Can Farm Animals Protect Children From Diseases
The effects of farming and nascency club on asthma and allergies
, I. Bibakis , 5. Bibaki-Liakou , A. Pedioti , I. Dimitroulis , J. Harris , A. J. Newman Taylor , P. Cullinan
European Respiratory Journal 2006 28: 82-88; DOI: 10.1183/09031936.06.00021305
Abstract
A farm babyhood is apparently protective in allergic disease, but studies of this effect in Europe have been confined to particular types of farming practice. This written report addressed whether or not this event was generalisable.
A cross-sectional survey of 800 schoolchildren living in rural Crete was undertaken. Standard questions relating to allergic disease were included and atopy was measured through skin-prick tests involving 10 local aeroallergens.
The prevalence of atopy was 24%, but associated symptoms were far less mutual. At all ages, children from farming families had more frequent contact with farm animals (mainly goats), but were no less likely to be atopic. Atopy and seasonal rhinitis were significantly and independently more common among first-born children.
This community has an intermediate prevalence of atopy but a very low frequency of allergic disease; farming does not seem to be an important determinant, maybe because information technology is of the wrong sort. Thus farming effects may be specific to local practices. First-born children in this community as well announced to be at increased risk of allergic disease.
- Allergic illness
- atopy
- birth order
- farming
- Greece
Babyhood asthma and allergic disease are distributed unevenly beyond Europe, with a decreasing prevalence from north to southward and from west to east 1. The reasons for this variation are unclear but are often, if loosely, attributed to westernisation, in itself perhaps a reflection of lower rates of microbial contact in early babyhood, leading to inappropriate regulation of a developing immune organisation. In keeping with this, several studies take reported that European children brought up against a farming groundwork have lower risks of atopy and some associated allergic diseases, specially hay fever 2, 3. Also widely reported is the observation that children from small sibships show increased risk of such allergies, a miracle consequent with a protective outcome of early infection 4.
For the most role, studies that take examined farming take involved children living in communities in which cows are kept, often in close proximity to the family unit dwelling house. Farming on Crete, an Eastern Mediterranean island, is very unlike from that in Key and Northern Europe. Cows are absent from the island, and, where livestock are kept, they are invariably goats or sheep, put out to graze on afar mountain slopes; animals are not kept in barns. Arable farming is of olives, vegetables or citrus fruits. For the near part, farmers live in villages some distance from their state. The stardom between farmers and their nonfarming neighbours is not always articulate and villagers who practise not consider themselves chiefly to exist farmers frequently take a small plot of land and often keep a few animals. In improver, many rural families proceed 1 or two goats in their courtyard at home, ofttimes accompanied by chickens or caged rabbits. Pet dogs and cats live outside.
In an earlier survey, it was reported that the prevalence of childhood atopy in a rural Cretan community was half that in Iráklion, the capital city 5. Amongst rural children, however, at that place was no relationship between atopy and parental farming. In order to investigate this farther, a second, more than detailed cantankerous-sectional survey was designed in order to include children living in a multifariousness of rural settings on the island. In improver to atopy, the rural distribution of allergic symptoms consequent with asthma or hay fever was examined.
METHODS
In 2001, all schoolchildren anile vii–xviii yrs and living in four previously unsurveyed areas of rural Crete were invited to take part in a report of the relationships between atopy or associated diseases and a farm upbringing. Ethical approving was obtained from The Scientific Commission at the Venezalion Infirmary (Iráklion, Crete) and the Ideals Committee at Purple Brompton and Harefield NHS Trust (London, Uk). All parents gave written informed consent.
Parents were asked to complete a questionnaire that elicited information about the respiratory wellness of their participating children, any siblings and the child's parents. Where possible, questions were translated directly from the International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire 6. Information was requested near levels of parental educational activity and occupation, and about their children's exposure to and contact with farm animals or pets and consumption of farm milk at three different stages of life: infancy, at 5 yrs of age, and during the past twelvemonth.
