Abstract
This study aimed to evaluate biomarkers of exposure to cholinesterase inhibitors insecticides (AChE and BuChE activities) and metals (As, Cd, Cr, Mn, Ni, and Pb blood levels) and their associations with biochemical, hematological, and immunological parameters in farmers from Southern Brazil. One hundred and sixteen individuals were divided into two groups: 62 farmers (exposed group) and 54 subjects non-occupationally exposed (NOE) to agrochemicals. Erythrocyte (AChE) and serum (BuChE) cholinesterases activities were significantly reduced as well as blood Cd and Pb levels were increased in farmers when compared to NOE group (p < 0.05). Farmers presented increased glucose and urea levels compared to NOE group, which were inversely associated with AChE and positively correlated with Cd (p < 0.05), respectively. In addition, Cd was inversely associated with the hematological cells counts, which were significantly reduced in farmers (p < 0.05). C3 complement was higher in farmers and was positively associated with blood Pb (p < 0.05). Surface protein expression analysis revealed a downregulation of LFA-1 and ICAM-1 in farmers. Inverse associations were found between LFA-1 and blood As, Cr, and Ni levels (p < 0.05). Taken together, our results pointed to a relationship between agrochemicals and metals exposure and biochemical, hematological, and immunological disorders that can lead to several chronic conditions.
Similar content being viewed by others
References
Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaie A (2004) Pesticides and oxidative stress: a review. Med Sci Monit 10(6):RA141–RA147 http://www.MedSciMonit.com/pub/vol_10/no_6/4163.pdf
Adu P, Forkuo EK, Issah A, Asumadu IO, Cadman-Sackey E, Quarshie AAA, Gyabaa S, Epharaim RKD (2019) High incidence of moderately reduced renal function and lead bioaccumulation in agricultural workers in assin south district, Ghana: a community-based case-control study. Int J Nephrol 2019:5368427. https://doi.org/10.1155/2019/5368427
Aguilera G, Colín-González AL, Rangel-López E, Chavarría A, Santamaría A (2018) Redox signaling, neuroinflammation, and neurodegeneration. Antioxid Redox Signal 28(18):1626–1651. https://doi.org/10.1089/ars.2017.7099
ATSDR – The Agency for Toxic Substances and Disease Registry (2012). Draft toxicological profile for cadmium. https://www.atsdr.cdc.gov/toxprofiles/tp.asp?id=48&tid=15. Accessed 15 Jan 2019
ATSDR – The Agency for Toxic Substances and Disease Registry (2015) Tox Guide. https://www.atsdr.cdc.gov/toxguides/index.asp. Accessed 15 Jan 2018
Baierle M, Charão MF, Göethel G, Barth A, Fracasso R, Bubols G, Sauer E, Campanharo SC, Rocha RCC, Saint’Pierre TD, Bordignon S, Zibetti M, Trentini CM, Avila DS, Gioda A, Garcia SC (2014) Are delta-aminolevulinate dehydratase inhibition and metal concentrations additional factors for the age-related cognitive decline? Int J Environ Res Public Health 11(10):10851–10867. https://doi.org/10.3390/ijerph111010851
Benedetti D, Nunes E, Sarmento M, Porto C, Santos CEI, Dias JF, Silva J (2013) Genetic damage in soybean workers exposed to pesticides: evaluation with the comet and buccal micronucleus cytome assays. Mutat Res 752(1–2):28–33. https://doi.org/10.1016/j.mrgentox.2013.01.001
Brucker N, Moro A, Charão M, Bubols G, Nascimento S, Goethel G, Barth A, Prohmann AC, Rocha R, Moresco R, Sangoi M, Hausen BS, Saint’Pierre T, Gioda A, Duarte M, Castro I, Saldiva PH, Garcia SC (2015) Relationship between blood metals and inflammation in taxi drivers. Clin Chim Acta 444:176–181. https://doi.org/10.1016/j.cca.2015.02.032
