID: 22743616.
Nordgren KK, Wallace KB. Keap1 redox-dependent regulation of doxorubicin-induced oxidative stress response in cardiac myoblasts. Toxicol Appl Pharmacol. 2014; 274(1):107-16. https://doi.org/10.1016/j.taap.2013.10.023 PMID: 24211725.
Kanzaki H, Shinohara F, Kajiya M, Kodama T. The Keap1/Nrf2 protein axis plays a role in osteoclast differentiation by regulating intracellular reactive oxygen species signalling. J Biol Chem. 2013; 288(32):23009-20. https://doi.org/10.1074/jbc.M113.478545 PMID: 23801334; PMCID: PMC3743476.
