Next Article in Journal
Effects of Digestion, Cell Culture Media, and Mucous on the Physical Properties, Cellular Effects, and Translocation of Polystyrene and Polymethacrylate Nanoparticles
Next Article in Special Issue
K252a Prevents Microglial Activation Induced by Anoxic Stimulation of Carotid Bodies in Rats
Previous Article in Journal
Rapid Assessment of Ocular Toxicity from Environmental Contaminants Based on Visually Mediated Zebrafish Behavior Studies
Previous Article in Special Issue
Hand Sanitizer Gels: Classification, Challenges, and the Future of Multipurpose Hand Hygiene Products
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Toxics
Volume 11
Issue 8
10.3390/toxics11080707
toxics-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Hematological and Biochemical Effects from Pesticide Exposure on Thai Vegetable Farmers

by
Siriphan Bunsri
1,
Nutnichawan Muenchamnan
1,
Warangkana Naksen
1,* and
Parichat Ong-Artborirak
1,2,*
1
Faculty of Public Health, Chiang Mai University, Chiang Mai 50200, Thailand
2
Department of Research and Medical Innovation, Faculty of Medicine Vajira Hospital, Navamindradhiraj University, Bangkok 10300, Thailand
*
Authors to whom correspondence should be addressed.
Toxics 2023, 11(8), 707; https://doi.org/10.3390/toxics11080707
Submission received: 24 July 2023 / Revised: 11 August 2023 / Accepted: 14 August 2023 / Published: 17 August 2023
(This article belongs to the Special Issue Environmental and Occupational Exposure to Chemical Agents and Health Challenges)
Browse Figure
Versions Notes

Abstract

:
Pesticide-related health concerns are a global public health issue. Few studies in Thailand have explored the hematological and biochemical effects of occupational pesticide exposure. The goal of this study was to investigate the effects of pesticides on the hematology, hepatic, and renal function of Thai vegetable farmers. A cross-sectional study was carried out in Chiang Mai, northern Thailand. A total of 124 apparently healthy vegetable farmers were interviewed about their lifetime exposure to agricultural pesticides. Blood samples were collected via venipuncture to be tested for complete blood count (CBC), liver function, and kidney function. Approximately 46% of the farmers were pesticide users who reported a history of pesticide use for their crops, while 54% were non-pesticide users. In the male farmers, the activities of aspartate aminotransferase (AST), mean corpuscular hemoglobin (MCH), and mean corpuscular hemoglobin concentration (MCHC) were significantly higher in the pesticide users compared to the non-pesticide users, while the estimated glomerular filtration rate (eGFR), hematocrit (HCT), and red blood cells (RBC) were significantly lower (p < 0.05). In the females, the pesticide users had significantly higher levels of alanine aminotransferase (ALT), alkaline phosphatase (ALP), and MCHC than the non-pesticide users (p < 0.05). Pesticide use among Thai vegetable farmers may cause hematological alterations and increase the risk of hepatic and renal dysfunction. Some hematological and biochemical parameters may be used for monitoring to protect them from the adverse health effects of occupational exposure to pesticides.

1. Introduction

Pesticides are still widely used in agriculture around the world. Thailand is an agricultural country that imports a large amount of chemicals, mostly glyphosate for herbicides and abamectin for insecticides [1]. Illegal and excessive pesticide use, as well as poor exposure prevention behaviors, such as using personal protective equipment (PPE) during pesticide application, have been noted among Thai farmers, particularly those who grow vegetables [2,3]. The use of pesticides can have both acute and chronic negative effects on human health, with a direct impact on farmers, and can also cause ecosystem damage, mainly affecting animals [4,5,6]. It is estimated that about 44% of farmers are poisoned by pesticides annually [7]. Exposure to pesticides may cause oxidative stress and DNA damage [8,9]. Many studies have also found an increased risk of cancers such as non-Hodgkin lymphoma, leukemia, brain, prostate, kidney, and liver [10,11,12,13,14].
Exposure to different pesticides may impact organ functions due to their cytotoxic effects, and multiple biomarkers may be used to monitor the early adverse effects of pesticides [15,16]. Numerous studies have revealed that individuals who are exposed to pesticides experience significant hemotoxic effects [16,17,18,19,20,21,22]. A study found significant hematological changes in Thai rice farmers [23]. However, little is known about the hematological effects of pesticide exposure in Thailand.
In addition, the effects of pesticides may include liver and kidney dysfunction, as measured by blood biochemical parameters. Many studies have found changes in liver function indicators, such as serum aspartate aminotransferase (AST), alanine aminotransferase (ALT), and alkaline phosphatase (ALP), associated with occupational pesticide exposure [15,16,20,22,24,25]. Alterations in these enzyme activities among Thai pesticide-using farmers are unclear due to previous studies yielding insignificant results [23,26,27].
According to literature reviews, pesticide exposure is a risk factor for the development of nephrotoxic effects, which include diminished renal function and chronic kidney disease (CKD) [28,29,30,31]. Exposure to certain pesticides may also increase the risk of end-stage renal disease [32]. Several studies have observed associations between exposure to herbicides and insecticides, including carbamates and organophosphates, and a lower estimated glomerular filtration rate (eGFR) [33,34,35,36]. Kidney function alterations have been reported in Thai farmers who use organophosphates and carbamates, depending on their use of PPE [37].
As evidence from research in Thailand is limited, this study was conducted to investigate the effects of pesticides on the hematological and biochemical parameters in vegetable farmers. The findings may be useful for the surveillance and prevention of pesticide-related adverse health effects among Thai farmers.