Carneiro FF, Rigotto RM, Augusto LGS, Friedrich K, Búrigo AC (2015) Dossiê ABRASCO: um alerta sobre os impactos dos agrotóxicos na saúde. Rio de Janeiro, Escola Politécnica de Saúde Joaquim Venâncio; Expressão Popular
Carrano AV, Natarajan AT (1988) International Commission for Protection against Environmental Mutagens and Carcinogens. ICPEMC publication no. 14. Considerations for population monitoring using cytogenetic techniques. Mutat Res 204(3):379–406. https://doi.org/10.1016/0165-1218(88)90036-5
Csavina J, Field J, Taylor MP, Gao S, Landázuri A, Betterton EA, Sáez E (2012) A review on the importance of metals and metalloids in atmospheric dust and aerosol from mining operations. Sci Total Environ 433:58–73. https://doi.org/10.1016/j.scitotenv.2012.06.013
da Silva J (2016) DNA damage induced by occupational and environmental exposure to miscellaneous chemicals. Mutat Res 770(Pt A):170–182. https://doi.org/10.1016/j.mrrev.2016.02.002
Defarge N, Spiroux de Vendômois J, Séralini GE (2018) Toxicity of formulants and heavy metals in glyphosate-based herbicides and other pesticides. Toxicol Rep 5:156–163. https://doi.org/10.1016/j.toxrep.2017.12.025
Donmez HH, Donmez N, Kisadere I, Undag I (2019) Protective effect of quercetin on some hematological parameters in rats exposed to cadmium. Biotech Histochem 94(5):381–386. https://doi.org/10.1080/10520295.2019.1574027
Duarte I, Mendonça RF, Korkes KL, Lazzarini R, Hafner MFS (2018) Nickel, chromium and cobalt: the relevant allergens in allergic contact dermatitis. Comparative study between two periods: 1995-2002 and 2003-2015. An Bras Dermatol 93(1):59–62. https://doi.org/10.1590/abd1806-4841.20186047
Duttaroy A, Zimliki CL, Gautam D, Cui Y, Mears D, Wess J (2004) Muscarinic stimulation of pancreatic insulin and glucagon release is abolished in m3 muscarinic acetylcholine receptor-deficient mice. Diabetes 53(7):1714–1720. https://doi.org/10.2337/diabetes.53.7.1714
Ellmann G, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of activity acetylcholinesterase. Biochem Pharmacol 7(2):88–95. https://doi.org/10.1016/0006-2952(61)90145-9
Fenga C, Gangemi S, Di Salvatore V, Falzone L, Libra M (2017) Immunological effects of occupational exposure to lead (review). Mol Med Rep 15(5):3355–3360. https://doi.org/10.3892/mmr.2017.6381
Gorman Ng M, Stjernberg E, Koehoorn M, Demers PA, Davies HW (2011) Exposure to pesticides and metal contaminants of fertilizer among tree planters. Ann Occup Hyg 55(7):752–763. https://doi.org/10.1093/annhyg/mer029
Gupta VK, Singh S, Agrawal A, Siddiqi NJ, Sharma B (2015) Phytochemicals mediated remediation of neurotoxicity induced by heavy metals. Biochem Res Int 2015:534769–534769. https://doi.org/10.1155/2015/534769
Harlin KS, Ross PF (1990) Enzymatic-spectrophotometric method for determination of cholinesterase activity in whole blood: collaborative study. J Assoc Off Anal Chem 73(4):616–619. https://europepmc.org/article/med/2211485
Hassanin NM, Awad OM, El-Fiki S, Abou-Shanab RAI, Abou-Shanab ARA, Amer RA (2018) Association between exposure to pesticides and disorder on hematological parameters and kidney function in male agricultural workers. Environ Sci Pollut Res Int 25(31):30802–30807. https://doi.org/10.1007/s11356-017-8958-9
Hernandez AF, López O, Rodrigo L, Gil F, Pena G, Serrano JL, Parrón T, Alvarez JC, Lorente JA, Pla A (2005) Changes in erythrocyte enzymes in humans long-term exposed to pesticides: influence of several markers of individual susceptibility. Toxicol Lett 159(1):13–21. https://doi.org/10.1016/j.toxlet.2005.04.008
