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| Human Health and Agroecosystems: Making the Links |

Document(s) 3 of 5
Donald C. Cole
Donald C. Cole McMaster Institute of Environment and Health, Hamilton, Ontario Institute for Work and Health, Toronto, Ontario Collaborator with International Potato Center, Quito, Ecuador Published in New Directions in Animal Production Systems. Proceedings of the Annual Meeting of the Canadian Society of Animal Science, July 5-8, 1998, Vancouver, British Columbia, Canada. Edited by R. Blair, R. Rajamahendran, L.S. Stephens,M.Y. Yang
Introduction Agroecoystems can be linked to human health in two fundamental ways: by providing the conditions for human well-being and by acting as a source of an environmental burden of human illness (Eyles et al, 1996). The former draws on health promotion frameworks emphasizing agroecosystems major positive contributions to human health through the provision of the fundamental conditions and resources for health such as "shelter,... food, income,... sustainable resources" in a climate of "peace, social justice and equity "(WHO et al., 1986). The latter draws more on the perspective of toxicology, microbiology and epidemiology, viewing agroecosystems as sources ofpotentially damaging exposures (outside humans) which result in a measurable (e.g. via environmental epidemiology) or an estimable (e.g. via risk assessment or simulation modelling) burden of human disease or other health impairment. Both are relevant toan understanding of relationships between agricultural development and health (Weil et al, 1991) and in keeping with notions of health and sustainability (WHO, 1992). In this paper, we will briefly review the range of important conditions and exposures in North America and the developing world. We will then focus on the a particular problematic technology of great importance in agroecosystems of both the developed and developing world, pesticide use (Forget et al., 1993), with a case example of integrated economic-environmental-health modelling in the potato production system of highland Ecuador (Crissman et al, 1998). We will conclude with some reflections on the challenges in research and policy that we face in order to promote positive agroecosystem-human health links throughout the world.
Conditions for Human Well-Being The internal organization and external linkages of agricultural communities strongly influence the social and economic conditions which are crucial for human development. Explorations of such relationships in the developing world exemplify a social medicine perspective where such features as land ownership or access are prime determinants of human morbidity (Laurel et al., 1977). In Ontario, researchers such as Wall, Ramsey and others (Smit et al 1998) have similarly demonstrated the importance of such factors as community cohesion, self-reliance, childcare supports and other factorsin providing the conditions for mental and physical health, particularly for women with children. Similarly, inadequate health services and out migration can result in labour losses which in turn impede the development of more labour intensive approachesto sustainable agriculture (Donham, 1992). Food production and income generation are two prime purposes of agricultural production. Both can have positive effects on individual and household nutritional status provided that intra-household distribution issues are considered as much as overall amount (Weil et al, 1991; Pitt et al., 1990). The role of women's use of such income for food purposes is crucial to positive impacts on health. In Canada, concerns nutritional concerns include accessibility related to income issues (Joint Steering Committee Responsible for Development of a National Nutrition Plan for Canada, 1996) as well as safety from widespread contamination (Waltner-Toews, 1996). Adequate supplies of water of good quality is another major condition for human health. The most pervasive human environmental health issue world-wide is access to drinking water and sanitation. There is good evidence that provision of such services, particularly in rural communities, can result in substantial reductions in morbidity and mortality (Esrey et al., 1986) and increase in infant growth (Esrey et al., 1992). Reductions in household work for women in rural communities is another positive benefit. Evidence of theserelationships is sufficiently sound that the percentage of households with access to clean drinking water and sanitation facilities can be used as indicators for an agroecosystem. Nitrate contamination of water supplies, particularly farm wells, is another water quality concern both in developing and developed countries (Bogárdi et al, 1991). Several Canadian studies have demonstrated nitrate levels in a small percentage of wells that are sufficiently high to prevent water use by infants because of the risk of methemoglobinemia (e.g. Anon, 1997). Major concerns about water quantity are most apparent where an entire region is in distress due to inappropriate agroecosystem management e.g. Uzbekistan (Smith, 1991). Massive reductions in available water along with increased water and soil contamination in the Aral Sea Basin have been implicated in excessive morbidity and rising infant mortality in the entire region (Glazovsky, 1995).