2. Materials and Methods

This cross-sectional study was conducted on farmers from the Mae On District in the Chiang Mai Province, northern Thailand (Figure 1). Both conventional and organic farmers are located in this agricultural region. The sample size for the study was calculated using the G*Power program for two mean independent comparisons, with a medium effect size of 0.5, power of 80%, and alpha of 5%. We increased the sample size to 25%, totaling 128 farmers. The inclusion criteria included being a male or female vegetable farmer between the ages of 18 and 65, having worked for at least a year, being free of any underlying medical conditions (such as hypertension, diabetes, cirrhosis, or kidney failure), not being pregnant, and being able to communicate in Thai. Convenience sampling was used to recruit study participants who were eligible through public relations by village health volunteers. Due to a sample loss during the data collection, we obtained completed data for 124 farmers at the end. This study protocol was approved by the Committee of Research Ethics, Faculty of Public Health, Chiang Mai University (Document No. ET004/2021). Prior to the data collection, all the study participants provided written informed consent.
The data were collected in 2021 between February and March. A face-to-face interview with the vegetable farmers was conducted by trained research assistants using a questionnaire. The questionnaire contained demographic variables (e.g., gender, age, body mass index, marital status, education, monthly family income, and distance from home to nearest farm), work-related information (e.g., work experience, farm size, and types of vegetables cultivated), health behaviors (e.g., smoking, drinking alcohol, caffeine consumption, supplement use, exercise, food consumption, and daily water consumption), and a question about their lifetime history of mixing or applying agricultural pesticides (ever-/never-use), which showed a good reliability of self-reported information on pesticide use [38]. The farmers were divided into two groups: pesticide users who reported having used pesticides on their crops and non-pesticide users who had never used pesticides. The pesticide users were also asked for additional information on the duration of their pesticide use, pesticide application, pesticide types and trade names, use of personal protective equipment (PPE), keeping and cleaning of agricultural equipment and pesticide containers, and pesticide container disposal.
Blood sampling was performed by nurses via venipuncture in the morning to evaluate the hematological and biological parameters. The blood samples were then transferred to the laboratory of Bangkok RIA Lab Co., Ltd. (Medical Technology Clinic) Chiang Mai Branch located in Chiang Mai, Thailand, which is certified by the Bureau of Laboratory Quality Standards, Ministry of Public Health. The hematological parameters from the complete blood count (CBC) tests included white blood cells (WBC), hemoglobin (HGB), hematocrit (HCT), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC), red blood cells (RBC), and platelets (PLT). The liver function test measured the serum AST, ALT, and ALP. To assess the kidney function, the eGFR was calculated from the creatinine using the CKD-EPI Equation for Whites [39].
The SPSS statistical program (SPSS Inc., Chicago, IL, USA) was used to analyze the data. The results of the study were described using frequency (n), percentage (%), arithmetic mean, standard deviation (SD), and median. The Chi-square test was used to compare the categorical variables, including the demographic characteristics, work-related information, and health behaviors between two farmer groups: pesticide users and non-pesticide users. The independent t-test and Mann–Whitney U test were used to compare differences in the continuous outcomes, such as the hematological and biological parameters for normal and non-normal data distributions, respectively, between the two farmer groups. A p-value of 0.05 was considered to be statistically significant. In this study, the p-values were not adjusted for multiple comparisons to avoid rejecting the null hypothesis, as this may lead to fewer errors of interpretation when the data are actual observations on nature, whereas an adjustment is required in confirmatory studies [40,41].

3. Results

Of the 124 vegetable farmers, 57 (46.0%) were pesticide users who reported a history of using pesticides for their crops, while 67 (54.0%) were non-pesticide users. The personal characteristics and work-related information of the two groups of farmers are shown in Table 1. It was found that the pesticide and non-pesticide users had significantly different sex proportions (p < 0.001). There were no differences in terms of proportions of age, body mass index, marital status, education, monthly family income, farm proximity, work experience, farm size, growing babycorn, and other vegetable cultivation between the two groups of farmers. In terms of health, a significant difference in the proportion of smokers was observed between the farmers who used pesticides and those who did not (p < 0.001), while there was no difference between the two groups in terms of the following health behaviors: alcohol consumption (no/sometimes, always), caffeine drinking (no/sometimes, always), supplement use (no, yes), exercise (no, yes), eating salty foods (very salty, moderately salty, less salty), plant food consumption (occasionally, more than once a week), meat consumption (rarely, every week, every day), and daily water consumption (<5 glasses, 5–7 glasses, 8–10 glasses, 11–13 glasses, >13 glasses). Because of the differences in sex proportions between the two groups, smoking was also observed to be different. As a result, subanalyses of the blood outcomes based on sex were performed.
The pesticide users were 61.4% male (n = 35) and 38.6% female (n = 22). The average duration of pesticide use was 12.2 ± 10.1 years (14.1 ± 10.8 years for males and 9.1 ± 8.3 years for females). There were 89.5% mixers (91.4% for males and 86.4% for females) and 89.5% sprayers (94.3% for males and 81.8% for females). The history of the individual pesticides used by the farmers is shown in Table 2. Paraquat (24.6%) and glyphosate (19.3%) were found to be the herbicides most commonly used by the farmers. Acetamiprid (26.3%) and carbaryl (21.0%) were the most commonly reported insecticides. Approximately 47.4% of the farmers always used all types of PPE when applying pesticides, including hats (93.0%), chemical respirators (49.1%), gloves (91.3%), long-sleeved shirts and long pants (100%), and boots (96.5%). Most kept their agricultural equipment and pesticides in a space separate from their home (54.4%), cleaned their agricultural equipment and containers on the farm (68.4%), and disposed of the pesticide packaging in a landfill (64.9%).
More than 90% of the vegetable farmers had CBC, ALP, AST, ALT, and eGFR values within the normal range. Comparisons of the hematological and biochemical parameters between the pesticide users and non-users are shown in Table 3 and Table 4. In the males, the mean HCT and RBC were significantly lower in the pesticide users compared to the non-users (p < 0.05). There were differences in the medians of the following outcomes between the pesticide users and non-users: MCH (28.7 vs. 27.55 pg), MCHC (32.6 vs. 31.3 g/dL), eGFR (102.55 vs. 112.58 mL/min/1.73 m2), and AST (27 vs. 19 units/L). In the females, the pesticide users had a significantly higher mean ALP than the non-users (p < 0.05). The pesticide users and non-users also had different medians for MCHC (31.2 vs. 30.9 g/dL) and ALT (19 vs. 15 units/L).

