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Relationship between butyrylcholinesterase activity and hepatic transaminases: a cross-sectional study in agricultural workers from Peru

Journal of Occupational Medicine and Toxicology volume 20, Article number: 2 (2025) Cite this article

Abstract

Introduction

Chronic exposure to pesticides causes various adverse health effects, mainly at a neurological level. However, there is little evidence focused on liver tissue injury and transaminase activity as indicators of effect.

Methods

A cross-sectional study was designed based on medical-occupational records of workers from an agro-export company in Peru to associate the levels of butyrylcholinesterase (BChE) transaminases (ALT and AST). Occupational medical records were reviewed to obtain demographic and occupational information and laboratory values of BChE activity and transaminases.

Results

We evaluated 459 records, and 69.9% were men. The mean age was 34.9 ± 11.5 years. BChE, ALT, and AST levels were 6238.8 ± 709.1 U/l, 34.4 ± 12.5 U/l, and 22.4 ± 8.5 U/l, respectively. The proportion of inhibited BCHE and elevated transaminase levels was 15.3% and 21.6%, respectively. We found a significant association between BChE inhibition and elevation of transaminases (AST: PR = 0.798, 95%CI: 0.716–0.889; ALT: PR = 0.419, 95%CI: 0.239–0.736).

Conclusion

The potential usefulness of transaminases is shown as a biomarker of exposure and monitoring in occupational health programs for the agro-industry.

Background

In the last two decades, a sustained increase in global agricultural production has been observed, among other reasons, due to the increased use of agrochemicals such as pesticides and fertilizers [1]. This situation leads to increased risks of occupational exposure and harmful effects on human life and the environment. It is estimated that 1.8 billion people in the world are linked to agricultural activities, of which approximately 25 million each year suffer involuntary poisoning from pesticides [2]. The most significant burden occurs in low- and middle-income countries due to the lack of occupational health programs and training on the use of chemical products [3]. These occupational groups present variable levels of risk and modes of exposure depending on participation and involvement, as observed in workers in formulating factories [4], preparers of mixtures, loading, and application (spraying) [5], among others [6].

Pesticides are a large family of chemical substances, natural or synthetic, used to control pests that compromise crops. One-third of world production depends on these products, which is why they have become indispensable in current agricultural practices [7]. Four large families are mentioned among the most used: pyrethroids, organochlorines (OC), organophosphates (OP), and carbamates [8]. These last two are the most involved in non-fatal acute occupational poisoning events [9,10,11].

The effects of acute poisoning are well known for a primary central and peripheral neurotoxic action mediated by inhibiting the enzyme acetylcholinesterase [12, 13]. Hyperstimulation of cholinergic receptors manifests with DUMBBELS syndrome (diarrhea, urination, miosis/muscle weakness, bronchorrhea, bradycardia, emesis, lacrimation, salivation/sweating) [14]. On the other hand, chronic subclinical exposure continues to accumulate evidence of various effects, including carcinogenesis, reproductive, immunological, cardiovascular, and hepatotoxic effects, among others [14, 15].

Considering that much of the metabolism of pesticides takes place in the liver, this organ is vital in assessing the first toxic effects. Structural, biochemical, and mitochondrial alterations have been reported, although the underlying mechanisms are not yet well-defined [16]. It is deduced that phase I reactions in liver microsomes modify pesticide molecules into highly reactive products, which would affect cellular structures and processes [17]. Some studies have associated the development of hepatic steatosis in humans [18]. At the same time, animal models show induction of hepatomegaly, vacuolization, and necrosis by OP [19, 20] and more degenerative changes such as binucleated hepatocytes and focal coagulative necrosis with carbamates [21]. In this sense, chronic exposure to subclinical doses would begin with early hepatotoxicity that could be evident, mainly through biochemical changes [22].