Environmental Burden of Human Illness Focusing on specific conditions leads us to consideration of frank environmental burdens of illness or the contribution of biological and chemical contaminants and physical exposures to human injury and disease, either via direct or indirect exposure pathways. Estimates of such environmental burdens of human illness have been made globally by the World Bank (1993). Form the broadest perspective, we could consider the full range of activities which provide inputs to agroecosystems. For example, diesel use in farm machinery, may contribute to elevated cancer rates among not only farmers but also a variety of other workers in the extraction, refining and transportation sectors. Such life cycle analysis of a technology (common in the energy sector) usually uncovers a range of other potential exposures and health outcomes that can be linked to a particular form of agroecosystem management. We can also identify a vast array of hazards facing human agricultural populations per se (Dosman, 1992). In a more focused way, a range of disciplinary studies make links between specific activities or exposures and particular health outcomes, often using epidemiological tools. At the regional level, cross-sectional surveys have shown plausibly linked, high prevalence rates of schistosomiasis or other waterborne infectious diseases in populations around agricultural irrigation facilities in lesser developed countries (Hunter et al., 1982). Exposure to animal and human waste can result in gastrointestinal illness among swimmers but of greater concern have been large outbreaks due to cryptosporidium species overwhelming the clearing capacity of municipal water filtration systems in Waterloo, Ontario, and Milwaukee, Minnesota, drawing from Lake Michigan (MacKenzie et al., 1994). Such outbreaks are linked to contamination by farm animal excreta which is much more efficiently managed at the level of the watershed than via engineering solutions at thepoint of water supply. Similar issues are faced in lesser developed countries with cholera and marine ecosystems (Epstein et al, 1993). More controversial are studies associating agricultural activity, crop, fertilizer and pesticide use with higher rates of congenital malformations among human newborns (White et al, 1988; Garry et al., 1996). Individually-based case-control studies have also demonstrated relationships between family pesticide use in the home, garden, orchard and yard and childhood brain cancer (Davis et al. 1992; Davis et al.,1993) and between greater farm pesticide use and prolonged time to pregnancy among couples working fruit farms in the Netherlands. Although such case-control studies are important in delineating potential exposure-health outcome relationships, they are rarely tied to particular agroecosystems. Experience in more developed countries with attempts to link management strategies with human exposures and human health outcomes in particular agroecosystems have been few. In Ontario, VanLeeuwen documented a link between degraded groundwater and a deterioration in residents' health status over a 13 year period (p 63 in Smit et al., 1998). Yet making such links is difficult in more developed countries both because of the multifactorial nature of most chronic diseases (i.e. smoking, pesticides and diesels fumes could all contributes to increased rates of cancer in farmers) and the generally low level of exposures. In contrast, members of agricultural communities in developing countries often have considerably higher exposures through multiple sources. We shall now turn to research done by a multi-disciplinary team on agricultural production, environmental contamination and human health effects of pesticides in one such set of South American communities (Crissman et al, 1998a). The focus in on the human health and economic relationships for the purposes of this paper, though similar detailed work was done on pesticide leaching through different soil types in different agroecological zones.
Potato Production in Highland Ecuador: A Case StudySetting Potatos have been cultivated for millenia in the inter-Andean valleys where they remain a dietary staple. For small farmers, potato production represents an efficient use of land, primarily because of its short vegetative cycle and relatively high value in food energy, protein and potential revenue (Crissman et al, 1998b). The chosen study site, was in the northern province of Carchi, near the Columbian border, in the canton of Montufar. It has a dispersed rural population farming potatoes, grains and dairy cattle around a small town, San Gabriel. Farmhouses are scattered along ridge-top farm access roads. Pastures and cultivated fields lie between forest remnants and old hedgerows, in any stage of the crop cycle.