4. Discussion

This study demonstrated the hematological and biochemical effects from pesticide exposure on Thai vegetable farmers. In terms of the hematological parameters, the pesticide users had lower HCT and RBC values, higher MCH and MCHC values in the male farmers, and only lower MCHC values in the female farmers. This may have been due to pesticide exposure altering iron homeostasis, which affects the red blood cells [42]. Long-term exposure could disrupt the balance between free radical production and antioxidant defenses, resulting in DNA damage [20]. This significant difference is consistent with previous findings for pesticide-exposed people, such as male pesticide sprayers and agricultural workers, including greenhouse workers [16,17,18,19,20,21,22]. In Thailand, a study found that rice farmers had significantly lower MCH and MCHC values [23], whereas other studies have found no difference in the CBC parameters for pesticide-using farmers [26,27]. These inconsistent results may be due to differences in the pesticide type, frequency, and duration in each study, as well as differences in individual immune responses [31]. Our findings indicated a higher risk of blood disorders such as anemia for vegetable farmers who are repeatedly exposed to pesticides, particularly men.
In our study, the pesticide users had significantly higher levels of serum enzymes that indicate hepatic damage, including AST for males and ALT and ALP for females. Our results are consistent with the findings of earlier studies, which have found elevated levels of these enzyme activities in farmers and agricultural workers, including pesticide sprayers [15,16,20,24,25,43]. High ALT and AST levels may indicate lysis of the liver cells and leakage of enzymes into the blood, causing cytotoxic effects [25]. Elevated ALP levels may be caused by an increased plasma membrane permeability or cellular necrosis [16,44]. Pesticide exposure, such as to organophosphate, may disrupt the liver metabolism and mitochondrial metabolic pathways caused by oxidative damage [45]. According to Khan et al., (2008) [15], pesticide residues such as methomyl, imidacloprid, cypermethrin, and methamidophos were positively correlated with ALT or AST in pesticide-exposed tobacco farmers. In line with these findings, the vegetable growers in our study were also exposed to these pesticides. Even though previous studies on Thai orchid farmers and rice farmers who used pesticides observed no difference in liver function tests such as AST, ALT, and ALP [23,26,27], our findings indicated the potential effects of pesticide exposure on hepatotoxicity among vegetable farmers.
In terms of renal function, eGFR was found to be lower in the male farmers who used pesticides. This significant difference was in agreement with previous findings for pesticide-exposed individuals, in which associations with lower eGFR were observed for organophosphates and carbamates, as well as herbicides such as atrazine and glyphosate [33,34,35,36]. Organophosphate exposure may alter the glomeruli, as well as the proximal and distal tubules [46,47]. Neonicotinoids have been identified as a possible risk factor for renal tubular dysfunction [48]. Renal tubule injury, resulting in inflammation and fibrosis, may also lead to the progression of CKD [49]. Previous research has found that lifetime exposure to pesticides such as glyphosate, paraquat, and organophosphates in paddy fields was associated with CKD in farmers [28]. Among Thai farmers, exposure to organophosphates and carbamates, as well as PPE use, were significantly associated with an increased risk of CKD [37]. This indicates that the farmers investigated in our study may be at a higher risk of renal injury as a result of not always using PPE, in particular chemical respirators. Another study found that glyphosate use and the intensity of exposure were related to serum creatinine, but not to eGFR [50]. Some pesticides used by farmers in this study, such as alachlor, atrazine, glyphosate, paraquat, and permethrin, have been linked to CKD [51]. According to our findings, long-term pesticide exposure may cause nephrotoxic changes and increase the risk of CKD in vegetable farmers.
In addition, these findings emphasize the importance of strict pesticide legislations and preventive measures for Thai farmers. In comparison to other countries, the pesticide regulation in Thailand is characterized by the lack of a consolidated, uniform system designed specifically for pesticide management, which has weakened the enforcement of the current regulations, resulting in pesticide misuse/overuse [2]. Regarding the study’s limitations, the cross-sectional design may not be able to draw a causal relationship between pesticide exposure and changes in the hematological and biochemical parameters. A larger sample size is required to increase the power of the analysis, as the data were subanalyzed based on gender. The study did not look into specific pesticides and the intensity of exposure. A pesticide residue analysis to assess internal exposure, such as urinary metabolites, is recommended for future research. Other factors, such as work clothing and heat stress, may also be considered. However, our findings add to the evidence on the effects of pesticide exposure on hematological and biochemical alterations among Thai farmers.

