Introduction

Poisoning due to pesticides and insecticides is a common occurrence in Senegal, particularly during the rainy season (from May to August). Each year, the department of Plants Protection of the Senegal Ministry of Agriculture is informed of the number of cases of diseases and deaths following the ingestion, contact, and/or inhalation of toxic substances (Boye, 1995). Unfortunately, these cases are not investigated, making it difficult to identify the main cause of poisoning in farmers.

In August of 2000 several cases of a disease characterized mainly by effort dyspnea, thoracic pain, and edemas of the lower limbs and face were observed in the area of the village of Tankon. This village is situated in the medical district of Sedhiou, Region of Kolda (see Figure 1). The administrative Region of Kolda is composed of three districts: Kolda of the same name, Sedhiou, and Velingara. No cases were observed in the district of Velingara. A rapid situation assessment carried out by the Sedhiou's district head doctor on August 30 indicated that six deaths (including three in the same family with the same clinical manifestations) had occurred in Tankon since July 2000. Three other deaths had occurred in the villages of Tievel Birane, Digante, and Samba Thioune, all located in a perimeter of 12 km (7.2 miles) around Tankon. Cases of deaths were also reported at the villages of Sare Daouda, Sare Sama, and Sare Doro Thiam, located in the area bordering the district of Kolda and at the villages of Sam Toulou and Sare Sara in the district of Kolda. They were for the most part adult men, and the first symptoms went back at 1 or 2 months from the moment of the examination. Apart from the described symptomatology, the patients presented hypotension and bradycardia. For those surviving the overall condition was preserved.

Figure 1.

Map 1: Area in which deaths and disease were observed.

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A two-stage investigation was carried out in September 5 to 10, 2000 and November 3 to 18, 2000, coordinated jointly by the National Service of Endemic Diseases (SNGE), the Pasteur Institute of Dakar (IPD), and the Health Division of the Region of Kolda.

First-stage investigation

Methods

At the first stage, the villages of Tankon and Sam Toulou, in which the number of illnesses and of deaths noted was larger, were selected to the investigation. There were three objectives of this stage: (1) to confirm the existence of an epidemic, (2) to document the cases of diseases and deaths, and (3) to obtain information to guide the search of the etiology.

Observations

The two villages are parts of an agricultural perimeter where cultures of rents (cotton and groundnut) are practiced alongside with food crops (corn and millet). Farmers' use of several types of pesticides and insecticides were described; most of these products were traded clandestinely.

Thirty-nine subjects were identified in the area. They presented thoracic pain (94.9%), edemas of members and face (76.9%), dyspnea (82.0%), or all the three signs (64.1%) from April 2000 to the day of the examination. In addition, approximately 50% of the subjects reported fever, 30.8% reported shivers, and 38.5% reported sweating. Abdominal pains were infrequent (20.5%) and primarily preceded death. There were rare neurological manifestations (2.6%), paresthesias without gravity. Hemorrhage was not observed and four subjects presented icterus, three among them just before death.

The Pasteur Institute of Dakar performed the laboratory analyses. Serologic tests to detect IgM for arboviruses (yellow fever, dengue 2, west nile, Rift Valley Fever, Chikungunya virus, and the Crimea Congo) on 57 samples were negative. Search of bacteriological agents was also negative after 10 days of setting in culture. Biological analyses carried out on four patients of Tankon presenting edemas of lower limbs, effort dyspnea, and thoracic pains between 19 to 45 days were close to the usual standards, with the exception of an intense neutropenia. Biological, virological, and toxicological analyses added to the clinical manifestations did not allow the identification of either the causes or the agent of this epidemic.

Epidemiological evidence suggested that the etiology of the intoxication is due to a pesticide or another chemical substance provoking a respiratory or cardiac disease. Clinical manifestations did not suggest an infectious etiology; fever was absent in 50% of the subjects; the general condition was preserved for the surviving cases. Biological parameters remained in the usual standards. In addition, there was no obviously evidence of interhuman transmission.

