Associations between Pesticide Metabolites and Decreased Estimated Glomerular Filtration Rate Among Solar Greenhouse Workers: A Specialized Farmer Group

Tenglong Yan Xin Song Xiaodong Liu Wu Liu Yonglan Chen Xiaomei Zhang Xiangjuan Meng Binshuo Hu Zhenxia Kou Tian Chen Xiaojun Zhu

Tenglong Yan, Xin Song, Xiaodong Liu, Wu Liu, Yonglan Chen, Xiaomei Zhang, Xiangjuan Meng, Binshuo Hu, Zhenxia Kou, Tian Chen, Xiaojun Zhu. Associations between Pesticide Metabolites and Decreased Estimated Glomerular Filtration Rate Among Solar Greenhouse Workers: A Specialized Farmer Group[J]. Biomedical and Environmental Sciences, 2025, 38(2): 265-269. doi: 10.3967/bes2025.013
Citation: Tenglong Yan, Xin Song, Xiaodong Liu, Wu Liu, Yonglan Chen, Xiaomei Zhang, Xiangjuan Meng, Binshuo Hu, Zhenxia Kou, Tian Chen, Xiaojun Zhu. Associations between Pesticide Metabolites and Decreased Estimated Glomerular Filtration Rate Among Solar Greenhouse Workers: A Specialized Farmer Group[J]. Biomedical and Environmental Sciences, 2025, 38(2): 265-269. doi: 10.3967/bes2025.013

doi: 10.3967/bes2025.013

Associations between Pesticide Metabolites and Decreased Estimated Glomerular Filtration Rate Among Solar Greenhouse Workers: A Specialized Farmer Group

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    Author Bio:

    Tenglong Yan, PhD Candidate, majoring in labor hygiene and environmental hygiene, E-mail: yantlyan@163.com

    Corresponding author: Tenglong Yan, PhD Candidate, E-mail: yantlyan@163.comXiaojun Zhu, PhD, E-mail: zhuxj_bj@126.com
  • Study concept and design, Data collection, Statistical analysis, Drafting the manuscript: Tenglong Yan; Data collection, Statistical analysis: Xin Song; Data collection, Revision of the manuscript for language and intellectual content: Wu Liu; Data collection: Yonglan Chen; Laboratory analysis: Xiaodong Liu; Laboratory analysis: Xiaomei Zhang; Laboratory analysis: Binshuo Hu; Laboratory analysis: Xiangjuan Meng; Revision of the manuscript for language and intellectual content: Tian Chen; Revision of the manuscript for language and intellectual content: Xiaojun Zhu; Revision of the manuscript for language and intellectual content: Zhenxia Kou. All authors participated in drafting and finally approved the manuscript.
  • The authors have no conflicts of interest to declare.
  • The protocol was approved by the Medical Ethics Committee of the Beijing Institute of Occupational Disease Prevention and Control (no. 2022011, June, 2022).
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  • 收稿日期:  2024-09-09
  • 录用日期:  2024-12-02
  • 网络出版日期:  2025-03-06
  • 刊出日期:  2025-02-20

Associations between Pesticide Metabolites and Decreased Estimated Glomerular Filtration Rate Among Solar Greenhouse Workers: A Specialized Farmer Group

doi: 10.3967/bes2025.013
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1) Authors’ Contributions: 2) Competing Interests: 3) Ethics:

English Abstract

Tenglong Yan, Xin Song, Xiaodong Liu, Wu Liu, Yonglan Chen, Xiaomei Zhang, Xiangjuan Meng, Binshuo Hu, Zhenxia Kou, Tian Chen, Xiaojun Zhu. Associations between Pesticide Metabolites and Decreased Estimated Glomerular Filtration Rate Among Solar Greenhouse Workers: A Specialized Farmer Group[J]. Biomedical and Environmental Sciences, 2025, 38(2): 265-269. doi: 10.3967/bes2025.013
Citation: Tenglong Yan, Xin Song, Xiaodong Liu, Wu Liu, Yonglan Chen, Xiaomei Zhang, Xiangjuan Meng, Binshuo Hu, Zhenxia Kou, Tian Chen, Xiaojun Zhu. Associations between Pesticide Metabolites and Decreased Estimated Glomerular Filtration Rate Among Solar Greenhouse Workers: A Specialized Farmer Group[J]. Biomedical and Environmental Sciences, 2025, 38(2): 265-269. doi: 10.3967/bes2025.013
  • This study investigates the relationship between pesticide metabolites and kidney function in solar greenhouse workers, a group with potentially higher chronic kidney disease (CKD) risk compared to general farmers. A total of 279 workers participated, with pesticide metabolites (AMPA, DMP, DEP, DMDTP, GLY, and DEDTP) measured in their urine. Estimated glomerular filtration rate (eGFR) was calculated using serum creatinine, age, gender, and BMI. Multiple linear regression analyses showed an inverse association between eGFR and metabolites AMPA, DMP, DMDTP, and overall pesticide metabolites. Notably, pesticide metabolite concentrations were higher in females, and gender-stratified analysis revealed stronger associations in women. The findings suggest that pesticide exposure is linked to a slight decline in kidney function among solar greenhouse workers, highlighting ongoing concerns about pesticide risks in this occupation.

    CKD and renal impairment are substantial global public health problems. CKD is responsible for an estimated 1.2 million deaths annually worldwide[1]. These solar greenhouse workers operated in enclosed, high-temperature environments, resulting in long-term exposure to potential hazards. Previous studies have demonstrated a higher risk of CKD in this group compared to general farmers, with a 20% lower estimated glomerular filtration rate (eGFR; 19.74 mL/min per 1.73 m2) compared to that of field workers[2]. However, the potential risk factors contributing to this increased risk remain unclear.

    Solar greenhouses are a type of agricultural facility widely used around the world. There are numerous hazards present in the solar greenhouse environment, but exposure to pesticides is one of the most typical hazards. To meet the needs of crop growth and pest control, organophosphorus pesticides, the most commonly used pesticides, are extensively utilized in greenhouse environments. Moreover, the enclosed nature of greenhouses hinders pesticide dispersion, which may lead to higher levels of pesticide exposure in this population. Some studies have reported that pesticide metabolites in urine are associated with subclinical kidney function decline in adults and children. Some researchers have asserted that certain pesticides exhibit significant nephrotoxicity, which may be an important reason for the increased prevalence of unexplained CKD in farmers. This study aimed to evaluate the association between pesticide exposure and kidney function among solar greenhouse workers. Participants were selected from a high-quality solar greenhouse vegetable production base in Northwest China. Measurements of six urinary pesticide metabolites were conducted to assess internal pesticide exposure levels. The eGFR was used as an indicator of renal function, and further analysis was performed to explore the relationship between pesticide metabolites and renal impairment.

    A cross-sectional study was conducted in Jingyuan County, Gansu Province, China, from May 3 to May 26, 2023. We adopted the cluster sampling method. Two hundred and seventy-nine solar greenhouse workers without hereditary kidney disease and diabetes were included. The inclusion criteria were as follows: (1) residing in the local area for ≥ 1 year; (2) aged 30–55 years; and (3) engaged in solar greenhouse work for ≥ 1 year.

    General demographic information and occupational details of the participants were collected through a structured questionnaire, which was administered by trained investigators through one-on-one interviews. In addition, 5 mL fasting peripheral blood and 15 mL morning urine samples were collected. A 0.5-mL aliquot of urine was used to determine the concentrations of six pesticide metabolites, namely, aminomethylphosphonic acid (AMPA), dimethylphosphate (DMP), diethylphosphate (DEP), dimethyldithiophosphate (DMDTP), glyphosate (GLY), and diethyl dithiophosphate (DEDTP). Serum creatinine levels were measured and used to calculate the eGFR[3].

    Differences in categorical parameters were evaluated using the chi-square test or Fisher’s exact probability method. Student’s t-test and Wilcoxon rank-sum tests were used to compare the means and medians of continuous parameters between groups. Pearson’s correlation analysis was performed to evaluate the correlation among pesticide metabolites. Linear models were used to investigate the correlations between eGFR and single pesticide metabolite in all solar greenhouse workers and in both sex subgroups. Statistical significance was set at α < 0.05 for two-tailed P values unless otherwise specified. To account for multiple comparisons, we applied a correction to the P-values. The adjusted threshold was set at 0.05 divided by 6 (number of comparisons), giving an adjusted threshold of 0.008.