Agricultural Production The agricultural research team selected two watersheds and within them forty collaborating farmers, with some replacement over the life of the project. Through detailed prospective recording by these farmers, it became clear that potato production is a risky, high cost venture, requiring many more labor days and purchased inputs than other field crops. On average, over 150 days were required per crop cycle, with about 1/6 of these performed by women, mostly in the planting and harvesting stages. Among purchased inputs fertiliser accounted for about 1/5 of total costs, follwed by supplies/services and pesticides (both about 1/8th). The collaborating farmers used 38 different fungicides and 28 different insecticides, applying to each plot, on average, more than 7 applications with 2.46 products in each application, almost all with backpack sprayers due to the hilly terrain. Forty-three different active ingredients (a.i.) were used but three compounds dominated: the dithiocarbamate fungicide, mancozeb, made up more than 80% of all fungicide a.i. applied; the carbamate, carbofuran, and the organophosphate, methamidophos, both restricted products in the US and Canada, made up 47% and 43% of all insecticide a.i. applied respectively. Structured farm observations and interviews of the farmers revealed a number of practices likely to increase pesticide exposure: mixing pesticides with hands and a stick (36/40 farms), leaking backpack sprayers (28/40), no use of effective person protective equipment other than rubber boots (38/40), storage of pesticides in the farmhouse (19/40) and potentially unsafe pesticide disposal (35/40).
Pesticide poisonings Prior to the initiation of the project, Carchi had the highest provincial rates of reported pesticide poisonings, 17 cases per 100,000 population. Active surveillance by the health research team uncovered a rate of 171/100,000, due predominantly to occupational exposures to organophospates and carbamates (Cole et al., 1993). Occupational exposure among agricultural working age males was the most common reason for poisoning (32/50 cases). 28/33 cases reported pesticide application as the work task just prior to poisoning, with over 80% citing the use of WHO Hazard Catergory I pesticides. The suicide rate of 17.1 suicides/100,000 and overall mortality rate of 20.5/100,000 were among the highest reported. At the then current exchange rates median costs associated with these poisonings were estimated as follows: public health care direct costs of $9.85/case; private health costs of $8.33/case; and lost-time indirect costs of $8.33 /agricultural worker, all over five times the daily agricultural wage of about $1.50 at the time. The last is particularly important given the major role for labour in the potato production system and the greater need for such labour that would be involved in integrated pest management strategies.
Cross-sectional survey methods In order to assess current health effects among the farm members, the health research team started with a census of the working and adult population associated with the chosen farms (Cole et al, 1998). Over 200 persons worked, about 2/3 family members and 1/3 contract labourers, the majority of the latter being relatively stable to each farm. Workers were predominantly male (82%) and one-sixth were teenagers. Among these workers, over one-thirdwere involved in all pesticide applications and another third participated in some applications. An additional 35 women reported little current direct agricultural work. The farm population thus included those not doing direct farm work (consumers), those performing work in the fields (exposed) and those applying pesticides (applicators). The health team decided to include all applicators, half the exposed and all consumers in the sampling frame, thereby oversampling the extremes of likely exposure to achieve greater contrast within the farm population. To compare the farm population with others, less involved with agriculture, we selected controls, matched on age, sex and years of formal education from the local non-farm population through community groups and the municipal government. Control occupations included housewives, students, labourers, skilled workers, small business persons and professionals. Individual exposure measures were obtained by an interviewer administered questionnaire. All groups were asked about current household potato consumption (and the number of persons in the household to facilitate the calculation of estimated weekly intakes in kg per person) as a potential route for pesticide ingestion via the main constituent of the local diet. Piped water for the area came from sufficiently high up the mountain to likely preclude pesticide exposure via water. (Hence the pesticide leaching part of the research will not be further elaborated). A record of prior pesticide poisonings by year was made. For all groups, work exposure assessments included the numbers of times using solvents and pesticides. Among the exposed and applicator farm population, information on past pesticide use (in years) by name and current use (in hours) during the last month were obtained from the participant. Based on the use pattern reported by the agricultural research team, we focused on effects of pesticides on the skin, the peripheral nervous system (motor and sensory innervations of the arms and legs) and neurobehavioural function (cognitive, motor and sensory performance). The field physician first conducted a complete visual examination of the skin, followed by a history of physician diagnosed skin and allergic disorders. For effects on the peripheral nervous system, we constructed a five item yes/no scale referring to the legs which included: a "going to sleep" sensation, cramping pain, paresthesias, progressive weakness and flaccidity. The same field physician was trained by the team's neurologist to conduct the examinations on all participants according to a standardized protocol. We also assessed vibration threshold and neurobehavioural or cognitive/practical function, building on a battery ( Neurobehavioural Core Test Battery) developed and tested by the World Health Organization. Important co-variates which could affect health outcomes included demographic factors, medical conditions, weight for height and several others for each specific test.