5. Conclusions

Our findings emphasized that occupational exposure to pesticides may alter hematological and biochemical parameters, reflecting hemotoxic, nephrotoxic, and hepatotoxic effects among Thai vegetable farmers who mixed or sprayed pesticides. These parameters might be useful in tracking the early negative effects of pesticides on Thai farmers’ health. An intensive intervention to provide knowledge about the potential risks of occupational pesticide exposure and promote the appropriate use of PPE, particularly chemical respirators, should be considered to minimize pesticide exposure and prevent health effects in Thai farmers. Moreover, pesticide-related problems must be recognized and prioritized by the government in order to develop effective policies and strategies, as well as to continue extremely strict actions for strengthening the weak legislation and regulations, ultimately leading to an actual reduction in these problems.

Author Contributions

Conceptualization, W.N. and P.O.-A.; methodology, W.N. and P.O.-A.; software, S.B.; validation, W.N. and P.O.-A.; formal analysis, S.B. and P.O.-A.; investigation, W.N. and P.O.-A.; resources, S.B. and N.M.; data curation, S.B. and P.O.-A.; writing—original draft preparation, S.B. and N.M.; writing—review and editing, W.N. and P.O.-A.; visualization, S.B. and P.O.-A.; supervision, W.N. and P.O.-A.; project administration, P.O.-A.; funding acquisition, N.M. and P.O.-A. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by CMU Junior Research Fellowship Program, Chiang Mai University.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Committee of Research Ethics, Faculty of Public Health, Chiang Mai University (Document No. ET004/2021).

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data are available upon request from the corresponding author.