Transaminases are liver enzymes widely used in the biomonitoring of various liver diseases [23]; however, they have yet to be well characterized in acute or chronic pesticide poisoning [16]. ALT (alanine aminotransferase) and AST (aspartate aminotransferase) are significantly increased when OP and carbamates are administered in rats [24]. However, the effect in humans appears to be less and more linked to ALT [25, 26]. Therefore, the assessment of transaminasemia would be critical in the early identification and monitoring of liver damage in occupational medicine [27]. Surveillance programs for pesticide exposure should consider biomarkers in addition to cholinesterase activity [28].

In Peru, at least four farmers go to health services every day for acute poisoning related to pesticides. The latest report from the epidemiology center shows 1,451 cases of acute poisoning for the year 2021, with more than 70% of these associated with the workplace due to exposure to carbamates and OP [29, 30]. On the other hand, no cases of chronic exposure or long-term effects have been identified. Therefore, the study aimed to evaluate the relationship between butyrylcholinesterase (BChE) activity and transaminasemia in Peruvian agricultural workers evaluated at an occupational clinic in Ica in 2019.

Methods

Design and participants

We designed a cross-sectional study based on secondary data analysis. We reviewed medical reports from occupational surveillance in companies exporting agricultural products in Ica, a city in south-central Peru located 300 km from the capital.

All records of workers with more than one year of continuous work in the company, including the variables of interest, mainly laboratory markers, were included. Records that refer to, or are presumed to have, diagnoses related to liver disorders, such as viral infections, drug use, or associated injuries, were excluded.

The medical records were reviewed individually to collect relevant and available information on job conditions; time spent working in the company, use of personal protection, activity, or type of work, as well as information about habits, lifestyle, tobacco consumption, alcohol, and body mass index (BMI), among others.

We performed the post hoc power estimation using the mean comparison module in two independent groups in the PASS v.20 program. Group sample sizes of 207 (warehouse, harvest, and fumigators) and 252 (administrative workers) achieve 100% power to detect a difference of 8.8 between the null hypothesis that both group means are 32.5 and the alternative hypothesis that the mean of group 2 is 23.7 with known group standard deviations of 14.7 and 5.0 and with a significance level (alpha) of 0.05000 using a two-sided two-sample t-test. The data for the post-estimation of power were extracted from the study published by Patil J et al. [31].

Techniques and instruments

The laboratory tests (AST, ALT, and BChE) were performed according to the health facility’s internal procedures and quality controls. A Greetmed model NV203 semi-automated biochemical analyzer and kits for AST and ALT (Elitech, United States) were used. The measurement methodology for all of them was UV-visible spectrophotometry in enzymatic kinetic reactions. In order to define hypertransaminasemia, both ALT and AST values were considered to exceed 41 and 38 U/L, respectively, as established by the manufacturer.

BChE activity in serum was analyzed similarly with a kit (Wiener Lab, Argentina). It was considered a surrogate indicator of exposure to OP pesticides and carbamates. The manufacturer established a reference cut-off value of 5500 U/L to identify whether a worker was probably exposed to pesticides or not.

Statistical analysis

The population characteristics were presented in frequencies, percentages, and central tendency measures with dispersion. The differences between transaminase groups were analyzed using the Mann-Whitney test after the identification of non-normality with the Shapiro-Wilk test. We used a robust Poisson regression analysis to estimate the strength of the relationship between BChE level and transaminasemia in a crude model, which was adjusted by selected consuphores with the construction of a DAG (directed acyclic graph). Differences were considered significant when p < 0.05. Data analysis was performed in Stata version 18 (StataCorp LCC, TX, USA).

Ethical aspects

The study was approved by the ethics committee of the Alas Peruanas University of Ica (Resolution N°3497-2018-DA-GT-D-FMHyCS-UAP, November 15th, 2018). Information from the records generated in the Occupational Clinic was used after requesting permission for data use. Informed consent was not required since the results were historical. The data were used strictly to comply with the objectives set out in the study, and the anonymity of the records was maintained, with no access to the personal data of each patient evaluated.

Results

We obtained 462 records and excluded three (one for hepatitis viral infection and two for hepatic steatosis), leaving 459 records of agricultural workers treated. 69.9% were men, and the average age was 34.9 ± 11.5 years. Regarding jobs, office administrators accounted for 54.9%, warehouse workers 15.3%, harvesters 22.2%, and fumigators 7.6%. The average working time in the study population was 4.3 ± 2.3 years, and 95.3% reported using personal protective equipment, mainly at the respiratory level (respirators with double gas filter) and dermal (waterproof overalls, hat, gloves, and boots), and mucous membranes (lenses). Regarding social habits, a high frequency (78.6%) of workers who report consuming alcoholic beverages is observed. It should be noted that the question asked was aimed at knowing whether they consumed alcoholic beverages occasionally (“social drinker”); no worker was considered an alcoholic. (Table 1)

Table 1 Descriptive characteristics of agricultural workers (n = 459)
Full size table

The bivariate analysis between the transaminase condition (normal and elevated) and each study variable shows that the participants’ sex is associated with high values of both transaminases. Likewise, BChE concentration above the reference value is significantly associated with the elevation of both transaminases, although more strongly in ALT. In the latter’s case, alcohol consumption is also an important variable that intervenes in the transaminase level. (Table 2)

Table 2 Variables independently associated with elevation of AST and ALT
Full size table

We used multivariate regression models for each elevated transaminase and BChE condition (normal or inhibited) adjusted for time and job position, use of PPE, alcohol consumption, tobacco consumption, BMI, age, and sex. A significant association of inhibited BchE with AST (PR = 0.798; 95%CI: 0.716–0.889; p < 0.001) and ALT (PR = 0.419; 95%CI: 0.239–0.736; p = 0.002) is observed. (Table 3)

Table 3 Association between butyrylcholinesterase activity and elevation of AST and ALT in multivariate analysis
Full size table

Discussion

The present investigation reported a significant association between transaminase activity and BChE in workers of an agricultural company. The results show that 15.3% of workers had BChE values lower than the reference value, and 21.6% had elevated levels of transaminases (ALT and AST).

The frequencies of agricultural workers with BChE depression are variable according to the context. Mambo et al., found 6% of cases with significantly inhibited BChE in pesticide handlers in Kenya [32]. On the contrary, it was found that up to 58.5% of workers had significantly reduced levels in Thailand [33]. Strelitz carried out a pre- and post-work assessment, finding up to 20% more inhibition of BChE in workers at the end of the day [34]. In this sense, it is necessary to consider the time and degree of exposure as determinants of the effect on markers of enzymatic activity.

The association analysis shows significance between them, with values lower than the cut-off point (BchE < 5500 IU) being a protective factor with less risk of presenting elevated liver enzymes. However, BChE must be carefully analyzed; previous reports indicate that this marker may behave variably depending on the type of pesticide. Patients with mild to moderate chlorpyrifos poisoning have severely inhibited BChE; conversely, it is not significantly inhibited in patients with dimethoate poisoning [35]. They recommend that various cut-off points and assessment levels should be evaluated when specifying exposure agents under this consideration.

Changes in liver enzymes have been widely evaluated in experimental studies with animals [36,37,38]; however, dysfunction assessed with transaminases in epidemiological studies of subclinical chronic exposure is still controversial [39]. The generalized posture is an increase in liver enzymes in exposed workers or at risk of exposure [31, 40, 41]. However, the opposite is also evidenced in studies with a decrease in these markers [42]. In our case, the focus was to demonstrate the association and risk of high levels of transaminasemia in cases of BChE inhibition. As a surrogate of pesticide exposure, it informs us of the suitability of the biomarker and information regarding worker evaluations.

Liver damage induced by pesticides such as paraquat involves altering the caspase pathway and, therefore, apoptotic processes in hepatocytes. It has also been shown that dichlorvos and monocrotophos increase the activity of some liver enzymes, such as ALT, and AST, causing liver injury in rats [43].

Our proposal provides relevant scientific information, considering that limited epidemiological reports have shown a significant association between biomarkers and transaminasemia as an indicator of liver damage, especially within the strict work environment.

Elevated levels of transaminases are characteristic of tissue-type liver damage. However, this may be transient since the enzymatic activity of transaminases can normalize when exposure to the agent that causes liver damage is restricted [44]. Furthermore, these levels may be a manifestation of acute liver injury [45], with alteration of many vital body functions. Therefore, exposure to pesticides is an activity that generates a greater probability that workers will debut with high levels of transaminases within the workplace.

Limitations

The main limitation is the impossibility of adequately defining the groups of exposed and unexposed workers based on contact with the toxic agent. Hence, a surrogate measure (BChE) is used as a proxy. Although it is reasonable to consider this assumption [34, 46], it cannot necessarily reproduce reality [35]. Furthermore, baseline BChE levels were not available for comparison. Likewise, the pesticide or pesticides used in the company’s processes have yet to be discovered since they are not described in the records. However, it is known that the use of these compounds in the local agricultural sector occurs under different mixtures [47].

Elevated transaminase activity can be due to multiple factors. We adjusted the analysis to avoid bias with the available variables logically related to the event. However, many relevant factors still need to be included, such as habits, medication consumption, physical activity, and other potential confounders regarding to AST/ALT and alcohol use. In the case of chronic hepatitis, these were ruled out at the time of the pre-occupational examination carried out by law on all workers before being hired by the company.

Conclusions

Our findings show that measuring the level of liver enzymes could contribute to the comprehensive evaluation of occupational cases exposed or at risk of pesticide exposure. These programs highlight the importance of permanent occupational surveillance since, based on them, preventive measures can be implemented, and occupational health can be improved.

It is recommended that BChE be measured as a biomarker of exposure. The observed significant association of BChE in the worker group establishes a potential profile for worker monitoring to predict and prevent health hazards from pesticides. In the absence of a homogeneous pattern of exposure, long-term studies on specific occupational groups would be necessary.

Data availability

No datasets were generated or analysed during the current study.

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Acknowledgements

We thank Universidad Continental for the payment of APC.

Funding

This research received no external funding.

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Authors and Affiliations

  1. Escuela de Tecnología Médica, Universidad Alas Peruanas, Lima, 150072, Peru

    Emily Ortiz-Delgado

  2. Escuela de Medicina, Facultad de Ciencias de la Salud, Universidad Peruana de Ciencias Aplicadas, Lima, 15067, Peru

    Guido Bendezu-Quispe

  3. Carrera de Medicina, Universidad Científica del Sur, 15058, Lima, Peru

    Fernando Soncco-Llulluy

  4. Facultad de Tecnología Médica, Universidad Nacional Federico Villarreal, 15003, Lima, Peru

    Jair Li

  5. Carrera de Medicina, Universidad Continental, Huancayo, 12000, Peru

    Jaime Rosales-Rimache

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Contributions

JRR and EOD. designed and conducted the study, collected and analyzed data, and wrote the manuscript; GBQ, FSL and JL. collected the data; GBQ, FSL, JL, and JRR. analyzed data and gave technical support; JRR. gave conceptual advice. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jaime Rosales-Rimache.

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Ethics approval and consent to participate

The study was approved by the ethics committee of the Alas Peruanas University of Ica (Resolution N°3497-2018-DA-GT-D-FMHyCS-UAP, November 15th, 2018). The use of informed consent was not required, since the results were historical.

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Ortiz-Delgado, E., Bendezu-Quispe, G., Soncco-Llulluy, F. et al. Relationship between butyrylcholinesterase activity and hepatic transaminases: a cross-sectional study in agricultural workers from Peru. J Occup Med Toxicol 20, 2 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12995-025-00450-z

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Journal of Occupational Medicine and Toxicology

ISSN: 1745-6673