In November 2000, a second team was sent to the area of the epidemics to perform a case–control study and to shed light on the etiology of the deaths. The other objectives of this second stage were to define the geographical area of the epidemic, to consult the files of the health centers and health posts of the area, and to improve description of the epidemic. This phase also involved interviews with personnel of the Ministry of Agriculture and chemical industries involved in the distribution and marketing of the pesticides in the region of Kolda.

Second-stage investigation

Methods

The second phase of the investigation took place between November 4 and 18, 2000. A case–control study was conducted in all villages in which deaths had been notified. It consisted of a study of the risk factors and practices in pesticide use. The case was defined as any human subject living in the area of the epidemic since January 2000, and having had dyspnea or edemas of members and face or thoracic pain since January 2000. The controls, paired by sex and age, were selected in the case household and in the nearest household to the case household.

Attempts were made to find records of the cases in the health centers and in the health posts without success. The files were, in general, badly kept. Cases of "dying just at the door," those consulting during the night, or those who were consulted informally by health personnel they knew and/or worked with were not registered in the files. Moreover, a considerable proportion of the cases crossed the borders to have medical consultations in Gambia. A significant number of cases sought care from a first-aid worker attending in a private consulting room in a small village close to Tankon. Although the information he provided was very detailed and agreed with information given by cases and controls, he was illiterate, and no information about the disease had been written and filed.

Initially, district health teams of Kolda and Sedhiou identified the cases. Residents spontaneously indicated other villages where cases of the disease had been observed. Nevertheless, due to the short time assigned to the investigation, some of these villages were not visited. Since the goal of the investigation was not to exhaustively search for cases, but to obtain a better description of the disease and to identify the causes of the epidemic, the number of villages not visited should not negatively influence the results of the investigation.

In addition to the data of the case–control study, interviews were carried out with members of five manufacturers and/or distributors of pesticides in the area: (1) the Company of Development of Textile Fibers (SODEFITEX), (2) the National Company of Oilseeds Trade of Senegal (SONACOS), (3) the Direction of the Protection of the Plants (DPV) of the Agriculture Ministry, (4) the National Company of Oilseeds and (5) Senegal Chemicals (SENCHIM). The Direction of the Analysis of the Prediction and Statistics (DAPS) of the Ministry of Agriculture was also consulted. The SODEFITEX is a mixed investment company that has as essential role the development of the industry of cotton in Senegal. The DPV is responsible for the definition and the implementation of actions aiming to fight against the depredators of agrocultures, particularly in relation with the rural populations. SONACOS is a state company affiliated to the DPV responsible for the support and follow-up of the agricultural activities related to the groundnut culture such as pesticide distribution, also in relation to rural populations. The SONAGRAINES is a private company that ensures for the Ministry of Agriculture the distribution of agricultural products such as fertilizers, herbicides, and pesticides. The DAPS is in charge of the of analysis, preparation, follow-up evaluation and control of the policies, programs, projects and actions of development and the collection, centralization, the treatment and the distribution of information and agricultural statistics.

Observations

The Epidemic Geographic Area

The geographic area of occurrence of the disease was approximately 40 km (24 miles) between the districts of Kolda and Sedhiou. It is a very enclosed area, linked to the main towns of the district by badly maintained tracks, making vehicular access to the area almost impractical during the rainy season. It was noted that there were no cases reported/identified in the villages located near the border with Gambia. The proximity allows residents of these villages to have easier access to medical attention from Gambia than from Senegal. The epicenter of the epidemic was the village of Sare Sama in the district of Kolda because the greatest numbers of cases of the disease were inventoried there.

The Disease

The cases occurred between the months of April and October 2000 (Figure 2). At the time of the investigation, 113 cases of disease including 22 deaths were recorded in 16 villages. Among these 113 cases, clinical manifestations are, by order of frequency: thoracic pain (87.3%), effort dyspnea (80.3%), edemas of the members (69.5%), fever (60.2%) and tachycardia (42.4%) (see Figure 3). Approximately 42% of the patients had sweating and 35.6% had facial edemas. The average duration of the disease before death was 15 days. Lethality was 21.6%. The majority of these deaths occurred in the villages before any medical intervention. At the time of investigation 13 (12.7%) were in convalescence and the 67 remaining (65.7%) were cured of the disease.