Acknowledgments

The authors would like to thank all of the farmers for their participation, as well as the public health officers and village health volunteers for their assistance in this study.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Statistics of Hazardous Chemicals Imported into Thailand. Available online: https://www.doa.go.th/ard/?page_id=386 (accessed on 20 May 2022).
  2. Panuwet, P.; Siriwong, W.; Prapamontol, T.; Ryan, P.B.; Fiedler, N.; Robson, M.G.; Barr, D.B. Agricultural Pesticide Management in Thailand: Situation and Population Health Risk. Environ. Sci. Policy 2012, 17, 72–81. [Google Scholar] [CrossRef] [PubMed]
  3. Kongtip, P.; Nankongnab, N.; Mahaboonpeeti, R.; Bootsikeaw, S.; Batsungnoen, K.; Hanchenlaksh, C.; Tipayamongkholgul, M.; Woskie, S. Differences among Thai agricultural workers’ health, working conditions, and pesticide use by farm type. Ann. Work. Expo. Health 2018, 62, 167–181. [Google Scholar] [CrossRef] [PubMed]
  4. Köhler, H.R.; Triebskorn, R. Wildlife ecotoxicology of pesticides: Can we track effects to the population level and beyond? Science 2013, 341, 759–765. [Google Scholar] [CrossRef] [PubMed]
  5. Tang, F.H.M.; Lenzen, M.; McBratney, A.; Maggi, F. Risk of pesticide pollution at the global scale. Nat. Geosci. 2021, 14, 206–210. [Google Scholar] [CrossRef]
  6. Ziliotto, M.; Kulmann-Leal, B.; Roitman, A.; Bogo Chies, J.A.; Ellwanger, J.H. Pesticide Pollution in the Brazilian Pampa: Detrimental Impacts on Ecosystems and Human Health in a Neglected Biome. Pollutants 2023, 3, 280–292. [Google Scholar] [CrossRef]
  7. Boedeker, W.; Watts, M.; Clausing, P.; Marquez, E. The global distribution of acute unintentional pesticide poisoning: Estimations based on a systematic review. BMC Public Health 2020, 20, 1875. [Google Scholar] [CrossRef]
  8. Kisby, G.E.; Muniz, J.F.; Scherer, J.; Lasarev, M.R.; Koshy, M.; Kow, Y.W.; McCauley, L. Oxidative stress and DNA damage in agricultural workers. J. Agromed. 2009, 14, 206–214. [Google Scholar] [CrossRef]
  9. Ledda, C.; Cannizzaro, E.; Cinà, D.; Filetti, V.; Vitale, E.; Paravizzini, G.; Di Naso, C.; Iavicoli, I.; Rapisarda, V. Oxidative stress and DNA damage in agricultural workers after exposure to pesticides. J. Occup. Med. Toxicol. 2021, 16, 1. [Google Scholar] [CrossRef]
  10. Alavanja, M.C.; Hoppin, J.A.; Kamel, F. Health effects of chronic pesticide exposure: Cancer and neurotoxicity. Annu. Rev. Public Health 2004, 25, 155–197. [Google Scholar] [CrossRef]
  11. Bassil, K.L.; Vakil, C.; Sanborn, M.; Cole, D.C.; Kaur, J.S.; Kerr, K.J. Cancer health effects of pesticides: Systematic review. Can. Fam. Physician 2007, 53, 1704–1711. [Google Scholar]
  12. Xie, B.; Hu, Y.; Liang, Z.; Liu, B.; Zheng, X.; Xie, L. Association between pesticide exposure and risk of kidney cancer: A meta-analysis. Onco Targets Ther. 2016, 28, 3893–3900. [Google Scholar] [CrossRef] [PubMed]
  13. VoPham, T.; Bertrand, K.A.; Hart, J.E.; Laden, F.; Brooks, M.M.; Yuan, J.M.; Talbott, E.O.; Ruddell, D.; Chang, C.H.; Weissfeld, J.L. Pesticide exposure and liver cancer: A review. Cancer Causes Control 2017, 28, 177–190. [Google Scholar] [CrossRef] [PubMed]
  14. Andreotti, G.; Beane Freeman, L.E.; Shearer, J.J.; Lerro, C.C.; Koutros, S.; Parks, C.G.; Blair, A.; Lynch, C.F.; Lubin, J.H.; Sandler, D.P.; et al. Occupational pesticide use and risk of renal cell carcinoma in the Agricultural Health Study. Environ. Health Perspect. 2020, 128, 67011. [Google Scholar] [CrossRef] [PubMed]
  15. Khan, D.A.; Bhatti, M.M.; Khan, F.A.; Naqvi, S.T.; Karam, A. Adverse effects of pesticides residues on biochemical markers in Pakistani tobacco farmers. Int. J. Clin. Exp. Med. 2008, 1, 274–282. [Google Scholar]
  16. Araoud, M.; Neffeti, F.; Douki, W.; Hfaiedh, H.B.; Akrout, M.; Hassine, M.; Najjar, M.F.; Kenani, A. Adverse effects of pesticides on biochemical and haematological parameters in Tunisian agricultural workers. J. Expo. Sci. Environ. Epidemiol. 2012, 22, 243–247. [Google Scholar] [CrossRef]
  17. Patil, J.A.; Patil, A.J.; Govindwar, S.P. Biochemical effects of various pesticides on sprayers of grape gardens. Indian J. Clin. Biochem. 2003, 18, 16–22. [Google Scholar] [CrossRef]
  18. Rastogi, S.K.; Singh, V.K.; Kesavachandran, C.; Jyoti Siddiqui, M.K.; Mathur, N.; Bharti, R.S. Monitoring of plasma butyrylcholinesterase activity and hematological parameters in pesticide sprayers. Indian J. Occup. Environ. Med. 2008, 12, 29–32. [Google Scholar] [CrossRef]
  19. Fareed, M.; Pathak, M.K.; Bihari, V.; Kamal, R.; Srivastava, A.K.; Kesavachandran, C.N. Adverse respiratory health and hematological alterations among agricultural workers occupationally exposed to organophosphate pesticides: A cross-sectional study in North India. PLoS ONE 2013, 8, e69755. [Google Scholar] [CrossRef]