Hoffman N, Tran V, Daniyan A, Ojugbele O, Pryor SC, Bonventre JÁ, Flynn K, Weeks BS (2006. Bifenthrin activates homotypic aggregation in human T-cell lines. Med Sci Monit 12(3): BR87–BR94. http://www.medscimonit.com/abstract/index/idArt/447101. Accessed 19 Jan 2018
Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68:167–182. https://doi.org/10.1093/bmb/ldg032
Jiao W, Chen W, Chang AC, Page AL (2012) Environmental risks of trace elements associated with long-term phosphate fertilizers applications: a review. Environ Pollut 168:44–53. https://doi.org/10.1016/j.envpol.2012.03.052
Juntarawijit C, Juntarawijit Y (2018) Association between diabetes and pesticides: a case-control study among Thai farmers. Environ Health Prev Med 23(1):3. https://doi.org/10.1186/s12199-018-0692-5
Kamel F, Hoppin JA (2004) Association of pesticide exposure with neurologic dysfunction and disease. Environ Health Perspect 112(9):950–958. https://doi.org/10.1289/ehp.7135
Kapka-Skrzypczak L, Sawicki K, Czajka M, Turski WA, Kruszewski M (2015) Cholinesterase activity in blood and pesticide presence in sweat as biomarkers of children’s environmental exposure to crop protection chemicals. Ann Agric Environ Med 22(3):478–482. https://doi.org/10.5604/12321966.1167718
Karami-Mohajeri S, Abdollahi M (2013) Mitochondrial dysfunction and organophosphorus compounds. Toxicol Appl Pharmacol 270(1):39–44. https://doi.org/10.1016/j.taap.2013.04.001
Klein C, Nieder P, Wagner M, Köhler H, Bittinger F, Kirkpatrick CJ, Lewis JC (1994) The role of metal corrosion in inflammatory processes: induction of adhesion molecules by heavy metal ions. J Mater Sci Mater Med 5(11):798–807. https://doi.org/10.1007/BF00213138
Kumar A, Yegla B, Foster TC (2018) Redox signaling in neurotransmission and cognition during aging. Antioxid Redox Signal 28(18):1724–1745. https://doi.org/10.1089/ars.2017.7111
Lionetto MG, Caricato R, Calisi A, Giordano ME, Schettino T (2013) Acetylcholinesterase as a biomarker in environmental and occupational medicine: new insights and future perspectives. Biomed Res Int 2013:321213–321218. https://doi.org/10.1155/2013/321213
Maqbool F, Mostafalou S, Bahadar H, Abdollahi M (2016) Review of endocrine disorders associated with environmental toxicants and possible involved mechanisms. Life Sci 145:265–273. https://doi.org/10.1016/j.lfs.2015.10.022
Martinez-Valenzuela C, Gómez-Arroyo S, Villalobos-Pietrini R, Waliszewski S, Calderón-Segura ME, Félix-Gastélum R, Alvarez-Torres A (2009) Genotoxic biomonitoring of agricultural workers exposed to pesticides in the north of Sinaloa State, Mexico. Environ Int 35(8):1155–1159. https://doi.org/10.1016/j.envint.2009.07.010
Merle NS, Noe R, Halbwachs-Mecarelli L, Fremeaux-Bacchi V, Roumenina RT (2015) Complement system part II: role in immunity. Front Immunol 6:257. https://doi.org/10.3389/fimmu.2015.00257
Mokarizadeh A, Faryabi MR, Rezvanfar MA, Abdollahi M (2015) A comprehensive review of pesticides and the immune dysregulation: mechanisms, evidence and consequences. Toxicol Mech Methods 25(4):258–278. https://doi.org/10.3109/15376516.2015.1020182
Mora AM, Wendel de Joode B, Mergler D, Córdoba L, Cano C, Quesada R, Smith DR, Menezes-Filho JA, Lundh T, Lindh CH, Bradman A, Eskenazi B (2014) Blood and hair manganese concentrations in pregnant women from the infants' environmental health study (ISA) in Costa Rica. Environ Sci Technol 48(6):3467–3476. https://doi.org/10.1021/es404279r
Moretto A, Colosio C (2013) The role of pesticide exposure in the genesis of Parkinson's disease: epidemiological studies and experimental data. Toxicology 307:24–34. https://doi.org/10.1016/j.tox.2012.11.021
