A previous study suggested that banned organochlorine pesticides were being used to protect illegal crops from pests. The study herein explored the exposure of individuals living in a region with such crops. Samples from 99 individuals were collected during 2005 and 2006 and organochlorine pesticides were quantified using chromatography in serum samples. We detected heptachlor (72.73%), 4,4-DDE (19.19%), aldrin (15.15%), γ-chlordane (12.12%), dieldrin (11.11%), α-chlordane (10,10%), α-endosulfan (8.08%), endosulfan (6.06%), β-endosulfan (5.05%), oxychlordane (3.03%), 4,4-DDT (3.03%), and 2,4-DDT (2.02%). Heptachlor had a skewed and negative distribution (median: 8.69 ng/l and maximum: 43.8 ng/l). A two-dimensional biplot suggested that mixtures present were endosulfan/4,4-DDT, aldrin/γ-chlordane, and oxychlordane/β-endosulfan/dieldrin. We didn't identify variables associated with exposure levels. These data suggest that banned organochlorine pesticides are used. This is an example of research in a war context, where the problem related with pesticides is complex, and their implications go beyond a toxicological or epidemiological problem.
Key words: Organochlorine pesticides; agriculture; communities; farmers; Colombia.
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Coca (Erythroxylum coca) and poppy (Papaver somniferum) are cultivated in Colombia, although such activities are considered illegal. According to estimations by the United Nations Office on Drugs and Crime, coca production ranged from 600 to 640 metric tons annually between 2004-2007.1 In response to this problem, the Colombian government has implemented various strategies to eradicate illegal crops. An important intervention is chemical eradication with the herbicide glyphosate, which has been used since 1984, with some brief interruptions during which other herbicides were used.2
In recent studies on potential adverse effects of glyphosate any banned pesticides were detected in environmental samples from regions with illegal crops.8 This suggested that some organochlorine pesticides may be used by coca or poppy growers to protect their crops, even though Colombia has restrictive legislation regarding its use. If this is the case, its use could have adverse effects on human health, especially for those exposed as a result of their work in these activities.9 In this country during approximately four decades DDT was used to protect different licit crops, however in 1986 its use was restricted to the malaria eradication program. Although actually there is a lot of DDT stored in governmental wineries, it was totally banned in 1993 (Sánchez). After other organochlorine pesticides were banned since their adverse effects on humans, animals and/or ecosystems, following similar actions in another countries (see Table 1).
Colombia is localized in the tropics, thus rainfall, temperature, sunlight, and microorganisms are important elements involved in pesticide dissipation. Rainfall is primarily responsible for the washing off of pesticides from their treatment sites. In regions with tropical temperatures vaporization of pesticides tends to be greater than temperate regions. In the tropics sunlight is intense, causing direct photolytic effects (photodecomposition) and faster pesticide degradation. Higher microbial activities and hence enhanced microbial degradation have been observed in tropical temperatures (Magallona). The behavior of these elements suggests that pesticide dissipation occurs more rapidly in tropical environments (Racke). Although there are few studies about this topic in Colombia (mainly in coastal environment) (Castro), theoretically the simple detection of organochlorine pesticides suggests actual illegal use or during the previous years.
Peasant growers may prefer to work in illicit crops because they can generate far higher earnings than with legitimate crops. If they use banned pesticides is difficult that they inform to authorities about exposure and related adverse effects. They would be committing a double crime according to Colombian law. These unobserved and forgotten individuals live with inherent conditions of vulnerability and are often neglected by health services. Furthermore, it is well known that exposure to toxic agents among vulnerable populations is a problem of environmental justice.10 Therefore, a priority should be to explore exposure levels and potential adverse health effects. It is, however, difficult and risky to conduct studies such as the one herein, where the research team could be a victim of violence in these regions.
The objective of this study was to evaluate the concentrations of 13 organochlorine pesticides in individuals living in regions where illegal crops are cultivated. This screening study was possible because an assessment of the health effects potentially associated with pesticides related with illegal coca or opium poppy crops was performed. This was a unique opportunity to explore the presence of some banned pesticides among a population usually forgotten by health authorities. In Colombia there are only two previous studies about organochlorine pesticides concentrations among different populations realized in 1973 and 1986 (Guerra; Hernández), thus this new study permits to actualize information about exposure to banned pesticides. The evaluation of exposure to permitted pesticides, as well as work conditions, is published elsewhere.11
Materials and methods
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During 2005 and 2006, a cross-sectional study was conducted with 112 agricultural workers from the following Colombian states: Antioquia, Guajira, Guaviare, Huila, Magdalena, Putumayo, Santander, and Tolima. The survey included demographic, occupational, toxicological and clinical data of agricultural workers. The unique inclusion criterion was that participants had used pesticides in farming activities during the past two years. The workers were informed about the goals of the study, and those who voluntarily agreed to participate individually provided written informed consent before they were administered a questionnaire and had a blood sample taken. This study was approved by the Research and the Ethics Technical Committee of the National Institute of Health, Colombia.