Figure 2.

Distribution of cases according to the month of the beginning of the disease and the final status of the case Kolda, Senegal, November 2000.

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Figure 3.

Symptoms reported by 113 cases Kolda Region, Senegal.

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Approximately 10% of the cases had sought care in public medical centers such as the health center of Kolda and health posts of the area, but no records of any of these cases could be found in health services' files. A private first-aid worker serving in the village of Goutou, close to Tankon, treated other patients. The treatment he used consisted of sulfate of atropine, corticoids, anti-inflammatory drugs, and traditional treatments containing plants and infusions with emetic properties. This treatment seems to have given good results as reported by cases.

The Epidemiology

The disease occurred mostly among young males: 82.3% of the cases were men aged between 12 to 60 years with a mean age of 35.5 years (32.6–3.4) and a median of 32 years. Ages of women ranged from 10 to 60 years with a mean of 32.3 years (27.4–37.2) and a median of 32 years. The possibility of a transmittable disease was excluded by the fact that the contacts very close to the patients (for example, wives and children) in the households did not contract the disease. There were two cases of children less than 13 years old and 20 cases of women (see Table 1).

Table 1 - Distribution of the cases by sex and age group.

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The case population consisted of farmers (74.1%), housewives (18.1%), tradesmen (1.7%), and 4.3% of various occupations such as craftsmen and marabouts — a kind of religious leader. All cases were involved in farm work during the period of groundnut planting. The cases were clustered in the same households rather than randomly distributed in the villages. In approximately 73% of the cases, there was more than one case in a household whereas for the control this proportion did not exceed 30% (see Table 2).

Table 2 - Odds ratio, 95% confidence interval (CI) and test for the odds ratio for risk of disease.

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The hypothesis of intoxication caused by medication was discarded. No particular drug could be identified as being the source of intoxication. In addition, data yielded that controls were overall sicker and used more drugs than the cases during the period preceding the epidemic. It is worth noting that in general the consumption of modern drugs by the population was small given the difficulty of access to the health centers and lack of financial resources.

Case–Control Study

The analysis of the data of the cases and the controls paired by sex and age group is presented in Table 3. The cases and the controls did not differ significantly from the factors studied: occupation, displacements during the last 6 months, the presence of pesticides in the household, and the handling of these pesticides. Indeed, there were no differences between cases and controls related to the presence of pesticides in the household. Cases and controls also reported having used the pesticides Granox and Spinox during the period that preceded the epidemics. Unfortunately, farmers who used pesticide clandestinely, fearing to be punished, made it difficult to obtain details on the type of use and dosages of the pesticides.

Table 3 - Distribution of the cases and the controls according to the number of cases that have occurred in the household.

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A significant difference was observed between cases and controls with regard to antecedents of other diseases during the last 6 months and the number of cases in the household. Cases were 7.3 times more likely not to have been sick and 3 times more likely not to have taken any medication during the last 6 months than the controls.

In approximately 73% of the cases, there was more than one person who had the disease in the household whereas at the control this proportion did not exceed 30% (see Table 3). Whereas risk of disease was not significantly associated with the frequency of contacts with cases outside of the household (²=0.11; P=0.75), the risk was 5.6 times higher (95% CI=3.1–10.4) when there was more than one case of the disease in the household.

Culture of Groundnut

The groundnut is an extensive crop and represents a surface of 179,042 acres in the region of Kolda. The surface used for cotton plantation does not exceed 50,000 acres. The review of the evolution in acreage, productivity in kilograms per hectare and total production of groundnut in Senegal shows that since 1998, with incentive in seeds and pesticides provided by the government, the groundnut oil farming recorded an important improvement as compared to the previous years (Ministry of Agriculture of Senegal Republic). Thus, in the whole of Senegal, the production increased from 416.8 kg/acre in 1998 to 440 kg/acre in 1999. This increase in acreage and gain in productivity resulted in a rise of the country's total production from 540,773 tons in 1998 to 950,000 tons in 1999 (Ministry of Agriculture, 2000). During 2000–2001, although there was an increase in the number of seed and pesticide recipients, certain areas of the country showed a reduction in the acreage. In the region of Kolda, a reduction was observed in the acreage at the same time, as there were improvements in productivity and increases of the total production of groundnut oil mill. According to experts from the Ministry of Agriculture, this phenomenon can be explained by the availability, in quantity and quality, of sufficient seeds and pesticides, as well as a good rainy season.