Each child was invited to undergo skin-prick tests, in accordance with the ISAAC protocol, involving a series of 10 common aeroallergens: grass pollen (Mediterranean mix), Parietaria, olive blossom, true cat fur, Dermatophagoides pteronyssinus and D. farinae, goat epithelium, Cladosporium, cockroach, and poultry, all purchased from ALK Abelló (Hungerford, UK). The negative and positive controls were saline and histamine respectively. A skin-prick examination issue was considered positive if it produced a hateful weal bore of ≥3 mm greater than that produced past the saline control.
Statistical assay
Consummate data were available for 797 children, 93% of those eligible. Children were categorised equally atopic if they gave ane or more positive immediate skin-prick test results. In gild to permit comparison with the before survey in Crete, a further category (standard atopy), defined by the presence of one or more than positive test results to any of the three pollens, either dust mite or true cat fur, was formed. Children were considered to endure from current seasonal rhinitis when they were reported to take had a runny or blocked nose (while not having a cold or influenza) over the past year during the months of March to September. Parents were divers as full-time farmers if either was a full-fourth dimension farmer; part-time farming indicated that either parent was a part-time farmer just neither was involved full-time. Only when neither the begetter nor the mother was involved in any kind of farming was the child considered to come from a nonfarming family unit.
All information was entered on to a computer database, and analyses were performed subsequently data checking and cleaning. The Pearson Chi-squared test was used to exam for associations betwixt categorical variables, and the medians of continuous variables were compared between groups by ways of the Kruskal–Wallis or Mann–Whitney test. Where appropriate, Cuzick's tendency examination was used for ordered exposure variables.
Explanatory variables associated with the outcome of interest (p<0.15) were included in multivariate logistic regression models and adjusted for those factors that either were significantly associated with atopy or confounded the clan between atopy and the principal exposure of involvement. Effect modification was assessed betwixt the variables retained in the final models.
RESULTS
Comparisons between farming and nonfarming households
A minority (14%) of the children were currently living in a nonfarming home; equal proportions of the rest were from full- or office-time farming families (table ane⇓). Most all (95%) current total-time farmers, but only 30% of part-time farmers and viii% of electric current nonfarmers reported that farming was their primary occupation at the fourth dimension their child was built-in.
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The distributions of age and sex of the surveyed children did not differ across the iii levels of farming. Levels of parental educational activity, conversely, varied systematically, with mothers and fathers who farmed having completed fewer years of schooling than other parents (p<0.005 for both). Children from nonfarming households tended to be from smaller families and were more oftentimes the first-built-in. These differences were significant. Reported asthma is rare in this community but was more common in the siblings of those children whose parents were farmers. This divergence was not apparent for seasonal rhinitis, reported past 5.9% of the full population. Parents who were current full-time farmers almost always reported that their primary occupation at the time of their child's nativity was farming. Children from farming homes, either total- or part-fourth dimension, were more probable to have electric current contact with sheep or goats and live in a home where these animals were kept in close proximity. This was also the case during infancy, at age 5 yrs (information not shown) and for all species of farm animals (goats, sheep, chickens, pigs and rabbits; data shown just for goats/sheep). Of children who currently lived in a abode where goats or sheep were kept in the courtyard, 53% were reported to have daily contact with the animals, 35% weekly contact and 13% no contact. During infancy, these proportions were reversed: 24, 18 and 58%, respectively.
Atopy, allergic disease and farming
Of the children, 24% were atopic; 19% showed standard atopy (tabular array 1⇑). These frequencies were the same in each of the four report areas. Atopic children were almost often sensitised to D. pteronyssinus (12% of all children) or cockroach (10%); prevalences of positive tests to D. farinae, any pollen or true cat fur were iii–half-dozen%. Of the children, <i% tested positive to whatsoever of the remaining allergens. Symptoms of allergic diseases were far less common than atopy. Simply 10 (1%) children were both atopic and wheezy over the by twelvemonth, and just fifteen (ii%) had seasonal rhinitis and a positive peel-prick examination outcome for i of the iii pollens.
None of these outcomes were obviously related to habitation in a farming home. When separate allergens were examined, the prevalence of cat fur sensitisation was almost three times higher amongst nonfarming children (ix versus 4 and 3% for full- and part-time farming children, respectively; ptrend = 0.06). Only children from full-fourth dimension farming families were sensitised to Cladosporium (2%). Furthermore, neither atopy nor current wheeze was associated with the frequency of consumption of home-produced milk, boiled or otherwise, during whatever stage of the child'due south upbringing (data non shown).
Children with regular animal contact, at whatever phase of life, were equally likely to exist atopic or have current wheeze than children with less frequent or no contact (table two⇓). Conversely, children who currently lived in homes where sheep or goats were kept nearby were less likely to be atopic (p = 0.01), although they had an equal prevalence of current wheeze. Children who lived in a home where goats or sheep were kept in the courtyard during either of the two earlier periods of life were also less often atopic, although these associations could easily accept arisen by chance.
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Nascency order
Of the children, 42% were the first-built-in (table 3⇓). They were older, albeit not greatly so, than other children only no more likely to be male person. Unsurprisingly, mothers and fathers of first-born children were younger at the time of their child's birth. Mothers with three or more children had received significantly fewer years of education (ptrend = 0.02). Reported parental asthma and allergies showed no clan with birth order.
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Atopy was more prevalent (ptendency = 0.01) amongst the offset-born children, but in that location were no differences at college birth orders. Similar results were observed for standard atopy (ptendency = 0.02). Of the remaining outcomes, only seasonal rhinitis (ptrend = 0.07) and seasonal rhinitis accompanied by a positive skin-prick examination result for pollen were associated with birth order (ptrend = 0.01).
Logistic regression analysis of the nativity order association indicated 3 independent determinants of atopy: male sex (odds ratio (OR) 2.3, 95% confidence interval (CI) one.half-dozen–three.two; p<0.0005), historic period (OR i.06, 95% CI one.0–1.13·yr-1; p = 0.07) and offset-born birth order (OR 1.68, 95% CI 1.two–two.4; p = 0.003).
Give-and-take
Childhood atopy, every bit measured by response to pare-prick testing, is not uncommon in this rural Cretan community. Symptoms consequent with associated allergic disease, conversely, are rarely reported. Despite clear differences in their contact with farm animals at all ages, no consistent differences in the rates of atopy and allergic disease were institute between those children whose parents were or were non farmers. Children who alive in houses where goats or sheep are kept adjacent to the domicile were significantly less often atopic (only not wheezy); given the big number of statistical tests carried out, this finding may have occurred by chance. Atopy was more common among first-born children, an association independent of the other variables measured.
Several explanations were considered for the apparent lack of a protective effect of a farm upbringing in this population. First is the possibility that a rural childhood in Crete is such that every child receives sufficient exposure to the protective gene(due south), and that, in this setting, a categorisation by parental farming status is insufficiently discriminatory. Table 4⇓ summarises seven earlier farming studies in which childhood atopy was assessed through utilise of pare-prick tests forth with the present findings, using comparable age groupings where possible. Amid children aged vii–8 yrs, the prevalence of atopy in the children of Cretan farmers was far college than that among farming children in Austria 7 but not dissimilar to estimates amidst farming children living in Sweden, Australia or Finland 8, 11, 12. Conversely, the prevalence of atopy among children of nonfarmers in Crete is consistently lower than that amidst similar children living in any of the other communities studied. Responses to the present questionnaire suggest that children of farming parents in Crete received systematically greater exposure to all farm animals at every stage of life, but, dissimilar in other studies 9–12, no systematic prove of whatever association between animal contact and the frequency of atopy could be found. Thus, the present authors think it improbable that there is a universal protective gene in this rural population.
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A 2d explanation lies in the design of the nowadays survey. Although primary education is essentially universal on Crete, an estimated 5% of rural children leave school at the age of 12 yrs. Many of these have work in farming, ofttimes equally goatherds. No differences were establish betwixt farm and nonfarm children aged <12 yrs, but it is believable that there is a small population of older children, missed through the present method of recruitment, who have both an intense subcontract exposure and a low prevalence of atopy.
A third, and perhaps most plausible, explanation is that farming of this type is indeed not protective. To date, all reports of a low prevalence of allergic respiratory disease in farm children accept been in communities in which cows (primarily) are kept and, for role of the year at least, housed in barns close to the family habitation. In these communities, the consumption of dwelling house-produced milk, often unpasteurised, is mutual. On Crete, in dissimilarity, no cows are farmed and animals are kept outdoors throughout almost the unabridged twelvemonth; moreover, caprine animal's milk is universally boiled before it is drunk, beingness otherwise considered unpalatable. Thus, a childhood farm exposure there is probably dissimilar both qualitatively and quantitatively. If this is the case, then information technology may provide important clues equally to the specificity of the protective farm effect observed elsewhere. Following the ecological observation that a protection confronting atopy in Australian children of farmers is confined to those living in a region in which livestock are ordinarily kept, Downs et al. 11 suggested that regional differences (perhaps in climate or soil type) may be relevant, or that nonanimal (in that example, cows or sheep) farms do non confer protection.
Although a high prevalence of atopy was constitute, the present findings suggest that electric current symptomatic allergic disease, atopic asthma or hay fever, is uncommon in this community, although the frequency of "ever wheeze" was high. Since the present assessment of clinical disease was based on parental responses to a cocky-completed questionnaire, some circumspection should be exercised in the interpretation of these observations. There are, with little incertitude, important cultural and linguistic influences that decide symptom reporting and it may exist that these are, at to the lowest degree in part, responsible for the apparently depression prevalence of disease in Crete. The English language word wheeze, for instance, has simply an approximate equivalent in Greek. However, a similar dissociation betwixt atopy and allergic disease has been observed elsewhere in Due south-East Europe 14 and farther afield 15; information technology may stand for a transitional phase between populations with depression frequencies of atopy and disease and those with high frequencies of both, such as in Northward-West Europe. In turn, these may reverberate gradations in important causative or protective environmental exposures. The present authors suggest that the high frequency of "e'er wheeze" reflects the probable high incidence of early respiratory infection, a design mutual amid rural communities in many parts of the world.
Children in the present population who were first-built-in showed significantly increased rates of atopy and seasonal rhinitis, an association that was independent of the other factors examined. No differences were observed between children of lower nativity orders. Similar observations have oft been fabricated previously, only, for the about part, in communities with high overall frequencies of childhood allergic disease. If it is argued that the lack of a farming issue in rural Crete is due to every kid receiving sufficient exposure to a putative protective and probably microbial factor, then an additional explanation is required for the observed birth society effect. There is now increasing evidence that it may be determined earlier birth and perhaps reflect pregnancy-related changes in maternal immunity 16–xviii.
In several simply not all respects, the observations reported here confirm those fabricated in an earlier study 5, in which parental farming did not explain apparently lower rates of atopy among children living in rural Crete than those living in the capital letter city. One important departure is that the prevalence of rural atopy in the present written report is approximately twice that measured iii yrs previously in a different, but not distant, part of the island. The rate reported here was unvarying over 4 dissever districts, which suggests that it is a valid estimate for the rest of the isle. It is possible that the original study area had a peculiarly low prevalence of atopy, in which case farther study there would be valuable. Alternatively, there has been a sharp increase in the frequency of atopy among children in rural Crete. Although the interval for this seems implausibly short, a similar increase over a similar period was observed amid children living in Leipzig, Germany xix. At that place, the rise was attributed tentatively to (unidentified) changes consistent on the reunification of Germany; no such major events take been credible in Crete.
Acknowledgments
The current authors are very grateful to the families and schools who took office in the present survey; and to the fieldworkers from Iráklion (Hellenic republic) and London (UK) who made the study possible.
- Received February 24, 2005.
- Accepted Feb 2, 2006.
- © ERS Journals Ltd
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