Handling of samples and quantification of pesticides. Blood samples (10ml) were drawn from an arm vein and collected in tubes without anticoagulant. After clotting, serum was separated by centrifugation. Serum samples were immediately frozen and sent to the Environmental and Occupational Health Group at the Colombian National Institute of Health. Organochlorine pesticides were quantified by gas chromatography. The 13 pesticides studied were: heptachlor, α-chlordane, γ-chlordane, oxychlordane, aldrin, dieldrin, β-BHC, 4,4-DDE 2,4-DDT, 4,4-DDT, α-endosulfan, β-endosulfan, and endosulfan sulfate.
Statistical methods. First, pesticide concentrations were described based on the percentage of detectable results, and central tendency and dispersion were measured (mean, standard deviation, 25th, 50th, 75th and 90th percentiles, and minimum and maximum values). Only heptachlor was detected in more than 70% of individuals. Since it had a skewed and negative distribution (p<0.001, skewness and kurtosis test for normality), its distribution was explored using kernel density estimators,12 a non-parametric way of estimating the probability density function of a random variable. The small sample size did not permit a more detailed analysis of other pesticides. Finally, mixtures of pesticides were investigated with a standardized two-dimensional biplot, which is a multivariate graphical method that expresses the variance-covariance of the variables, the values of the observations in relation to the variables, and the Euclidean distances between observations.13 All analyses were performed with the Stata 11 statistical program (Stata Corporation, College Station, Texas).
Table 1 shows the organochlorine pesticide concentrations detected. Note that information was used for only 99 individuals. Some individuals (n=13) were excluded because their serum samples could not be processed. All organochlorine pesticides, except heptachlor, were detected in less than 20% of individuals. β-BHC was not detected among participants. An important finding was the notable negative asymmetry in concentration distributions.
Table 2 shows the principal characteristics of study participants according to whether or not heptachlor was detected. There were no differences with regard to sex, age, education level, occupational exposure, use of personal protective equipment, or opinions about the government's chemical eradication program. The only difference found was related to geographical location, due to sparse exposure to heptachlor in the state of Antioquia. Additionally, we explored whether or not 40 different commercial pesticides were associated with the presence of heptachlor, but we did not detect differences between exposure groups (with and without heptachlor).
Figure 1 shows the kernel density probability plot of heptachlor serum levels using 3.2938 as the smoothing parameter. Note that most participants had low concentrations <20 ppb (ng/L), although a few agricultural workers had concentrations above 40 ppb (ng/L). Figure 2 shows the two-dimensional biplot of 12 organochlorine pesticides and serum levels. Note that the majority of individuals had very low concentrations. It was possible to identify the following three mixture patterns among agricultural workers with higher serum levels: oxychlordane, β-endosulfan, and dieldrin; aldrin and γ-chlordane; and endosulfan and 4,4-DDT.
The main results of this study were the low exposure levels to organochlorine pesticides observed in the majority of participating individuals, with only a few individuals with high levels of organochlorine pesticides. Since the tropical climate of studied regions the presence of these pesticides suggests clandestine utilization of banned pesticides in Colombia, which is consistent with the previous report where organochlorine pesticides were detected in water in similar regions.8 In addition, our study was able to detect a higher number of pesticides.
The presence of heptachlor suggests persistent use, given this pesticide and chlordane having been banned since 1988. In addition, two previous studies in Colombia have reported heptachlor in human blood. The first, in 1973, detected heptachlor in peasants (median 4 ppb, minimum 2, and maximum 26),14 and in 1980 heptachlor was found in factory workers (mean 11 ppb), workers applying pesticides (between 0.5 to 0.75 ppb), and inhabitants from rural regions (mean 0.25 ppb).15 In a recent meta-analysis, heptachlor was the only pesticide associated with the occurrence of breast cancer, and therefore exposure to heptachlor must not be overlooked.16
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This study was exploratory and had some methodological limitations. The primary restriction is the lack of representativeness of findings, and it is therefore not possible to extrapolate results to the entire Colombian population. This was due to the logistic difficulties in regions with illegal crops and informal militia groups, where there is a large degree of population mobility. This is one of several well known challenges for researchers studying vulnerable populations.17 Health research in war contexts is, indeed, a challenge to researchers. Obtaining data can be very difficult and risky because research teams may be threatened by any of the sides in an armed conflict. A few years ago, Jimba recognized this difficulty during a medical research study with children from the Gaza Strip.18 Nevertheless, scientific research in these conditions can be used to solve some of the problems present during times of war. Good examples are studies on malaria, dysentery, epidemic typhus, wartime nutrition, and infections due to wounds among Allied soldiers during World War II,19,20 as well as the mental health of children living in war zones.21
In conclusion, where environmental health is concerned, social vulnerability is often associated with problems of injustice that are characterized by greater exposure, albeit known or unknown, to agents potentially harmful to human health.22 The results of our study indicate that only a small proportion of individuals were exposed to organochlorine pesticides, and that levels of organochlorine pesticides among participants were low, with the exception of heptachlor. It suggests that chlordane was the main pesticide used in regions with illegal crops, but unfortunately we do not know whether this pesticide is used directly on coca and poppy crops or on legal crops. The organochlorine pesticides used in Colombia during more than 40 years were cyclic hydrocarbons, very stable in different ecosystems and non-biodegradable. Their biomagnification and bioaccumulation effects can explain the presence among these peasants.23 This data will serve as a baseline for subsequent assessments of the environmental and health problems associated with eradicating illegal crops and pesticides.
Debido al conflict armado es difícil tener acciones que vigilen el uso de plaguicidas ***