Cross-sectional survey results On personal pesticide-related measures, farm groups reported more former poisonings, particularly the applicators. As expected, estimated individual potato consumption was significantly higher in the farm groups, with applicators reporting the highest mean consumption exceeding six kilograms per week. Such figures indicate clearly the role of potatoes as a staple in the region, reflecting their ready availability and responding to the caloric requirements of physical work on the farm. Among the relevant non-pesticide exposures, the controls reported more difficulties with alcohol than the farm groups but applicators had the highest scores among the farm population. These differences reflect the gender-based differences in agricultural work and alcohol consumption. Skin findings on physical examination showed differences across exposure groups. Conjunctivitis (n=9) was only found among applicators, consistent with the irritant effects of pesticides either airborne or transferred to the eyes by rubbing with the hands. Dermatitis (n=119, 48%) was most common among the exposed and applicators, in areas likely to be exposed to pesticidessuch as the hands and forearms. This is consistent with higher annual workers' compensation incidence rates for occupational skin disease in the agricultural sector in Canada and other jurisdictions (O'Malley et al, 1988). Often farm members indicated that fungicide use aggravated the dermatitis, perhaps accounting for the higher rates found in the those generally exposed during farm labour compared to direct applicators. Logistic regression results for dermatitis (present or absent) for various combinations of the exposure groups showed that the number of years using fungicides, but not current use, was consistently strong as a predictor of dermatitis for all farm groups (odds ratio = 1.12, or a 12% increase in risk for each year of use). For the exposed with a mean of 10.5 years of use, this would mean odds of having dermatitis of 2.3, important enough given its potentially disabling nature. Using polytomous logistic regression analyses, we found that applicators had significantly greater odds for more current peripheral nerve symptoms (odds ratio, OR=3.1), signs of poor coordination (OR=4.3), abnormal deep tendon reflexes (OR=2.9) and reduced power (OR=2.1) than controls. Mean toe vibration threshold scores on a logarithmic scale, were significantly higher among applicators ( = 0.035) and those reporting previous pesticide poisonings ( = 0.074). Our findings on applicators are consistent with those of New York agricultural applicators who experienced greater coordination problems during the spraying season and had higher vibration thresholds than controls for the dominant foot (Stokes et al., 1995). Among the other significant predictors, was potato consumption which may indicate residues as per those for carbofuran in Canada, the latter above maximum residue limits (Neidert et al., 1994). Potatoes may also contain naturally occurring toxic glycoalkaloids which can produce nervous system effects. As cash crops, potato contaminants could be exported to markets lying outside the ecosystem where they are produced. Pesticide contamination has been found in other components of the Quito diet (Bolaños et al, 1986) and the Canadian diet (Neidert et al., 1994) with concern about such widespread intake most document for children in the United States (National Academy of Sciences, 1993). Neurobehavioural function for the farm population was generally worse than for controls, including working teenagers. Women consumers did worse in spatial, psychomotor and motor functions, the generally exposed group did worse on spatial tests and the applicators did worse on attention tests. Men did worse on spatial tests and those with problems with alcohol demonstrated decreased attention. Potato intake still accounted forsome drop in overall neurobehavioral performance.