Pesticides

In the 2000–2001 agricultural period, several pesticides were used in the area of Kolda: at the time of storage, between December 1999 and January 2000; for the conservation of seeds, between February and March 2000; and at the time of distribution of seeds to farmers and planting, between May and the end of August 2000.

SONACOS and SONAGRAINES distributed pesticides to small farmers and heads of households an amount of seeds and fungicides made up of 15% Thiram, 7% Benomyl, and 10% Carbofuran. Annually, the Ministry of Agriculture promotes bids to the purchasing of fungicide. In 1999, SECHIM, the manufacturer of Granox, won the bid, and in 2000, SPIA the manufacturer of Spinox was the winner. The two products have exactly the same composition.

The components Thiram, Benomyl (C14–H18–N4–O3) and Carbofuran (C12–H15–N–O3) are pesticides from the chemical group of carbamates. Among all classes of pesticides, carbamates are most commonly used because the alternatives (organochlorines and organophosphates) are extremely toxic and have a problem of delayed neurotoxicity. Carbamate is a generic name given to salts of the carbamic acid whose formula is NH₂CO₂H. Thiram is a biscarbamate, which is a generic name given to the molecules containing at least two carbamate, thiocarbamate, or dithiocarbamate groups. Thiram contains two dithiocarbamate groups connected one to the other by sulfur atoms (C6–H12–N2–S4). Carbamates are widely used in agriculture for the protection of vegetable crops and seeds from fungal disease. Carbofuran and Thiram are highly toxic; they may be fatal if inhaled, swallowed, or absorbed through the skin, even though effects of contact and/or inhalation may be delayed. Benomyl is mildly toxic but may be also fatal if inhaled, ingested, or absorbed through the skin. Thiram is commercialized as a wettable powder, dustable powder, slurry for seed treatment, dry seed treatment, and suspension concentrate (Hartley and Kidd, 1987). Carbofuran is found as a granule, flowable, wettable powder, and flowable concentrate for seed treatments (Farm Chemicals Handbook, 1994). Benomyl is found as a dry flowable, oil dispersible, wettable powder (Farm Chemicals Handbook, 1991).

Carbofuran is commonly used as an insecticide, nematicide, or acaricide in agricultural practices throughout the world. It is the most toxic of the three substances. Exposure causes a rapidly reversible direct cholinesterase inhibition. Overstimulation of muscarinic and nicotinic receptors can result in toxic manifestations of central and peripheral nervous systems. Carbamates are well absorbed from all routes of exposure. Poisoning may occur from inhalation, oral, dermal, or ocular exposure; however, the compound is more toxic by ingestion than by dermal contact (Rumack, 2001; Hall and Rumack, 2001). The substance breaks up under extreme heat, producing toxic fumes that give off nitrogen oxides. A dangerous concentration of particles suspended in the air can, however, be reached quickly by dispersion, especially if the product is in the powder form. In recent years in western countries, carbamates are mostly presented as a liquid preparation that is less toxic than the powder formulation (Simpson and Burmingham, 1977). The effects of exposure even of short duration can be delayed and there is a possibility of cumulative effects (Gupta, 1994).