    Table 1 presents the characteristics of 279 solar greenhouse workers categorized by sex. The mean age of all participants was 47.55 ± 5.08 years, with no significant difference between males (47.69 ± 4.59 years) and females (47.43 ± 5.47 years; P = 0.682). A statistically significant difference in educational level was found (P = 0.024), as a higher percentage of females (32.9%) than males (19.7%) had a primary school education. Smoking habits and alcohol consumption also differed significantly between sexes. A higher prevalence of smoking and alcohol consumption was found in male participants (smoking: 60.6%; alcohol: 30.7%) than in female participants (smoking: 0.7%, alcohol: 3.9%). The average working experience was (15.08 ± 9.17 years), with no significant difference between males (15.92 ± 8.75 years) and females (14.37 ± 9.48 years; P = 0.159). The average number of solar greenhouses was 1.66 ± 0.78, with male participants owning more (2.06 ± 0.78) than the female participants (1.36 ± 0.78), albeit without a significant difference (P = 0.208). Urine creatinine levels were significantly higher in males (1.86 ± 0.84 mg/g) than in females (1.50 ± 0.68 mg/g; P < 0.001). However, no significant sex differences were observed for eGFR (P = 0.912). The median concentrations of AMPA, DMP, DEP, DMDTP, and GLY were 2.57 μg/g, 1.39 μg/g, 0.23 μg/g, 0.14 μg/g, and 0.94 μg/g, respectively. The total median concentration for the above five metabolites was 196.46 nmol/g. Further sex-specific comparisons showed that median concentrations of DMP, DEP, and GLY metabolites were higher in females than in males (all P < 0.05; Table 1). We found a high detection rate of four pesticide metabolites in the urine of solar greenhouse workers. AMPA, DMP, DEP, and GLY were detected in the urine samples of almost all the workers. Some other studies have also examined these pesticide metabolites in farmers, but have reported lower concentrations or exposures rates. Specifically, Connolly, Campbell, and their colleagues found that the median concentration of AMPA in farmers was below than 1 μg/g[4,5], which is much lower than our finding among solar greenhouse workers (3.51 μg/g), indicating that the solar greenhouse workers had at high level of organophosphorus pesticide exposure.

    Table 1.  Characteristics of the solar greenhouse workers by sex

    Variables All (n = 279) Male (n = 127) Female (n = 152)
    Age (years)* 47.55 ± 5.08 47.69 ± 4.59 47.43 ± 5.47
    ≤ 45 87 (31.2) 40 (46.0) 47 (54.0)
    > 45 192 (68.8) 87 (45.3) 105 (54.7)
    BMI (kg/m2)* 24.56 ± 3.98 24.16 ± 3.82 24.89 ± 4.09
    < 24 126 (45.2) 59 (46.5) 67 (44.1)
    ≥ 24 153 (54.8) 68 (53.5) 85 (55.9)
    Education
    Primary school 75 (26.9) 25 (19.7) 50 (32.9)
    Middle school 170 (60.9) 82 (64.6) 88 (57.9)
    High school and above 34 (12.2) 20 (15.7) 14 (9.2)
    Smoking habits
    Yes 79 (28.3) 77 (60.6) 2 (1.3)
    No 200 (71.7) 50 (39.4) 150 (98.7)
    Alcohol
    Yes 45 (16.1) 39 (30.7) 6 (3.9)
    No 234 (83.9) 88 (69.3) 146 (96.1)
    Work experience (years)* 15.08 ± 9.17 15.92 ± 8.75 14.37 ± 9.48
    ≤ 10 103 (36.9) 41 (32.3) 62 (40.8)
    > 10 176 (63.1) 86 (67.7) 90 (59.2)
    Number of greenhouses 1.95 ± 1.37 2.06 ± 1.36 1.86 ± 1.38
    ≤ 1 100 (35.8) 41 (32.3) 59 (38.8)
    > 1 179 (64.2) 86 (67.7) 93 (61.2)
    Urine creatinine concentration (mg/g)* 1.66 ± 0.78 1.86 ± 0.84 1.50 ± 0.68
    eGFR (mL/min per 1.73 m2)* 111.50 ± 16.87 111.40 ± 17.01 111.62 ± 16.74
    AMPA 2.57 (1.82, 3.25) 2.46 (1.76, 3.18) 2.58 (1.83, 3.33)
    DMP 1.39 (0.76, 2.04) 1.15 (0.66, 1.98) 1.48 (0.97, 2.25)*
    DEP 0.23 (0.14, 0.42) 0.18 (0.12, 0.34) 0.27 (0.16, 0.48)*
    DMDTP 0.14 (0.06, 0.26) 0.14 (0.05, 0.25) 0.14 (0.07, 0.27)
    GLY 0.94 (0.63, 1.67) 0.80 (0.54, 1.56) 1.09 (0.74, 1.89)*
    Total* 196.46 (143.09, 249.74) 191.40 (139.14, 244.00) 201.01 (144.88, 255.05)
      Note. *The variables are presented as ± SD, or n (%). , mean. SD, standard deviation. BMI, body mass index. eGFR, estimated glomerular filtration rate. AMPA, aminomethylphosphonic acid. DMP, dimethylphosphate. DEP, diethylphosphate. DMDTP, dimethyldithiophosphate. GLY, glyphosate.