  20. Ahmadi, N.; Mandegary, A.; Jamshidzadeh, A.; Mohammadi-Sardoo, M.; Mohammadi-Sardo, M.; Salari, E.; Pourgholi, L. Hematological abnormality, oxidative stress, and genotoxicity induction in the greenhouse pesticide sprayers; investigating the role of NQO1 gene polymorphism. Toxics 2018, 6, 13. [Google Scholar] [CrossRef]
  21. Leili, M.; Ghafiuri-Khosroshahi, A.; Poorolajal, J.; Samiee, F.; Smadi, M.T.; Bahrami, A. Pesticide residues levels as hematological biomarkers-a case study, blood serum of greenhouse workers in the city of Hamadan, Iran. Environ. Sci. Pollut. Res. Int. 2022, 29, 38450–38463. [Google Scholar] [CrossRef]
  22. Khan, M.; Nazir, I.; Nazir, S.; Wadood, M.; Irfan, G.; Nasir, S.S. Impact of chronic exposure of organophosphorus pesticide on hematological and biochemical parameters of agriculture workers: A cross sectional study. J. Pharm. Negat. Results 2023, 14, 3059–3067. [Google Scholar]
  23. Suwannahong, K.; Sridon, A.; Pongstaporn, W.; Thongmuang, P.; Sudjaroen, Y. Biochemical and Hematological Status in Rice farmers with Chronic Pesticide Exposure, Suphan Buri, Thailand. Indian J. Public Health Res. Dev. 2020, 11, 1285–1290. [Google Scholar]
  24. Patil, J.A.; Patil, A.J.; Sontakke, A.V.; Govindwar, S.P. Occupational pesticides exposure of sprayers of grape gardens in western Maharashtra (India): Effects on liver and kidney function. J. Basic. Clin. Physiol. Pharmacol. 2009, 20, 335–355. [Google Scholar] [CrossRef] [PubMed]
  25. Manfo, F.P.T.; Mboe, S.A.; Nantia, E.A.; Ngoula, F.; Telefo, P.B.; Moundipa, P.F.; Cho-Ngwa, F. Evaluation of the effects of agro pesticides use on liver and kidney function in farmers from Buea, Cameroon. J. Toxicol. 2020, 2020, 2305764. [Google Scholar] [CrossRef] [PubMed]
  26. Aroonvilairat, S.; Kespichayawattana, W.; Sornprachum, T.; Chaisuriya, P.; Siwadune, T.; Ratanabanangkoon, K. Effect of pesticide exposure on immunological, hematological and biochemical parameters in Thai orchid farmers—A cross-sectional study. Int. J. Environ. Res. Public Health 2015, 12, 5846–5861. [Google Scholar] [CrossRef]
  27. Sudjaroen, Y.; Suwannahong, K. Comparison of biochemical, hematological parameters and pesticide expose-related symptoms among organic and non-organic farmers, Singburi, Thailand. Asian J. Pharm. 2017, 11, 235–241. [Google Scholar]
  28. Jayasumana, C.; Paranagama, P.; Agampodi, S.; Wijewardane, C.; Gunatilake, S.; Siribaddana, S. Drinking well water and occupational exposure to Herbicides is associated with chronic kidney disease, in Padavi-Sripura, Sri Lanka. Environ. Health 2015, 14, 6. [Google Scholar] [CrossRef]
  29. Valcke, M.; Levasseur, M.E.; Soares da Silva, A.; Wesseling, C. Pesticide exposures and chronic kidney disease of unknown etiology: An epidemiologic review. Environ. Health 2017, 16, 49. [Google Scholar] [CrossRef]
  30. Prudente, I.R.G.; Cruz, C.L.; Nascimento, L.C.; Kaiser, C.C.; Guimarães, A.G. Evidence of risks of renal function reduction due to occupational exposure to agrochemicals: A systematic review. Environ. Toxicol. Pharmacol. 2018, 63, 21–28. [Google Scholar] [CrossRef]
  31. Wan, E.T.; Darssan, D.; Karatela, S.; Reid, S.A.; Osborne, N.J. Association of pesticides and kidney function among adults in the US population 2001–2010. Int. J. Environ. Res. Public Health 2021, 18, 10249. [Google Scholar] [CrossRef]
  32. Lebov, J.F.; Engel, L.S.; Richardson, D.; Hogan, S.L.; Hoppin, J.A.; Sandler, D.P. Pesticide use and risk of end-stage renal disease among licensed pesticide applicators in the Agricultural Health Study. Occup. Environ. Med. 2016, 73, 3–12. [Google Scholar] [CrossRef]
  33. García-Trabanino, R.; Jarquín, E.; Wesseling, C.; Johnson, R.J.; González-Quiroz, M.; Weiss, I.; Glaser, J.; José Vindell, J.; Stockfelt, L.; Roncal, C.; et al. Heat stress, dehydration, and kidney function in sugarcane cutters in El Salvador--A cross-shift study of workers at risk of Mesoamerican nephropathy. Environ. Res. 2015, 142, 746–755. [Google Scholar] [CrossRef] [PubMed]
  34. Abdul, K.S.M.; De Silva, P.M.C.S.; Ekanayake, E.M.D.V.; Thakshila, W.A.K.G.; Gunarathna, S.D.; Gunasekara, T.D.K.S.C.; Jayasinghe, S.S.; Asanthi, H.B.; Chandana, E.P.S.; Chaminda, G.G.T.; et al. Occupational paraquat and glyphosate exposure may decline renal functions among rural farming communities in Sri Lanka. Int. J. Environ. Res. Public Health 2021, 18, 3278. [Google Scholar] [CrossRef] [PubMed]
  35. Prudente, I.R.G.; Souza, B.R.S.; Nascimento, L.C.; Gonçalves, V.S.D.S.; Silva, D.S.D.; Rabelo, T.K.; Alves, O.; Junior Santos, A.C.; de Rezende Neto, J.M.; Tavares, D.D.S.; et al. Nephrotoxic effects caused by occupational exposure to agrochemicals in a region of Northeastern Brazil: A cross-sectional study. Environ. Toxicol. Chem. 2021, 40, 1132–1138. [Google Scholar] [CrossRef] [PubMed]
  36. Shearer, J.J.; Sandler, D.P.; Andreotti, G.; Murata, K.; Shrestha, S.; Parks, C.G.; Liu, D.; Alavanja, M.C.; Landgren, O.; Beane Freeman, L.E.; et al. Pesticide use and kidney function among farmers in the Biomarkers of Exposure and Effect in Agriculture study. Environ. Res. 2021, 199, 111276. [Google Scholar] [CrossRef] [PubMed]