Mostafalou S, Eghbal MA, Nili-Ahmadabadi A, Baeeri M, Abdollahi M (2012) Biochemical evidence on the potential role of organophosphates in hepatic glucose metabolism toward insulin resistance through inflammatory signaling and free radical pathways. Toxicol Ind Health 28(9):840–851. https://doi.org/10.1177/0748233711425073
Nascimento SN, Charão MF, Moro AM, Roehrs M, Paniz C, Baierle M, Brucker N, Gioda A, Barbosa F Jr, Bohrer D, Ávila DS, Garcia SC (2014) Evaluation of toxic metals and essential elements in children with learning disabilities from a rural area of southern Brazil. Int J Environ Res Public Health 11(10):10806–10823. https://doi.org/10.3390/ijerph111010806
Nascimento S, Baierle M, Göethel G, Barth A, Brucker N, Charão M, Sauer E, Gauer B, Arbo MD, Altknecht L, Jager M, Dias ACG, Salles JF, Saint’Pierre T, Gioda A, Moresco R, Garcia SC (2016) Associations among environmental exposure to manganese, neuropsychological performance, oxidative damage and kidney biomarkers in children. Environ Res 147:32–43. https://doi.org/10.1016/j.envres.2016.01.035
Nascimento S, Göethel G, Gauer B, Sauer E, Nardi J, Cestonaro L, Correia D, Peruzzi C, Mota L, Machry RV, Furlanetto TW, Saint’Pierre T, Gioda A, Arbo MD, Garcia SC (2018) Exposure to environment chemicals and its possible role in endocrine disruption of children from a rural area. Environ Res 167:488–498. https://doi.org/10.1016/j.envres.2018.07.039
Pai MH, Chien YW, Tsai YH, Hu YM, Yeh SL (2008) Glutamine reduces the expression of leukocyte integrins leukocyte function-associated antigen-1 and macrophage antigen-1 in mice exposed to arsenic. Nutr Res 28(8):544–549. https://doi.org/10.1016/j.nutres.2008.05.004
Panahi P, Vosough-Ghanbari S, Pournourmohammadi S, Ostad SN, Nikfar S, Minaie B, Abdollahi M (2006) Stimulatory effects of malathion on the key enzymes activities of insulin secretion in langerhans islets, glutamate dehydrogenase and glucokinase. Toxicol Mech Methods 16(4):161–167. https://doi.org/10.1080/15376520500191623
Park S, Kim SK, Kim JY, Lee K, Choi JR, Chang SJ, Chung CH, Park KS, Oh SS, Hoh SB (2019) Exposure to pesticides and the prevalence of diabetes in a rural population in Korea. Neurotoxicology 70:12–18. https://doi.org/10.1016/j.neuro.2018.10.007
Pohanka M (2014) Inhibitors of acetylcholinesterase and butyrylcholinesterase meet immunity. Int J Mol Sci 15(6):9809–9825. https://doi.org/10.3390/ijms15069809
Pournourmohammadi S, Farzami B, Ostad SN, Azizi E, Abdollahi M (2005) Effects of malathion subchronic exposure on rat skeletal muscle glucose metabolism. Environ Toxicol Pharmacol 19(1):191–196. https://doi.org/10.1016/j.etap.2004.07.002
Prozialeck WC, Lamar PC, Edwards JR (2016) Effects of sub-chronic Cd exposure on levels of copper, selenium, zinc, iron and other essential metals in rat renal cortex. Toxicol Rep 3:740–746. https://doi.org/10.1016/j.toxrep.2016.09.005
Quinteros E, Ribó A, Mejía R, López A, Belteton W, Comandari A, Orantes CM, Pleites EB, Hernández CE, López DL (2017) Heavy metals and pesticide exposure from agricultural activities and former agrochemical factory in a Salvadoran rural community. Environ Sci Pollut Res Int 24(2):1662–1676. https://doi.org/10.1007/s11356-016-7899-z
Rahimi R, Abdollahi M (2007) A review on the mechanisms involved in hyperglycemia induced by organophosphorus pesticides. Pesticide Biochem Physiol 88(2):115–121. https://doi.org/10.1016/j.tox.2014.04.009
Rocha GHO, Lini RS, Barbosa F Jr, Batista BL, Souza VCO, Nerilo SB, Bando E, Mossini SAG, Nishiyama P (2015) Exposure to heavy metals due to pesticide use by vineyard farmers. Int Arch Occup Environ Health 88(7):875–880. https://doi.org/10.1007/s00420-014-1010-1
