Pesticide use behavior, cognitive impairment and the model of safety standard of pesticide use among farmworkers in Indonesia

Ethical consideration

This study was approved by the Ethical Committee of Medical Research at The University of Jember on 4 November 2022, with No. Registration: 1769/UN25.8/KEPK/DL/2022.

Study design and sampling

This study used a cross-sectional design, in which the authors were eager to understand and assess the association of outcome- and predictor-variables at the same time. In this study, cluster random sampling was used. The study area was divided into five locations, namely west, east, north, south, and center area, in which the total sample included 500 farmworkers distributed in each location. Table 1 recorded the distribution of samples. In this study, 10 out of 28 sub-districts were selected as study areas, namely: Ambulu, bangsalsari, kalisat, pakusari, Puger, semboro, sukowono, sumberbaru, tanggul, Umbulsari. All participants were proportionately distributed in each sub-district.

Variables

The outcome- and predictor-variables include cognitive impairment and pesticide use behavior, respectively. Cognitive impairment was measured using the Montreal Cognitive Assessment Indonesian version (MoCa-Ina) that was previously validated.¹² The MoCa has been widely used to assess cognitive impairment among populations.^13–15 The MoCa-Ina assesses diverse cognitive domains, namely: attention and concentration, executive functions, language, memory, conceptual thinking, calculations, visuoconstructional skills and orientation. The maximum score of MoCA-Ina is 30 points, and the main categories are divided into two groups, namely normal (score: ≥26 points) and cognitive impairment (score: <26). In addition, one point is given to participants with formal education that lasted approximately 12 years with a total score of less than 30 points.

The variable of pesticide use behavior referred to the Integrated Pest Management Principal by Directorate General of Horticulture Production, Indonesian Ministry of Agriculture including quality, target, type, time, doses, utilization of pesticide (6T).¹⁶ There were 18 questions in which each question has one point. This variable is categorized into three group: a) favorable (13-18 points), b) moderate (7-12 points), and c) worse (0-6 points).

Data on farmworker characteristics were also collected, including sex, age, working duration (years), type of commodity, pesticide exposure (hours), pesticide dissemination, time of pesticide dissemination, pesticide storage. All participants provided written informed consent and agreed to participate in this study.

Data collection

Data on characteristics and pesticide use behavior among farmworkers were collected using a quantitative questionnaire whereby a trained surveyor read/asked listed-questions in the questionnaire to help the participant, in which the answers of the participant were noted in the questionnaire by the surveyor. The role of the trained surveyor was to assist the respondent by describing the question and filling the respondent’s answer in the questionnaire. The questionnaire was generated based on literature study, a review of the relevant literature, as reported by Yaddanapudi and Yaddanapudi.¹⁷ The questionnaire consisted of characteristics on farmworkers and pesticide use behavior that referred to the Principal of Integrated Pest Management of Directorate General of Horticulture Production - Indonesian Ministry of Agriculture Moekasan.¹⁶ The questionnaire can be found as Extended data.⁴⁷

The validity and reliability of the questionnaire were tested in a pilot study using 20 participants. Validity and reliability were measured using Product Moment Pearson and Alpha Cronbach, respectively, as performed in previous studies (Dewi and Sudaryanto¹⁸ and Binus¹⁹). Based on Pearson’s r test, the r score of the questionnaire ranged from 0.413 to 0.831 (p<0.05), Sugiyono²⁰ noted that questionnaires with r score > 0.3 and p value <0.05 are valid. In addition, the Cronbach’s Alpha score of the questionnaire is 0.710, Putri et al.,²¹ reported that the questionnaire is reliable if the Alpha Cronbach score >0.6. The validity and reliability tests were assessed in IBM SPSS Statistics (RRID:SCR_016479) version 25.

Following the administration of this questionnaire, participants were administered the MoCa-Ina instrument¹² to collect the data regarding cognitive impairment. The data were collected after ethical clearance was established (data collection was from 5 November to 1 December 2022).

Analysis

In order to achieve the objectives, several analyses have been conducted in this study, namely:

Pesticide residue in agricultural products

Table 2⁴⁷ presents the traces of pesticide residue in 15 samples of agricultural products in a local market in Jember. Based on Table 2, 10 out of 15 samples confirmed positive traces of pesticide residue of chlorpyriphos class of organochlorin.

Pesticide use behavior and cognitive impairment

Table 3 reported the cognitive impairment score among farmworkers. Based on Table 3, 70% of participants (350 farmworkers) showed impaired cognitive ability with a MoCa-Ina score less than 26 points. On the other hand, 30% of participants showed a normal score.

Table 4 presents the pesticide use behavior based on Integrated Pest Management Principal among farmworkers. Based on Table 4, the quality, dose, type and utilization of pesticide, targeted pest of pesticide, and time of pesticide dissemination is favorable among farmworkers (approximately 82% to 99%). However, 29% of participants did not use PPE during pesticide dissemination. Further explanatory analysis showed that farmworkers did not always follow the IPM criteria, they did not use appropriate pesticides for the specific type of plant (16.4%), they used unstandardized doses not following the label instructions (17.4%), and they used excessive doses of pesticide (18.2%).

Table 5 presents the tiers of pesticide use behavior among farmworkers. Based on Table 5, 92.4% of participants (462 farmworkers) showed favorable pesticide use behavior. Meanwhile, 7.6% of participants showed moderate use behavior.

Table 6 noted the association between characteristics and pesticide use behavior of farmworkers in terms of cognitive impairment. Based on Table 6, participants >50 years old (71.4%), male (70.6%), working duration >10 years (71.7%), planting tobacco (89.9%), >2 hour of pesticide exposure (70.9%), performing pesticide dissemination 3-4 time per month (72.6%), time of pesticide dissemination of 15.00-17.00 (81.6%), and pesticide storage indoors (80.2%) were highly distributed in the cognitive impairment category. In the variable of pesticide use behavior, moderate level behavior (65.7%) was associated with cognitive impairment.

Bivariate analysis by chi-squared test presents the significance of the type of commodity and pesticide storage in terms of cognitive impairment among farmworkers (p<0.05). According to logistic regression analysis, other commodities (tobacco), pesticide exposure >2 hour, pesticide dissemination at night and pesticide storage outdoors were associated with cognitive impairment (p<0.05).

Model of safety standard for pesticide use among farmworkers

The model of safety standard of pesticide use is shown in Figure 2. As visualized in Figure 2, four factors are suggested to influence pesticide use among farmworkers, namely: the behavior of farmworkers (knowledge, attitude, and personal hygiene), implementation of integrated pest management principal (quality, doses, type, targeted pest, time of disseminating, utilization of pesticide), PPE utilization (head and face protection, goggles, mask, body protection, safety boots, and gloves), and pesticide waste control (waste control in water, land, and air).

Figure 2. The model of safety standard of pesticide use among farmworkers.

PPE, personal protection equipment.

Characteristics and pesticide use behavior associated with cognitive impairment

The unsafe pesticide use behavior among farmworkers such as excessive dose of pesticide use not using protection during pesticide dissemination and pesticide use not following its label leads to adverse effects on health in both farmworkers and consumer populations. The chemical substances of pesticides may directly impact farmworkers, causing either acute or chronic diseases. Fucic et al.,²⁷ noted that various pesticide types elevate the risk of diabetes, cancer, and neurodegeneration, including cognitive impairment. Health issues among consumers or populations is associated with the consumption of agricultural products containing pesticide residue. Furthermore, pesticide waste also pollutes the environment.²⁸

Table 2 reports the availability of pesticide residue in agricultural products. According to Table 2, 66.67% (10 out of 15 samples) contain the pesticide of chlorpyriphos, as found by using Pesticide Detection Card analysis. The presence of the chemical substances of pesticides in agricultural products is well documented.²⁹ Ardiwinata³⁰ and Hendriadi³¹ reported that pesticide residue of insecticide (organochlorine, organophosphate, carbamate, pyrethroid) and fungicide (dimethomorph, fenobucarb, propineb, benomyl) exists in agricultural products.^30,31 The presence of organochlorine substances in the environment is high due to its persistence. In addition, based on observations of farmworker behavior in this study, it was found that cover blanket systems in pesticide use have been implemented, which lead to increases in the amount of pesticide residue among agricultural products.

As mentioned in Table 3, cognitive impairment, as assessed using the MoCa-Ina, among farmworkers is highly distributed (70% participants) in the impaired category (total score <26 points). Pesticide exposure and mild cognitive impairment is associated with neurotoxic dysfunction. High exposure to pesticides stimulates the inhibitor of cholinesterase enzyme. The impairment of cholinesterase enzyme leads to failure in hydrolysis of acetylcholine that has a critical role in passing stimulation from nerves to muscle cells and gland organs, consequently pesticide exposure can cause cognitive impairment, involuntary tremors in muscles, convulsion, and death.⁹ This finding is consistent with studies by Marucci et al.,³² and Mutia et al.,³³ which found that the inhibition of brain acetylcholine catabolic enzymes, acetylcholinesterase, and butyrylcholinesterase elevate brain acetylcholine levels that cause cognitive dysfunction such as Alzheimer’s disease. Furthermore, Aloizou et al.,³⁴ also reported that low dose exposure of pesticides and other chemical substances trigger hormetic neurobehavioral effects, and this effect is exacerbated by vitamin deficiency among farmworkers.

Tables 4 and 5 show pesticide use behavior based on the integrated pest management principals among farmworkers. Based on Table 3, the quality-, dose-, type- and utilization- of pesticides, targeted pest of pesticide, and time of pesticide dissemination is favorable among farmworkers, in which 92.4% of participant were in the favorable category and only 7.6% of participants were in the moderate category. In accordance with the behavior of pesticide use among farmworkers, Damalas and Koutroubas³⁵ reported that pesticide use behavior is critical for accurate risk assessment, whereas perception, attitude and self-efficacy drive safety behavior among farmworkers.

This study found that a high number of participants have good or favorable pesticide use behavior, in which Endalew et al.,³⁶ noted that 61.3% showed good practice of pesticide use in Ethiopia. Nevertheless, there were still high numbers of farmworkers that did not use PPE and use unfit pesticides for the specific type of plant and unstandardized doses that lead to increased risks of negative health effects among farmworkers. This finding is in agreement with Gesesew et al.,³⁷ whereas only 42% of farmers in Rural Irrigation Villages in Southwest Ethiopia rarely used PPE. Struelens et al.,³⁸ also mentioned that high percentages of farmers in Bolivia were incorrectly following pesticide dose recommendation. PPE use during pesticide dissemination is recommended among farmworkers for protection as the chemical substances of pesticides can enter the human body through inhalation, as well as oral and skin routes. Chittrakul et al.,³⁹ found that inappropriate use of PPE may elevate urinary organophosphate metabolite levels.

Table 6 reports the association between characteristics and pesticide use behavior with cognitive impairment among farmworkers, being >50 years old (71.4%), with a working duration >10 years (71.7%), male (70.6%), planting tobacco (89.9%), with >2 hour of pesticide exposure (70.9%), performing pesticide dissemination 3-4 times per month (72.6%), with a time of pesticide dissemination between 15.00 and 17.00 (81.6%), and storing pesticides indoors (80.2%) were highly distributed in participants with cognitive impairment. In the variable of pesticide use behavior, 65.7% of those in the moderate category had cognitive impairment. Yet, the chi-squared test showed significant associations between the type of commodity and pesticide storage with cognitive impairment (p<0.05). Furthermore, logistic regression analysis showed that other commodity (tobacco) (AOR: 0.21 (CI: 0.09 – 0.46)), pesticide exposure duration >2 hours (AOR: 0.52 (CI:0.27 – 0.10)), time of pesticide dissemination between 16.00-22.00 (AOR: 5.77 (CI: 1.12 – 29.85)), and pesticide storage outdoors (AOR: 1.81 (CI:1.13 – 2.90)) were associated with cognitive impairment (p<0.05).

The findings of this study showed that pesticide storage outdoors had an AOR>1 toward cognitive impairment, which indicates that pesticide storage outdoors is a risk factor. Based on observations, farmworkers often stored pesticides close to the main house building, where the chemical substance still enters the house toward their ventilation. The AOR of pesticide exposure duration >2 hours was less than 1. Based on theoretical concept, farmworkers are susceptible to long-term exposure of pesticides, which leads to adverse health outcomes. However, there are several rational as to why the AOR pesticide exposure duration is less than 1, namely: a) information of pesticide exposure duration is based on recall from farmworkers that led to misinformation, b) the pesticide disseminating process is often conducted in the morning, which is the recommended time. Therefore, the authors hypothesize that low or no exposure dose may appear, c) the high level of favorable pesticide use among farmworkers reduces the risks of pesticides. This study found that the AOR of time of pesticide dissemination between 16.00-22.00 is >1. It indicates that farmworkers spraying pesticide over that time are at risk for cognitive impairment. Several rationales correspond to this issue, including unfavorable conditions (temperature and humidity) for pesticide spraying and farmworkers being unable to detect wind duration during that time. In addition, a noteworthy finding has been found in this study that the AOR of type of commodity (tobacco) is less than 1. The authors hypothesize that the utilization of pesticides among farmworkers of tobacco is less than other farmworkers, and has favorable pesticide use behavior. However, further study is necessary.

All populations are vulnerable to the adverse effects of pesticides, in which children, pregnant women and older adults are more susceptible. The cognitive impairment or decline among participants >50 years old, working duration >10 years, spraying pesticide 3-4 times per month and >2 hour of pesticide exposure may be due to chronic exposure of the chemical substances of pesticides. The low dose of chemical substance is absorbed by the body and leads to several responses, particularly inhibiting the cholinesterase enzyme.⁹ Ganie et al.,⁴⁰ reported that organophosphates, one of the pesticide types, is causing cholinergic crisis, intermediate syndrome, organophosphate-induced delayed neuropathy and chronic organophosphate-induced neuropsychiatric disorder. A study by Jallow et al.,⁴¹ found that pesticide application among farmworkers in Kuwait is also approximately two times a month.

This study found that most participants conducted an unstandardized protocol toward pesticide, including pesticide dissemination between 16.00 and 22.00 and indoor storage that stimulate cognitive impairment. The application of pesticides should be appropriate. Disseminating during the cooler part of the day (mild temperature: 27°C and high humidity: >45%) is recommended, in which the morning hours are the best conditions for spraying.⁴² In addition, EPA Australia⁴² also noted that pesticides should be stored in either an isolated, stand-alone building or a cupboard within multipurpose buildings. This study found a noteworthy finding. Although the AOR <1, the explanatory analysis showed that cognitive impairment was highly distributed among tobacco farmers. Therefore, further study is necessary to assess the pesticide use among tobacco farmers and its association with cognitive impairment.

The model of safety standard of pesticide use among farmworkers

As shown by Figure 2, the model of safety standard of pesticide use contains four main factors, namely: a) farmworker behavior, b) PPE utilization, c) application of integrated pest management, and d) waste control. Farmworker behavior plays an important role in pesticide use, in which appropriate behavior toward pesticide use may reduce the negative effects of pesticides. In order to improve farmworker behavior, increasing knowledge, attitude, and personal hygiene are necessary, in which continuing training from District Agriculture Office (DAO) among farmworkers is important. Ngah et al.,⁴³ found that positive attitude influences safe practices among workers, in which attitude was influenced by knowledge. Therefore, increasing knowledge should improve behavior among farmworkers. The habits of good personal hygiene should be implemented, including washing hands with soap, nail hygiene, and body cleanliness.⁴⁴

The factor of PPE utilization is reasonable to protect farmworkers. Farmworkers should be warned about the adverse health effects of pesticides and be urged to use PPE to protect their health, such as head or face protection, goggles, mask, body protection, safety boots, and gloves.⁴² The DAO is not only disseminating information about PPE but also provides the PPE tool kits. However, the authors suggest social approaches such as farmer-group donations to initiate the PPE procurement. EPA Australia⁴² also reported that PPE should be stored close to pesticides. In addition, minimum PPE should be printed on pesticide labels, in which pesticide manufacturers should consider the special conditions of farmers, including education level and age of farmer.⁴⁵

The implementation of Integrated Pest Management (IPM) principal is prominent. Using pesticides with appropriate quality, type and target is necessary, including specific pesticides for targeting particular pests or weeds. The proper time of dissemination and utilization of pesticides should be considered. The perception of risk of loss by the reduction of pesticide use remains an issue among farmworkers. Hence, unstandardized pesticide use and not implementing IPM principals are common, including excessive dose usage. The excessive dose of pesticide use was found in this study. This finding corroborates to Damalas,⁴⁶ who found that only 15.2% of the farmers in their study population were willing to reduce pesticide use. Therefore, implementing the IPM principal among farmworkers may reduce negative health effects due to exposure to the chemical substances of pesticides.

The waste control factor is important to reduce the concentration of chemical substances of pesticides in the environment. Waste control can be conducted by bioremediation, phytoremediation, and other methods. Physical waste such as the pesticide container or expired pesticide should be collected and stored in an isolated building, then transferred to an official waste management office to eliminate the waste. In addition, the awareness of farmworkers regarding waste control is necessary.

Limitations

There are several limitations needed to be mentioned in this study, including: 1) only 15 types of agricultural products were used for the assessment of pesticide residue, 2) the questionnaire used to measure IPM principal in this study was limited to only 18 questions, which does not provide detailed enough information, and 3) the model is not yet implemented in the population hence the author cannot monitor and evaluate the model. The authors suggest further research to assess the pesticide residue among the agriculture products distributed in each local market in Indonesia, thus it would be useful for future studies to identify and detect the pesticide residue within processed food products (agriculture and fish products). The development of an IPM principal questionnaire is necessary to provide more detailed information among farmworkers, particular in Indonesia. The model of safety standard of pesticide use should be assessed with further studies by using a mixed method approach (quantitative and qualitative study).