Intoxication by inhalation with carbofuran causes muscarinic and nicotinic signs of intoxication. The digestive signs are almost absent as compared to intoxication by ingestion and respiratory symptoms appear very early: cough, throat pain, asthmatic dyspnea, and bronchial hypersecretion (ICSC, 1993). Following there is the fast appearance of the muscarinic and nicotinic signs of intoxication. The muscarinic signs are myosis, hypersalivation, bradycardia, arterial hypotension, and asthmatic dyspnea. The nicotinic signs are muscular fasciculations, cramps, involuntary movements, and paralysis of the respiratory muscles, then tachycardia, hypertension, confusion, ataxia, convulsive coma, risk of haemodynamic shock, and bronchial obstruction by hypersecretion and bronchoconstriction (Teletox). The antidote to carbofuran intoxication is atropine 2 to 4 mg IV in the adult and 0.04 to 0.08 mg/kg in the child until the disappearance of the bronchospasm (ASITEST). In California, symptoms most commonly reported by 34 farmers presenting illness following exposure to carbofuran were nausea, headache, eye irritation, muscle weakness, tearing, vomiting, and salivation. The most commonly observed sign was bradycardia (Anonymous, 1999).

Thiram is a fungicide. It can enter the human body through the inhalation of dust, among other routes. Thiram is not a cholinesterase inhibitor. Toxic effects of thiram are mostly related to its metabolism and inhibition of certain enzymes produced by thiram or its metabolites. Excessive exposure to thiram may produce irritation of mucous membranes, conjunctivitis, rhinitis, sneezing and coughing in the exposed subject (Dalvi, 1988). Treatment of thiram intoxication is mainly supportive. No specific antidote is commercially available. In a group of 223 workers in the former USRR, mostly between 20 and 50 years of age and engaged in the manufacture of thiram generally for more than three years, various clinical and pathological manifestations including ocular irritation, coughing, thoracic pain, tachycardia, dermal lesions, myocardial dystrophy, clinical and subclinical liver dysfunction, and asthenia were reported (Cherpack et al., 1971).

Benomyl is a carbamate fungicide with a low degree of toxicity. Exposure is not associated with signs and symptoms of cholinergic stimulation. Systemic symptoms have rarely been reported following exposure. Nevertheless, by inhalation exposure, cough or difficulty in breathing, respiratory tract irritation, bronchitis, and pneumonitis may develop (Rumack, 2001).

Planting and the Use of the Pesticides

In the framework of Senegal's new agricultural policy, the improvement of the productivity of groundnut farming is a priority to the government. It includes extending the list of the small farmers profiting from the seeds and the pesticides. For the 2000–2001 agricultural campaign, recipients were not only the heads of households but also the heads of families. In Senegal, as in most African countries, the household is commonly called "the widen family" composed of the father — the head, his wives, their descendants, their spouses, grandchildren, other relatives, and domestics. A household can accommodate several families. A family is just the nuclear family as known in western countries: a man, his wife, and their children. Thus, the quantity of pesticides available and in circulation could be doubled in each household.

During planting, the farmers use a seeder to spread out groundnut seeds on the ground. A certain quantity of pesticide is put into the seeder, which is then filled with groundnut seeds. Various people from the household operate the equipment, which is drawn by an animal from traction. They are in general the young men, who are strong enough to handle the seeder. During the installation of the powder in the container and mixing of the product with seeds, the individuals are exposed to the product by inhalation and contact. No protective measures (i.e., gloves and masks) are used. According to the direction of the wind, the individuals who handle the powder sometimes inhale quantities of the product during the filling of the seeder. The period of planting takes place between May and July depending on the beginning of the rains and lasts between 5 and 10 days according to the size of the land to be cultivated.

Among the new recipients of the distributed seeds many did not cultivate for various reasons, in particular because they either ate the seeds, did not have enough workers to participate in the farm work, or thought that the seeds were not of good quality. The majority of those who did not plant but received the seeds then sold the unused pesticides to the neighbors who used them in greater quantity in their fields.

In addition, certain villages did not have time to update the list of recipients, or did it very late and did not receive seeds or pesticides. This was the case with some villages around Tankon (Goutou Demba Ba, Goutou Demba Diop, and Goutou Samba Diallo, for example). Cases of the disease were not observed in these villages.