    The estimated associations between pesticide metabolite levels and eGFR are shown in Table 2, with the multiple linear regression analysis adjusted for variables including sex, age category, BMI, smoking and drinking habits, work experience, and the number of greenhouses. The results showed a significant negative correlation between AMPA metabolite levels and eGFR (β = −0.299, 95% confidence interval [CI]: −0.349 to −0.155, P < 0.001), indicating that evaluated higher concentrations of AMPA were associated with a reduced eGFR. Similarly, significant negative correlations were observed between DMP and DMDTP metabolite levels and eGFR (β = −0.294, 95% CI: −0.344 to −0.150, P < 0.001; β = −0.160, 95% CI: −0.324 to −0.015, P = 0.007, respectively). Conversely, no significant associations were found between DEP or GLY metabolites and eGFR. A significant negative correlation was observed between the total concentration of pesticide metabolites and eGFR (β = −0.008, 95% CI: −0.012 to 0.005, P = 0.005). More details about the association between metabolites and eGFR are shown in Supplementary Tables S1S6. Some previous studies have shown that exposure to organophosphate pesticides, such as DDT and chlorpyrifos, is negatively correlated with CKD and eGFR[6]. For example, DAP metabolites are associated with increased subclinical kidney injury in children with CKD[7]. Our study provided preliminary evidence for an association between organophosphate pesticide levels and reduced eGFR, with the level of the metabolites AMPA, DMP, and DMDTP associated with the decreased eGFR.

    Table 2.  Estimated association of organophosphorus pesticide metabolites and eGFR

    Variables Β** 95% CI P-value
    AMPA −0.299 −0.349, −0.155 < 0.001*
    DMP −0.294 −0.344, −0.150 < 0.001*
    DEP 0.043 −0.040, 0.084 0.483
    DMDTP −0.160 −0.324, −0.015 0.007*
    GLY −0.040 −0.081, −0.001 0.041
    Total** −0.008 −0.012, −0.005 0.005*
      Note. *P < 0.05. β: regression coefficient. CI: confidence interval. AMPA: dminomethylphosphonic acid. DMP: dimethylphosphate. DEP: diethylphosphate. DMDTP: dimethyldithiophosphate. GLY: glyphosate. All pesticide metabolites were log-transformed before being entering into the model. “Total” represents the total mass concentration of the five metabolites. Variables of sex, age category, BMI, smoking and drinking habits, work experience, and number of greenhouses were adjusted in the multiple linear regression. **β corresponds to a 1 SD change in log-transformed metabolite levels.