  37. Sombatsawat, E.; Barr, D.B.; Panuwet, P.; Robson, M.G.; Siriwong, W. Pesticide-induced changes in cholinesterase activity and chronic kidney disease of unknown etiology among farmers in Nakhon Ratchasima, Thailand. Hum. Ecol. Risk Assess. 2021, 27, 2038–2050. [Google Scholar] [CrossRef]
  38. Blair, A.; Tarone, R.; Sandler, D.; Lynch, C.F.; Rowland, A.; Wintersteen, W.; Steen, W.C.; Samanic, C.; Dosemeci, M.; Alavanja, M.C. Reliability of reporting on life-style and agricultural factors by a sample of participants in the Agricultural Health Study from Iowa. Epidemiology 2002, 13, 94–99. [Google Scholar] [CrossRef]
  39. Levey, A.S.; Stevens, L.A.; Schmid, C.H.; Zhang, Y.L.; Castro, A.F.; Feldman, H.I.; Kusek, J.W.; Eggers, P.; Van Lente, F.; Greene, T.; et al. CKD-EPI (Chronic Kidney Disease Epidemiology Collaboration). A new equation to estimate glomerular filtration rate. Ann. Intern. Med. 2009, 150, 604–612. [Google Scholar] [CrossRef]
  40. Rothman, K.J. No adjustments are needed for multiple comparisons. Epidemiology 1990, 1, 43–46. [Google Scholar] [CrossRef]
  41. Bender, R.; Lange, S. Adjusting for multiple testing—When and how? J. Clin. Epidemiol. 2001, 54, 343–349. [Google Scholar] [CrossRef]
  42. Schreinemachers, D.M.; Ghio, A.J. Effects of environmental pollutants on cellular iron homeostasis and ultimate links to human disease. Environ. Health Insights 2016, 10, 35–43. [Google Scholar] [CrossRef] [PubMed]
  43. Wafa, T.; Nadia, K.; Amel, N.; Ikbal, C.; Insaf, T.; Asma, K.; Hedi, M.A.; Mohamed, H. Oxidative stress, hematological and biochemical alterations in farmers exposed to pesticides. J. Environ. Sci. Health B 2013, 48, 1058–1069. [Google Scholar] [CrossRef] [PubMed]
  44. Celik, I.; Yilmaz, Z.; Turkoglu, V. Hematotoxic and hepatotoxic effects of dichlorvos at sublethal dosages in rats. Environ. Toxicol. 2009, 24, 128–132. [Google Scholar] [CrossRef] [PubMed]
  45. Karami-Mohajeri, S.; Ahmadipour, A.; Rahimi, H.R.; Abdollahi, M. Adverse effects of organophosphorus pesticides on the liver: A brief summary of four decades of research. Arh. Za Hig. Rada Toksikol. 2017, 68, 261–275. [Google Scholar] [CrossRef] [PubMed]
  46. Desai, S.N.; Desai, P.V. Changes in renal clearance and renal tubular function in albino mice under the influence of Dichlorvos. Pestic. Biochem. Physiol. 2008, 91, 160–169. [Google Scholar] [CrossRef]
  47. Sobolev, V.E.; Sokolova, M.O.; Jenkins, R.O.; Goncharov, N.V. Molecular mechanisms of acute organophosphate nephrotoxicity. Int. J. Mol. Sci. 2022, 23, 8855. [Google Scholar] [CrossRef]
  48. Taira, K.; Kawakami, T.; Weragoda, S.K.; Herath, H.M.A.S.; Ikenaka, Y.; Fujioka, K.; Hemachandra, M.; Pallewatta, N.; Aoyama, Y.; Ishizuka, M.; et al. Urinary concentrations of neonicotinoid insecticides were related to renal tubular dysfunction and neuropsychological complaints in Dry-zone of Sri Lanka. Sci. Rep. 2021, 11, 22484. [Google Scholar] [CrossRef]
  49. Liu, B.C.; Tang, T.T.; Lv, L.L.; Lan, H.Y. Renal tubule injury: A driving force toward chronic kidney disease. Kidney Int. 2018, 93, 568–579. [Google Scholar] [CrossRef]
  50. Mueangkhiao, P.; Siviroj, P.; Sapbamrer, R.; Khacha-Ananda, S.; Lungkaphin, A.; Seesen, M.; Jaikwang, P.; Wunnapuk, K. Biological variation in kidney injury and kidney function biomarkers among farmers in Lamphun province, Thailand. Environ. Sci. Pollut. Res. Int. 2020, 27, 12386–12394. [Google Scholar] [CrossRef]
  51. Kshirsagar, A.V.; Zeitler, E.M.; Weaver, A.; Franceschini, N.; Engel, L.S. Environmental Exposures and Kidney Disease. Kidney360 2022, 3, 2174–2182. [Google Scholar] [CrossRef]
Toxics 11 00707 g001
Figure 1. Location of study area in Mae On District in Chiang Mai, Thailand. Adapted from https://commons.m.wikimedia.org/wiki/File:Thailand_Chiang_Mai_locator_map.svg, (accessed on 31 July 2023).
Figure 1. Location of study area in Mae On District in Chiang Mai, Thailand. Adapted from https://commons.m.wikimedia.org/wiki/File:Thailand_Chiang_Mai_locator_map.svg, (accessed on 31 July 2023).
Toxics 11 00707 g001
Table 1. Demographic and work characteristics of pesticide and non-pesticide users among vegetable farmers (n = 124).
Table 1. Demographic and work characteristics of pesticide and non-pesticide users among vegetable farmers (n = 124).
FactorPesticide Users (n = 57)Non-Users (n = 67)p-Value
Sex <0.001
Male35 (61.4%)12 (17.9%)
Female22 (38.6%)55 (82.1%)
Age 0.153
≤35 years5 (8.8%)13 (19.4%)
36–55 years34 (59.6%)40 (59.7%)
>55 years18 (31.6%)14 (20.9%)
Body mass index (BMI) 0.261
Underweight (<18.5 kg/m2)1 (1.8%)2 (3.0%)
Normal (18.5–22.9 kg/m2)21 (36.8%)25 (37.3%)
Overweight (23.0–29.9 kg/m2)21 (36.8%)15 (22.4%)
Obese (≥30 kg/m2)14 (24.6%)25 (37.3%)
Marital status 0.079
Single/Divorced/Widowed6 (10.5%)15 (22.4%)
Married51 (89.5%)52 (77.6%)
Education 0.129