During the investigation, the team interviewed various members in the households about the use of pesticides. Thefarmers familiarly call these products "the powder." These powders are named the "pink powder" or the "bluepowder" according to the brand, the company of manufacture, and the year of distribution. For example, this year one speaks about blue powder, to refer to Spinox manufactured by the SPIA and distributed into 2000 with the seeds. In 1999, it was the red powder, which referred to the Granox manufactured by Sechim, which won the bid in 1999. According to the SONACOS, when 1-year-old pesticide remains, it is distributed at any beginning of the groundnut campaign with the first farmers who come to withdraw the seeds. This was the case for the marketing year 1999–2000 when the remainder of Granox used during the preceding campaign was distributed to the first farmers receiving the seeds.

These products have many other uses than their initial designation. They are used in the hair to kill lice, on the walls to kill termites, under the mattresses to kill bugs, among other domestic uses. Although the handling of these products is prohibited from use by women (childbearing age) and by the children, the team observed that the boxes were accessible and the women were the first users. Unfortunately, most of the interviewed farmers were unable or did not want to specify the quantity, the brand or the color of the pesticides received during the current year or the previous years. In the same households, some people invariably denied the use of such products, whereas others affirmed the opposite. An analysis of four samples of the two products used by the farmers in the phase of groundnut planting (Granox and Spinox) did not show any irregularity in the content of active matters in the products. A comparative analysis of the two formulas that were found in the houses confirms that the products present the same chromatographic profile. No other analyzable active substance was detected by the gas chromatography procedure. The Wolff Laboratory in Paris carried out these analyses.

Discussion

The observations above make it possible to draw several conclusions. First, the fact that the cases are clustered in the same households and in certain age brackets, rather than by chance in the villages, argues in favor of an internal source of contamination to the households. Second, the idea of contact with a sick person does not constitute a risk factor. Third, the hypothesis of an infectious disease can be eliminated if the subjects having a very close contact to the cases in the households were not affected (i.e., wives, children). Fourth, there was almost no case in children (2 over 113) and very little cases among women (20 among 113). Furthermore, the age and sex distribution of cases made it possible to exclude the argument of contamination coming from basic food. In the households, the meals are prepared for the whole family, and although the meals are comprised of several dishes, they are prepared under the same conditions for all members of the household. In the same way, individuals in the household consume water taken from various containers or pots within the house but this water comes from the same sources. These observations corroborate the assumption of intoxication. The fact that the controls used more medicines than the cases during the previous months does not argue in favor of intoxication due to this kind of substance.

There was no difference between the cases and the controls with regard to the main occupation: farm work. The distribution of the episodes of diseases in time and space shows that the cases were concentrated in the area of groundnut culture after the beginning of the rains and for the period of farming work, with a maximum peak during August, which corresponds to the month when farmers had begun or finished planting. All the cases in males and a considerable proportion of females were involved in this activity. Although this relationship could not be established for a certain number of females, the distribution of cases recalls a mode of contamination related to the culture of groundnut. However, the cases and the controls all were farmers and participated in the work of groundnut planting, the greatest number of various diseases in controls shows that they were less exposed to farming work than the cases because of their illnesses.

Conclusion

The signs and the symptoms of the disease suggest intoxication by carbamates and clinical manifestations indicate a mixture of effects of carbofuran and thiram. Why did this epidemic occur in that particular year? The hypothesis is that the extension of the number of pesticide recipients caused an overconsumption of these products and thus an overexposure of the subjects who handle the seeders, i.e., young males and a small proportion of women who work in groundnut fields. Moreover, many of the new farmers, not being accustomed to handling the pesticides, could overestimate the necessary amount to fill the seeder. Why did the epidemic occur in this area of the Region of Kolda and not in other areas of the country that also practice the groundnut culture? Kolda was the only area of Senegal to present an increase in the productivity and total production of groundnut while decreasing the acreage. This means a greater concentration of people and pesticides in the same space, thus increasing the exposure of a greater number to the risk of intoxication. It is to be considered regrettable that the policy of distribution of pesticides in Senegal, which presents without any doubt a risk of poisoning, is not accompanied by better information to the farmers on the danger of these products, and of the necessary precautions to be taken during their use, in particular to wash hands, to use masks and gloves, and to deviate from the wind.

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