Ecological associations between asthma prevalence and potential exposure to farming

The prevalence of asthma has increased dramatically since the 1980s. In the USA, during the period 1980–1996, the prevalence of self-reported asthma increased by 75% overall and 74% among children aged 5–14 yrs 1. In 2001, the prevalence of physician-diagnosed asthma among children (0–17 yrs) and adults (≥18 yrs) was 8.7% and 6.9%, respectively 2.

The mounting problem of asthma in developed countries worldwide has sparked a variety of clinical and epidemiological research regarding the aetiology and exacerbation of the disease. One focus of recent aetiological research has been the effect of environmental factors on the development and behaviour of the immune system in children. These studies have examined the “hygiene hypothesis” of immunological development, which, in its simplest form, asserts that the developing immune system must be confronted with microbial material in order to function appropriately. Otherwise, the immune system “turns on” mechanisms that create an over-reaction to exposures, resulting in allergy and asthma. Support for the hygiene hypothesis has been found in European, Australian, New Zealand and Canadian studies of farm children, who appear to have asthma less frequently than children who have not grown up on farms 3–10. The specific farm exposures responsible for this apparent protective effect have not been identified, but it is thought that exposure to endotoxin from livestock and poultry may be a contributing factor in the reduced asthma prevalence among farm children.

An ecological study was conducted using existing data to examine the overall relationship between asthma prevalence and farming exposures in North Carolina, USA. The study sought to determine whether there might be a basis for further research to evaluate the relationship of farming and asthma inNorth Carolina, where there are a variety of farm types and sizes.

Subjects and methods

Estimates of asthma prevalence among 7th and 8th grade children (aged 12–14 yrs) were obtained from the North Carolina School Asthma Survey (NCSAS), 1999–2000, designed and conducted by the North Carolina Dept of Health and Human Services and the University of North Carolina School of Public Health, NC, USA 11. The survey was adapted from the International Survey of Asthma and Allergies in Childhood (ISAAC) written and video questionnaires, and assessed current symptoms of wheezing and cough, as well as self-reported, physician-diagnosed asthma 12. Responses to these items estimated the prevalence of physician-diagnosed asthma and wheezing with and without physician diagnosis.

The survey response rate was 66.8% (128,568 out of 192,248) for 7th and 8th grade children enrolled in public school during 1999–2000. Response rates by school were 88% (499 out of 565) and 99 out of 100 counties. One county hadunusable data due to a broken video tape, leaving the data from 98 out of 100 counties for analyses. Demographic information obtained from the statistical branch of the North Carolina Dept of Public Instruction was used to compare participants with nonparticipants. There were no significant differences in socioeconomic status (enrolment in the free school lunch programme), race, or sex among children who participated and those who did not 12.

County-specific data about agriculture, including numbers of livestock and poultry, and acres of crops, were obtained from the Agricultural Statistics Division of the North Carolina Dept of Agriculture and Consumer Services 13. Statistics on cattle were reported from January 1, 2002, and statistics on hogs, pig, poultry, and crops were reported from December 1, 2001. Counties did not report livestock or poultry if their numbers did not meet the minimum for census; these included <1,000 hogs or pigs, <200 beef or milk cattle and <500,000 broilers (chickens raised for meat). Counties did not report crops if they did not harvest >200 acres.

Data regarding the number of farms and total acreage ofeach county were obtained from the 1997 Census of Agriculture 13. These statistics are compiled and published by the U.S. Dept of Commerce every 5 yrs. Population estimates and descriptions of county populations were obtained from the U.S. Census Bureau 14.

Results

The mean, median, range and IQR of county-specific asthma prevalence and farm exposures are shown in table 1⇓.

The number of farms, acreage of hay and numbers of beef and milk cattle were all associated with modest but statistically significant decreases in asthma prevalence (table 2⇓). The largest decreases in asthma prevalence were associated with increasing numbers of beef cattle (−7.76% per IQR increment), acres of hay (−7.24% per IQR increment) and numbers of farms (−5.02% per IQR increment). Smaller, but still statistically significant, negative associations were observed for dairy cattle and broilers, whereas the associations with hogs and pigs and acres of wheat were negligible (table 2⇓).

A similar pattern of results was observed for wheezing without a diagnosis of asthma (table 3⇓), although the associations were generally weaker. The results were unchanged when counties with the lowest prevalence (4%) and with <50 participants (n=2) were excluded from the analysis. Omitting the adjustments for parental smoking, socioeconomic status, race and sex did not materially change the estimates, nor did the use of alternative indicators of socioeconomic status, including county mean income and education.

Discussion

This study suggests that certain farm exposures may be associated with lower frequency of asthma in school children. County-specific ecological measures were used to examine the relationship between asthma prevalence in school children and farm exposures in North Carolina, and it was found that statistically significant decreases in asthma prevalence were associated with hay acreage, number of farms, and numbers of beef and dairy cattle. The prevalence of asthma was not significantly associated with wheat acreage or the numbers of pigs and hogs.

These ecological findings are consistent with the hypothesis that some exposures related to farming are protective against childhood asthma. Hypotheses that farming might have protective effects focus on conditions that result in a richer microbial environment, including larger families, exposure to livestock (particularly cattle), and exposure to higher levels of endotoxin, a cell wall component of Gram-negative bacteria 15.

The focus has turned to endotoxin as a protective factor because of its potential to suppress the innate immune responses involved in immunoglobulin E-mediated allergy 15. Endotoxin is ubiquitous in the environment, but levels tend to be high in environments where there are farm animals, such as cows, horses, and pigs 3, and during wheat harvest 17.

As in any ecological study, the finding of an association at the population level does not necessarily imply that the same relationship exists among individuals. Individual-level confounding is particularly difficult to control and may have affected the results, despite adjustments for ecological indicators of smoking, ethnicity and socioeconomic level. Interpretation of the findings for hogs and pigs was complicated by the observation that intensive hog operations are concentrated in areas with high proportions of poor, non-White residents 18. Therefore, race and poverty may be causes of exposure, as well as potential confounders.

Despite the well-known limitations of ecological studies, this study is, nevertheless, useful as a cost-effective initial examination of the overall relationship between asthma and exposures to farming in the USA 19. The few studies examining these relationships in the USA have resulted in equivocal findings. One study measured asthma prevalence in two counties in Iowa, where the predominant land use is farming 20. The potential protective effect of farming was observed in only one of the study counties, and asthma prevalence was similar to that found in large mid-western cities. The authors suggested that there might be little difference in environmental exposures between farm and non-farm residents, since agricultural exposures are ubiquitous in Iowa. A case-control study nested within the Children's Health Study in southern California examined the relationships between asthma and a variety of environmental exposures, and found that children who had ever been exposed to farm animals or crops and crop dust had an increased risk of asthma compared with children who had never had those exposures 21.

The current findings of associations between reduced asthma prevalence among adolescents and indicators of exposure to farming in North Carolina, USA, provide a stimulus for further study with measurement of exposure atthe individual level to investigate exposures that may be protective against the development of asthma.