Role of pesticides in farm productivity and farmer health Work done in the Philippines in rice production had showen that reduced pesticide use could improve rice farmer productivity and farmer's health simultaneously (Rola and Pingali, 1993). Using more dynamic cost functions and a more epidemiologically grounded measure of farmer health impairment, the neurobehavioural score, we set up a system of simultaneous equations to test the effects of health on the efficiency of input allocation decisions and output decisions (Antle et al, 1998a). Our results showed that farmers with higher neurobehavioural function obtained lowered cost of production per hectare and thus higher productibity, consistent with better managerial capacity. Increased use of the insecticide carbofuran increased crop production but it also lowered neurobehavioural function to such an extent that the overallcrop production declined. This would be aggravated by the effective subsidies for importation of pesticides such as carbofuran by trade and exchange policies operative in Ecuador at the time of the study (Lee & Espinoza, 1998).
Integrated simulation model and analysis We extended this analysis using simulation modelling of health-output tradeoffs under current conditions across different agro-ecological zones (Antler et al, 1998b). Because of the different levels of inputs due to different climactic conditions and soil characteristics lower zones (higher inputs) had steeper trade-offs than higher zones (lower inputs). In simmulations of scenarios with greater use of integrated pest management (IPM) and farm worker self-protection practice scenarios, the tradeoff curves shift so that for any particular level of crop production, the decline in mean neurobehavioural score across the farm population as a whole, would be reduced. The prediction is that better agroecosystem management through greater cultural and biological controls and reduced chemical inputs should have a positive impact on the health of farm members and by extension, external consumers.
Directions Detailed, micro-level inter-disciplinary work, such as that we have just described, can provide crucial empirical bases for designing different agroecosystem management approaches that include the wider socio-economic environment and the more local agro-ecology and human health conditions. Conducting the research, we had to focus on the key policy issues of pesticide use, rather than consider all the potential determinants of health, and consider questions of scale explicitly. However rooted people may be in a particular agroecosystem, they also have far greater mobility than soil or climate features that environmental colleagues had to consider, or the set of farm plots worked by each collaborating farmer that agricultural economic colleagues had to measure and model. Necessarily, the matches are not truly deterministic but rather "fuzzy". Further, we had to focus on a limited time horizon, in which long term and rarer health effects such as cancer, were not truly measurable, and hence could not be included in the research. Organizationally, the International Potato Centre had far greater strengths in the documentation of agricultural production than human health researchers could easily expect to develop. However, their capacities in the environmental and health area were considerably weaker, making linkage with other researchers essential. Although inter-disciplinary research is increasingly being funded, such organizational hubs will need to become increasingly multi-disciplinary to engage in research and monitoring the range of effects that are likely to occur with agroecosystem change. Joint work benefits considerably from close sharing of theoretical, measurement and analysis perspectives and should hopefully give rise to better change strategies, which can themselves be evaluated. Areas for priority research could start with moving from farm or watershed level measures to indicators at regional levels or above for monitoring purposes, checking the extent to which such aggregation maintains validity of the relationships. Yet we should not be paralyzed in this work by the general epidemiological distaste for ecological/regional level work in contrast to individual level work. Dangers abound as much with individual level fallacies and ecological-level fallacies in trying to understand the "true" determinants of human health status. As well, further joint documentation of existing conditions agriculturally or environmentally should be expanded to include human health improvements (or deterioration) with changes to agricultural production strategies. A fine example of alternative approaches is provided by a recent volume on partnerships for sustainable agriculture (Thrupp, 1996). Yet few of thesecase studies systematically documented any concommittant changes in human health that either occurred or could be expected with alternative agricultural production strategies. Another area of research would be the removal of economic barriers or the development of economic incentives to promote more integrated rural development approaches in which social and technical aspects of human health are paid heed to(e.g. Wall, Ramsey in Smit, 1998) <PALIGN="JUSTIFY">Finally, on a more personal note, we must foster the increasing commitment of health professionals to linking current ecosystem management approaches and human health, in research, policy and practice (CPHA, 1992).
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Agroecosystem Management for Improved Human Health: Implications for International Development The following papers were presented at a panel discussion of the Annual Meeting of the Canadian Society of Animal Science, July 5-8, 1998, Vancouver, British Columbia, Canada. The papers were published in the conference proceedings, New Directions in Animal Production Systems, edited by R. Blair, R. Rajamahendran, L.S. Stephens, M.Y. Yang.

Document(s) 3 of 5
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