Epidemiology of Hay Fever: Towards A Community Diagnosis: Review
Epidemiology of Hay Fever: Towards A Community Diagnosis: Review
REVIEW
Introduction                                                              contact all children with the same birth dates who were
Symptoms of rhinitis (sneezing, running and blocking of                   resident in Britain during 1965, 1969, 1974, 1981 and
the nose) occur occasionally in all individuals. However,                  1991 (at ages 7, 11, 16, 23 and 33 years). The following
the seasonality of allergic rhinitis induced by grass and                 question was asked in interviews with participants at age
tree pollens is characteristic and much of our under-                     23 years (in 1981): have you suffered from hay fever in
standing of the epidemiology of allergic rhinitis relies                  the last 12 months?
upon self-reported or doctor-diagnosed 'hay fever'.                          A range of potential explanatory variables were col-
Much less is known about the prevalence or distribution                   lated from the information collected by midwives at birth
of perennial allergic rhinitis and non-allergic rhinitis [1].             and by interviewers at each of the four follow-ups.
Since exposure to airborne pollen is almost universal in                  Paternal occupation at the birth of the index child was
countries such as Britain, the distribution and determi-                  classified according to the Registrar-General's social
nants of hay fever (other than its seasonal pattern) may                  classes used in 1951 [10]. The child's own current or
provide an insight into the epidemiology of atopy in                      last occupation at age 23 years was classified by the 1981
general.                                                                  social classes [11]. The classes used were I (professional
                                                                          and managerial), II (intermediate), IIIN (skilled non-
   This paper explores the association of geographical,                   manual), HIM (skilled manual), IV (semi-skilled) and V
social and family factors with hay fever as reported by a                 (unskilled). The numbers of older and younger children
national sample of young British adults who had been                      in the household were determined at the 1969 follow-up,
followed from birth. The findings are presented in                        when most families could be assumed to be complete.
greater detail than in earlier reports [2-4] and are                      Older children of the family who were currently living
discussed in the context of historical and geographical                   away from home, but aged under 21 years, were included
variations in hay fever prevalence. These epidemiological                 in the total.
observations ('community presentation') will be used to
construct a working hypothesis ('community diagnosis')                       Areas of residence at birth and at age 23 years were
to explain why hay fever apparently emerged as a post                     each classified by the region and degree of urbanization.
industrial revolution epidemic [5] and continues to                       The local authority areas of birth were classified as
increase in prevalence in modern Britain [6,7]. The                       conurbations, county boroughs (outside conurbations)
implications for future trends in prevalence ('community                  or administrative counties (predominantly urban or
prognosis') will be discussed.                                            rural as indicated by their population density at the
                                                                          1961 census). The counties of residence in 1981 were
                                                                          classified as conurbations (Greater London and metro-
Methods                                                                   politan counties) or non-metropolitan counties.
All births in England, Scotland and Wales during 1 week                      Additional factors which were considered in the
in March 1958 formed the target sample for a perinatal                    analysis were self-reported cigarette smoking (at age 23
morbidity and mortality survey [8]. The National Child                    years); parental reports of housing tenure (at age 7
Development Study [9] has attempted to trace and                          years), shared use of kitchen, bath or toilet with another
                                                                          household (at age 7 years), housing density (persons per
                                                                          room at age 11 years), and mode of infant feeding
                                                                          (reported at the 7-year follow-up); and the following
Correspondence: Dr D. P. Strachan, Department of Public Health            features of the birth record: sex, birthweight, maternal
Sciences, St George's Hospital Medical School, Cranmer Terrace,
London SW17 ORE, UK.                                                      age, parity and smoking during pregnancy.
Based on an invited contribution to a plenary session at the meeting of
                                                                             Statistical analysis was performed using SAS [12].
the British Society of Allergy and Clinical Immunology, City              Multiple logistic regression models were fitted by the
University, London, UK, 7 September 1994.                                 method of maximum likelihood using the PLR program
296
                                                                                                    Epidemiology of hay fever      297
Table 1. Prevalence (%) of hay fever in the past year at 23, by area of residence at 23
in BMDP [13]. These analyses were restricted to 9356                   3009); urban counties (15-6%, 476/3059); county
(76%) of the 12 355 respondents at age 23 years, who                   boroughs (16-1%, 392/2429); and conurbations other
had full information on all variables included in the                  than London (14-7%, 272/1847); but was substantially
models.                                                                higher among those bom in Greater London (22-5%, 358/
                                                                       1589). The London excess was mainly attributable to the
                                                                       northwest to south-east gradient regional gradient by area
Results
                                                                       of birth [3].