Primary school35 (61.4%)32 (47.8%)
Secondary school or higher22 (38.6%)35 (52.2%)
Monthly family income 0.816
<10,000 Baht (<285 USD)25 (43.9%)28 (41.8%)
≥10,000 Baht (≥285 USD)32 (56.1%)39 (58.2%)
Farm proximity 0.489
<300 m.23 (40.4%)23 (34.3%)
>300 m.34 (59.6%)44 (65.7%)
Work experience 0.079
≤5 years11 (19.3%)23 (34.3%)
6–10 years9 (15.8%)14 (20.9%)
11–20 years13 (22.8%)15 (22.4%)
≥21 years24 (42.1%)15 (22.4%)
Farm size 0.170
<8000 m227 (47.4%)40 (59.7%)
≥8000 m230 (52.6%)27 (40.3%)
Growing babycorn 0.186
No23 (40.4%)35 (52.2%)
Yes34 (59.6%)32 (47.8%)
Other vegetable cultivation 0.389
No22 (38.6%)31 (46.3%)
Yes35 (61.4%)36 (53.7%)
Growing rice 0.252
No40 (70.2%)53 (79.1%)
Yes17 (29.8%)14 (20.9%)
Table 2. History of individual pesticide use among vegetable farmers.
Table 2. History of individual pesticide use among vegetable farmers.
Chemical ClassCommon NameWHO ClassPesticide Users (n = 57)
Herbicide 30 (52.6%)
Bipyridylium ParaquatII14 (24.6%)
GlycineGlyphosateIII11 (19.3%)
Phenoxy2,4-DII3 (5.3%)
Chloroacetamide/AnilideAlachlorII1 (1.8%)
TriazinesAtrazineIII1 (1.8%)
Insecticide 48 (84.2%)
OrganophosphateChlorpyrifosII1 (1.8%)
MethamidophosIb1 (1.8%)
DichlorvosIb1 (1.8%)
ProfenofosII1 (1.8%)
CarbamateCarbarylII12 (21.0%)
MethomylIb8 (14.0%)
CarbofuranIb3 (5.3%)
CarbosulfanII2 (3.5%)
NeonicotinoidAcetamipridII15 (26.3%)
ImidaclopridII8 (14.0%)
DinotefuranIII1 (1.8%)
AvermectinAbamectinIb7 (12.3%)
EmamectinII4 (7.0%)
PyrethroidCypermethrinII4 (7.0%)
PhenylpyrazoleFipronilII5 (8.8%)
SpinosynSpinetoramU4 (7.0%)
Note: Ib = Highly hazardous; II = Moderately hazardous; III = Slightly hazardous; and U = Unlikely to present acute hazard in normal use.
Table 3. Hematological parameters between the two groups of vegetable farmers.
Table 3. Hematological parameters between the two groups of vegetable farmers.
Outcome Pesticide Users (n = 57)Non-Users (n = 67)p-Value
Mean (SD)Mean (SD)
WBC
(mm3)		All6979 (1596)6671 (1669)0.299 a
Male7021 (1612)6818 (1323)0.696 a
Female6912 (1605)6639 (1744)0.528 a
HGB
(g/dL)		All13.76 (1.56)12.92 (1.71)0.005 a
Male14.44 (1.20)14.73 (1.42)0.497 a
Female12.69 (1.48)12.52 (1.51)0.666 a
HCT
(%)		All42.84 (4.37)41.64 (5.10)0.166 a
Male44.51 (3.45)47.08 (4.17)0.040 a
Female40.18 (4.44)40.46 (4.50)0.810 a
MCV
(fL)		All84.91 (10.91)81.22 (12.44)0.149 b
Male87.76 (9.33)83.08 (13.07)0.294 b
Female80.36 (11.88)80.81 (12.39)0.588 b
MCH
(pg)		All27.31 (4.05)25.24 (4.07)0.005 b
Male28.56 (3.60)26.01 (4.20)0.047 b
Female25.31 (4.00)25.08 (4.06)0.822 b
MCHC
(g/dL)		All32.11 (1.29)31.05 (0.67)<0.001 b
Male32.48 (1.34)31.29 (0.48)0.017 b
Female31.53 (0.96)31.00 (0.69)0.014 b
RBC
(106/mm3)		All5.10 (0.62)5.18 (0.70)0.502 a
Male5.12 (0.66)5.74 (0.60)0.006 a
Female5.08 (0.57)5.06 (0.67)0.942 a
PLT
(mm3)		All249,947 (58,755)267,567 (58,711)0.098 a
Male234,971 (49,762)240,417 (30,485)0.724 a
Female273,773 (65,024)273,491 (61,839)0.986 a
Abbreviations: WBC, white blood cell; HGB, hemoglobin; HCT, hematocrit; MCV, mean corpuscular volume; MCH, mean corpuscular hemoglobin; MCHC, mean corpuscular hemoglobin concentration; RBC, red blood cell; and PLT, platelets. a Independent t-test; b Mann–Whitney U test.
Table 4. Liver and kidney function tests between the two groups of vegetable farmers.
Table 4. Liver and kidney function tests between the two groups of vegetable farmers.
Outcome Pesticide Users (n = 57)Non-Users (n = 67)p-Value
Mean (SD)Mean (SD)
ALP
(U/L)		All73.84 (24.64)65.30 (20.11)0.036 a
Male71.63 (23.72)71.83 (14.48)0.978 a
Female77.36 (26.22)63.87 (20.98)0.020 a
AST
(U/L)		All29.65 (24.86)18.85 (8.58)<0.001 b
Male35.91 (29.87)24.08 (13.88)0.033 b
Female19.68 (5.87)17.71 (6.58)0.115 b
ALT
(U/L)		All29.28 (24.06)19.57 (14.30)<0.001 b
Male35.83 (28.31)30.17 (20.35)0.366 b
Female18.86 (7.85)17.25 (11.63)0.029 b
eGFR
(mL/min/1.73 m2)		All102.75 (13.59)106.54 (11.56)0.169 b
Male99.66 (14.60)110.00 (11.07)0.020 b
Female107.66 (10.31)105.79 (11.63)0.569 b
Abbreviations: ALP, alkaline phosphatase; AST, aspartate aminotransferase; ALT, alanine aminotransferase; and eGFR, estimated glomerular filtration rate. a Independent t-test; b Mann–Whitney U test.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Bunsri, S.; Muenchamnan, N.; Naksen, W.; Ong-Artborirak, P. The Hematological and Biochemical Effects from Pesticide Exposure on Thai Vegetable Farmers. Toxics 2023, 11, 707. https://doi.org/10.3390/toxics11080707

AMA Style

Bunsri S, Muenchamnan N, Naksen W, Ong-Artborirak P. The Hematological and Biochemical Effects from Pesticide Exposure on Thai Vegetable Farmers. Toxics. 2023; 11(8):707. https://doi.org/10.3390/toxics11080707

Chicago/Turabian Style

Bunsri, Siriphan, Nutnichawan Muenchamnan, Warangkana Naksen, and Parichat Ong-Artborirak. 2023. "The Hematological and Biochemical Effects from Pesticide Exposure on Thai Vegetable Farmers" Toxics 11, no. 8: 707. https://doi.org/10.3390/toxics11080707

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop