1. Introduction
Pesticides are widely used in agriculture with a goal of enhancing productivity, which, in turn, can improve nutrition for the 795 million people experiencing food insecurity worldwide [
1]. Nonetheless, the extensive use of pesticides globally has also triggered growing concerns regarding environmental impacts and adverse health effects [
2,
3,
4]. Several organochlorine pesticides were associated with metabolic syndrome [
5]. Approximately 105 pesticides have been identified as endocrine disruptors affecting the natural hormone balance in the human body [
6]. Accumulating evidence suggests that endocrine disrupting chemicals can contribute to the development of diverse chronic diseases, including metabolic disorders such as diabetes [
5]. Thailand ranks fourth in annual pesticide consumption worldwide [
7] and in 2017, Thailand imported 198,317 tons of pesticides, including 148,979 tons of herbicides, 21,601 tons of insecticides, and 19,923 tons of fungicides [
8]. Importation and domestic production continue to increase, despite efforts by the Thai government to restrict the import of some pesticides, and proposals for new agrochemical regulations.
Since the 1990s the use of organic farming has been gradually increasing in Thailand [
9]. Driven by factors related to government initiatives to encourage sustainable agriculture in line with King Rama the Ninth’s self-sufficiency policy, as well as market demands, the use of organic farming practices is growing [
10]. At present, Thailand is ranked 60th in the world and the eighth in Asia in terms of organic agricultural area (45,587 hectares), which, in 2015, represented only 0.2% of the total agricultural area in Thailand [
11]. Rice was the major crop grown organically, occupying 60% of the organic land area, followed by other cash crops such as sugarcane, peanuts, and corn (20%), and diverse kinds of vegetables and fruits (4%) [
10].
As part of a longitudinal study of the non-communicable disease impacts of occupational pesticide exposures, we examined the baseline cross-sectional data on the prevalence of adverse biomarkers that are risk factors for the development of metabolic diseases such as diabetes, stroke and cardiovascular disease. We focused this analysis on the comparison of conventional farmers who currently use pesticides with organic farmers who do not currently use pesticides in order to investigate the role of current pesticide use plays in the risk of developing adverse metabolic biomarkers.
4. Discussion
High pesticide residues have been found in fruits and vegetables in Thai food markets and are a current public health concern [
4,
17,
18]. As a result, many Thai people are increasingly choosing organic food. The Thai Pesticide Alert Network (Thai-PAN) tested 296 samples of fruits and vegetables from five areas of Thailand in 2016 and found that 51.4% of the fruits and vegetables granted the “Q (quality) mark” by the Thai National Bureau of Agricultural Commodity and Food Standards were contaminated with pesticide residues above the maximum residue limit (MRL) [
19].
Most of the organic farmers in this study (86.9%) had previously been pesticide-using farmers before recognizing the toxicity of the pesticides they used and switching to organic farming. As a result, they were, on average, older than the conventional farmers and also had higher education levels. This finding is similar to that of a study by Chouichom (2010) that reported longer-term farm experience (higher age) and higher education were supporting factors in the adoption of an organic farming system [
20,
21].
The conventional farmers were more likely to be male, probably because the inclusion criteria specified that the conventional had to spray pesticides and most of sprayers in Thailand are male. This may also explain the higher use of alcohol and smoking among conventional farmers, as these behaviors are more typical among Thai males. The prevalence rate of smoking in Thailand was 41.7% in males and 1.9% in females in 2007 [
22]. Females aged 15–18 years old and those over 60 years old had the lowest and highest smoking rates, at 0.1% and 3.6%, respectively [
22]. Males aged 15–18 years old and 41–59 years old had the lowest and highest rates, at 14.2% and 47.5% respectively [
22]. However, another explanation for the difference in smoking and alcohol use may be that training in organic farming emphasizes promotion of a better quality of life [
23]. Almost 48% of organic farmers regularly undertook heavy exercise. Regular physical exercise has been documented for primary and secondary prevention of several chronic diseases (e.g., cardiovascular disease, diabetes, cancer, hypertension, obesity, depression) and premature death [
24].
Regarding stress, both groups encountered similar stress problems, which could be due to economic difficulties. Approximately 35% of conventional and organic farmers were in debt and 57% of the organic farmers had a second job in addition to agricultural work. In 2013, of the 4.8 million people living in rural areas where most are working in agriculture, 10.9% lived in poverty. The poverty line in 2015 was USD83/month [
25]. Organic farming in Thailand is still at an early stage where the majority of the organic products are rice and fresh vegetables [
26]. At present, the Royal Project Foundation, a government program, has helped farmers to overcome the initial constraints to conversion from conventional to organic farming. Nonetheless, organic farmers still encounter concerns as price stability, product marketing, and the need for continued government support [
27].
Most conventional farmers (85%) lived within 1 km of their farms which could result in greater opportunity for pesticide spray drift and take-home pesticide exposures. Most of the organic farmers (65.1%) drank bottled water, while most conventional farmers drank filtered tap water. Pesticide contamination levels in commercial bottled water or government-provided tap water have not been reported. In addition, a small percentage of both conventional (5.1%) and organic (2.7%) farmers reported drinking well water, where the pesticide contamination of the ground water has not been assessed. The selection of drinking water depends on availability, affordability and safety perception. Eighty-nine percent of the pesticide using farmers reported home use of insecticides to get rid of mosquitoes and other insects. Mosquito repellants may contain insecticides depending on the brand used. For example, most mosquito coils contain pyrethroids.
In this study we found a prevalence of metabolic syndrome of 38% among conventional farmers and 40% among organic farmers. This compares to the working population Thai professionals and office workers in Bangkok where the overall prevalence was 15.2% and was approximately three times higher in men than women (25.8% vs. 8.2%). Among this “white collar” population, the most common abnormalities in men were high blood pressure (45.0%), BMI >25 kg/m
2 (40.7%), and hypertriglyceridemia (38.7%) [
28]. Among women they were high blood pressure (22.8%), BMI > 25 kg/m
2 (20.9%), and low HDL-cholesterol (18.4%). In the general Thai population, the prevalence of metabolic syndrome was 23.2% for adults aged ≥20 years (19.5% in men and 26.8% in women) from the fourth Thai National Health Examination Survey (NHES IV) 2008–2009. In rural areas, men who had metabolic syndrome were older and more obese, with higher levels of blood pressure, fasting plasma glucose, and triglycerides but lower levels of HDL and education than those who did not [
29]. In this current study, 74% of organic farmers had BMI in the normal range, which was significantly greater than the conventional farmers (58%). However, there was no significant difference between the percentages of conventional and organic farmers who had an abnormal % body fat or an abnormal waist circumference. This may be because the criteria for normal and abnormal % body fat and waist circumference take into account gender, while the criteria for abnormal BMI does not account for gender. Because there were more men in the conventional farmer group, and men tend to have more muscle mass, their BMI may be higher and fall into the “abnormal” range even though their % body fat or waist circumference do not. Another explanation for the difference in BMI could be that organic farming is more labor-intensive, while chemical farmers use more agricultural machinery in their operations [
20]. However, use of insecticides [
30] or other persistent organic pollutants (POPs) [
31] and endocrine disrupting chemicals (EDC) [
32], like those used by conventional farmers, have previously been linked to increased risk of obesity. Pesticides may cause obesity by altering homeostatic metabolic set-points, disrupting appetite controls, perturbing lipid homeostasis to promote adipocyte hypertrophy, or stimulating adipogenic pathways that enhance adipocyte hyperplasia during development or in adults [
33,
34].
Conventional farmers were significantly more likely to have abnormally high biomarker levels for TC and LDL, but organic farmers were more likely to have abnormally low biomarker levels for HDL. Abnormally high TC and low HDL are two risk factors for metabolic syndrome. This may explain why there was no significant difference in metabolic syndrome between these two farming types. The prevalence of metabolic syndrome in the current study (38.2–40.1%) is considerably lower than the 60% in the Anniston Health Study sample [
35] carried out in agricultural workers, because our study recruited subjects free of a current diagnosis of diabetes, high blood pressure, and thyroid or heart disease. In this study there was no significant differences in abnormal blood pressure between conventional and organic farmers. However, Samsuddin et al. (2016) found that mosquito control workers with chronic mixed pesticide exposure had significantly higher brachial and aortic diastolic and systolic blood pressure levels compared to the control group [
36]. POP exposure may contribute to excess adiposity and other forms of metabolism dysfunction [
31]. Organochlorine pesticide exposure was significantly associated with the risk of metabolic syndrome in the Anniston Health Study population, while no association was observed for PCBs [
5].
Organic and conventional farmers differed in a variety of characteristics, including education, age, gender, alcohol and smoking behavior, exercise, water consumption patterns, food intake, pesticide use at home, and years of pesticide use. Once these factors were controlled for in multivariate models for the risk of an abnormal health outcome/biomarker level, there still remained an association between farming group and most health outcomes. This suggests that current pesticide use (near-term exposure) may be an important risk factor in altering metabolic biomarkers. This finding should be replicated in other contexts to ensure that it is generalizable to other populations of farmers currently using pesticides versus those who do not. In the Dominican Republic, a study of pesticide-using vs. organic farmers found significantly higher rates of nuclear anomalies among the pesticide using farmers compared to non-exposed organic farmers, suggesting the pesticide farmers could be at higher risk for developing cancer [
37]. In addition, pesticide-using farmers had significantly increased symptom frequencies related to symptoms of neurotoxicity, parasympathic effects, and acetylcholine esterase inhibition compared to organic farmers [
38]. The biology of these effects are not known, but there is increasing evidence linking exposure to endocrine disrupting chemicals (EDCs) with obesity and metabolic syndrome in animals, especially when exposures occur early in life [
32]. For diabetes, there is growing evidence from human studies linking exposure to EDCs with type 1 and 2 diabetes [
39,
40]. In a meta-analysis of 14 epidemiologic studies, there was an increased risk of coronary heart disease among those with subclinical hypothyroidism (normal thyroxine (T4) with high thyroid stimulating hormone (TSH)) [
41]. Triglycerides, TC, and LDLs have been shown to increase with increasing TSH levels, and HDL decrease with increasing TSH levels [
42]. In addition, as TSH levels increase, both systolic and diastolic blood pressure increase [
43].
The strength of this study is that it is the first to compare organic and conventional farmers’ health outcomes and the first in Thailand to examine metabolic syndrome risk factors and outcomes among Thai farmers. However, a limitation of the study is its cross-sectional approach, which makes it difficult to propose causal associations. The comparison of current pesticide uses versus those who do not currently use pesticides (organic) was confounded by a number of demographic and behavior factors that differed between the two groups. Thus, we cannot be sure that even after including a number of these factors in our final model, that the designation of organic versus conventional is not a surrogate for additional uncontrolled behavioral risk factors rather than the current use of pesticides. Future work will include evaluation of the longitudinal differences in health outcomes in these two groups as well as studies of the impact of acute pesticide exposures on some of the biomarkers evaluated here.