    We further conducted sex-stratified analysis to account for potential variations (Table 3). There were no interactions between sex and pesticide metabolite levels. Among males (β = −0.211, 95% CI: −0.353 to −0.069, P = 0.004) and females (β = −0.282, 95% CI: −0.420 to −0.145, P < 0.001), significant negative correlations were found between AMPA metabolite levels and eGFR. No significant associations were found between DMP, DEP, DMDTP, or GLY metabolite levels and eGFR in either sex subgroup. A significant negative correlation was found between the total concentration of pesticide metabolites and eGFR in females (β = −0.004, 95% CI: −0.006 to −0.002, P = 0.006), but not males (β = −0.003, 95% CI: −0.005 to −0.001, P = 0.043). All associations were adjusted for age category, BMI, smoking and drinking habits, work experience, and the number of greenhouses in linear regression analyses. Subgroup analysis indicated that the results were robust (Supplementary Tables S7S12). In previous studies, we reported a higher prevalence of CKD in female workers than in male workers[2]. However, in this study, slightly significant differences in eGFR were observed between the two groups. Hormonal factors unique to females, such as estrogen levels, have been implicated in altering the metabolism and elimination of xenobiotics, including pesticides[8].

    Table 3.  Estimated association of organophosphorus pesticide metabolites with egfr by sex subgroup

    Variables Male (n = 127) Female (n = 152)
    β** 95% CI P-value β** 95% CI P-value
    AMPA −0.211 −0.353, −0.069 0.004* −0.282 −0.420, −0.145 < 0.001*
    DMP −0.012 −0.095, 0.072 0.779 0.064 −0.029, 0.158 0.176
    DEP 0.320 −0.042, 0.682 0.082 −0.004 −0.236, 0.227 0.969
    DMDTP 0.524 −0.269, 0.816 0.371 −0.260 −0.326, 0.194 0.009
    GLY 0.048 −0.027, 0.123 0.203 0.029 −0.021, 0.078 0.253
    Total −0.003 −0.005, −0.001 0.043 −0.004 −0.006, −0.002 0.006*
      Note. *P < 0.05. β, regression coefficient. CI, confidence interval. AMPA, dminomethylphosphonic acid. DMP, dimethylphosphate. DEP, diethylphosphate. DMDTP: dimethyldithiophosphate. GLY, glyphosate. All pesticide metabolites were log-transformed before entering the model. “Total” represents the total mass concentration of these five metabolites. Variables of age category, BMI, smoking and drinking habits, work experience, and number of greenhouses were adjusted in the multiple linear regression. **β corresponds to a 1 SD change in log-transformed metabolite levels.

    This study presents the first report of internal pesticide metabolite exposure among workers in solar greenhouses. However, several limitations should be recognized. First, as a cross-sectional study, our findings only establish an association between pesticide levels and eGFR, and they cannot determine causal relationships. Although the likelihood is low, the possibility of a reverse association between pesticide metabolite levels and changes in eGFR may exist. This is because renal dysfunction can affect the excretion of urinary solutes. Second, our assessment of renal function relied solely on the eGFR due to the nature of our study population, which consisted of healthy individuals with a low prevalence of proteinuria and CKD. This limited our ability to obtain more comprehensive indicators. However, our study still provided evidence for the relationship between pesticide exposure and kidney function impairment. Third, the outdoor agricultural workers from the same location were not selected as controls, which limited our ability to conclusively determine whether solar greenhouse workers were exposed to higher levels of pesticides. Fourth, the adjusted confounding factors may not have accounted for all potential confounders, such as heat exposure; hereditary kidney disease; and dietary intake, particularly the consumption of meat and sugary beverages[9,10]. Despite these limitations, our findings still provided evidence for the relationship between pesticide exposure and reduced kidney function.

    Our findings indicated that solar greenhouse workers are exposed to a certain level of pesticides, with female workers showing higher levels of internal exposure than male workers. The level of exposure observed in the current study was associated with a slight decline in kidney function. Our findings contribute additional evidence to the study of the potential mechanisms involved in kidney function decline. Moreover, the exposure of farmers and solar greenhouse workers to pesticides must be limited, and there is a need for stricter exposure limits for pesticides.

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