Sauvé S, Cook N, Hendershot WH, McBride MB (1996) Linking plant tissue concentrations and soil copper pools in urban contaminated soils. Environ Pollut 94(2):153–157. https://doi.org/10.1016/s0269-7491(96)00081-4
Scott-Taylor TH, Axinia SC, Amin S, Pettengell R (2018) Immunoglobulin G; structure and functional implications of different subclass modifications in initiation and resolution of allergy. Immun Inflamm Dis 6(1):13–33. https://doi.org/10.1002/iid3.192
Sharma B, Singh S, Siddiqi NJ (2014) Biomedical implications of heavy metals induced imbalances in redox systems. Biomed Res Int 2014:640754–640726. https://doi.org/10.1155/2014/640754
Silverio ACP, Machado SC, Azevedo L, Nogueira DA, Graciano MMC, Simões JS, Viana ALM, Martins I (2017) Assessment of exposure to pesticides in rural workers in southern of Minas Gerais, Brazil. Environ Toxicol Pharmacol 55:99–106. https://doi.org/10.1016/j.etap.2017.08.013
Sungur M, Guven M (2001) Intensive care management of organophosphate insecticide poisoning. Crit Care 5(4):211–215. https://doi.org/10.1186/cc1025
Trost BM, Tracy JS (2017) Carbon-nitrogen bond formation via the vanadium oxo catalyzed sigmatropic functionalization of allenols. Org Lett 19(10):2630–2633. https://doi.org/10.1021/acs.orglett.7b00961
WHO, World Health Organization (1996) Trace elements in Human Nutrition and Health. WHO, Geneva, Switzerland
WHO – World Health Organization (2016) Health topics - Pesticides. http://www.who.int/topics/pesticides/.
Wysocki J, Kalina Z, Owczarzy I (1985) Serum levels of immunoglobulins and C3 component of complement in persons occupationally exposed to chlorinated pesticides. Med Pr 36(2):111–117
Xiao X (2017) Effects of permethrin, a pyrethroid insecticide, on glucose and lipid metabolism. Doctoral Dissertations, University of Massachusetts Amherst
Yuan G, Dai S, Yin Z, Lu H, Jia R, Xu J, Song X, Li L, Shu Y, Zhao X (2014) Toxicological assessment of combined lead and cadmium: acute and sub-chronic toxicity study in rats. Food Chem Toxicol 65:260–268. https://doi.org/10.1016/j.fct.2013.12.041
Zodape GV, Tayade M (2016) Presence of metals Cu, Zn, Fe, Na and Pb, in commercially important Shrimp’s and water sediments collected from Gorai creak of Mumbai suburb of west coast, India. Modern Environ Sci Eng 2:302–311. https://doi.org/10.15341/mese(2333-2581)/05.02.2016/003
Acknowledgments
The authors would like to thank the volunteers from Agudo and Porto Alegre, RS, Brazil. Especially to the Banrisul and Mr. Sérgio Arantes who were essential for the development of this study. The authors wish to thank all the people who volunteered to participate in this study. The authors are also grateful to Fernando Freitas and Otávio Lovison for their help during sample collection.
Funding
This work was supported by (FAPERGS/MS/CNPq/SESRS n. 03 2017 – PPSUS 2017, grant to S.C. Garcia), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES/PROEX), PROREXT/UFRGS and also Conselho Nacional de Pesquisa e Desenvolvimento (CNPq)/Universal (n°420379/2016-9, grant to M.D. Arbo). L.V. Cestonaro received a CAPES MSc. research fellowship. S.C.Garcia was receipt of a CNPq Research Fellowship.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest:
Additional information
Responsible editor: Lotfi Aleya
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cestonaro, L.V., Garcia, S.C., Nascimento, S. et al. Biochemical, hematological and immunological parameters and relationship with occupational exposure to pesticides and metals. Environ Sci Pollut Res 27, 29291–29302 (2020). https://doi.org/10.1007/s11356-020-09203-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-09203-3