                                                                          Of the responders at age 23 years, 2919 (25%) had
Geographical variation                                                 moved from their region of birth. When adjusted by
Among 12355 cohort members interviewed at age 23,                      multiple logistic regression for region of birth and region
2036 (16-5%) reported hay fever in the past year. The                  of residence at 23, migrants as a group had a high
prevalence varied substantially across the regions of                  prevalence of hay fever at 23 (odds ratio 1-22, 95%
Britain, being higher in the south and lower in the north              confidence interval 1-10-1-35, P < 0-001). After
(Table 1). Comparisons within regions between the major                adjustment for this general migrant effect, and the risk
conurbations and surrounding non-metropolitan counties                 associated with the region of birth, the risk associated with
did not reveal any consistent urban-rural variation (Table             the region of residence at 23 had a small independent effect
1). When analysed by area of birth, the prevalence differed            which was of borderline statistical significance
little among those born in rural counties (16-2%, 486/                 (0-05 < i ' < 0-10). In contrast, the influence of region of
Table 2. Prevalence (%) of hay fever in the past year at 23, by father's social class and number of children in the household
 'Includes members of the family under 21 living away from home in 1969.
298       D. P. Strachan
Table 3. Prevalence (%) of hay fever in the past year at 23, by numbers of older and younger children in the household at age 11
'Includes members ofthe family under 21 living away from home in 1969.
birth was strong and independent of both region at 23 and              Although tests of heterogeneity are presented in Table
the general migrant effect (P < 0001).                              4, much of the variation in hay fever by paternal social
                                                                    class and numbers of older and younger children was
                                                                    attributable to linear trends in risk, each of which were
Family circumstances
                                                                    highly significant (P < 0 001). The gradients by numbers
Table 2 shows the relationship between hay fever at age             of older and younger children in the household were
23, household size at age 11 and paternal social class at           significantly different from each other (P < 0 001). The
birth. The prevalence of hay fever declined with increas-           effect of maternal age was of lesser significance
ing family size and was lower among the offspring of                {P < 0 05).
unskilled and semi-skilled manual workers (IV & V) than
those of skilled workers (III) or professional, managerial
and intermediate groups (I & II). These effects were                Factors not associated with hay fever at 23 years
independent of each other, with a 25-fold variation in              Other factors were assessed by adding them individually
prevalence across the cells of the Table.                           to the core model in Table 4. The following variables did
   Table 3 shows the joint effects of older and younger             not make a significant independent contribution to the
children upon the prevalence of hay fever at age 23                 risk of hay fever at 23: male sex (adjusted odds ratio 1 04,
among the index children. Both exerted an independent               95% confidence interval (0-93-1-17), birthweight less
effect, but the number of older children appeared to be             than 2500g (1-02, 0-76-1-36), maternal smoking during
the more influential variable.                                      pregnancy (0-91, 0-79-1-03), birth in a conurbation or
                                                                    county borough (1-02, 0-91-1-15), household crowding
                                                                    (more than one person per room) at age 11 (101, 0-73-
Independent risk factors                                            1-38).
Table 4 shows the variables which made a significant                   Maternal parity and number of older children in the
{P < 0 05) independent contribution to the risk of hay              household at age 11 were highly correlated and their
fever. This 'core' model was based upon 9356 subjects               independent effects could not be estimated with preci-
with complete data, 1548 (16 5%) of whom had hay                    sion. However, the number of older children in the
fever. Holding other factors constant, hay fever at 23 was          household appeared to be the more influential variable.
more common among breastfed children of younger,
professional parents, born in the southeast, brought up
in small households living in owner-occupied housing                Discussion
with sole use of kitchen, bath and toilet. Regular cigar-
ette smokers at 23 reported less hay fever than non-                The rising prevalence of hay fever
smokers; subsidiary analyses showed a similar prevalence            Anecdotal evidence suggests that hay fever was extremely
in never smokers and ex-smokers at age 23.                          rare in Britain before the industrial revolution, and
                                                                                         Epidemiology of hay fever      299
emerged as a complaint of the urban educated classes in         and levels of allergen-specific IgE among Japanese
the 19th century [5]. A large population survey in              school children [21]. The exception to this general rule
Switzerland in 1926 found only 0-28% of 77000 respon-           seems to be in Australia, where there was no appreciable
dents to be suffering from hay fever [14]. At that time, the    change in the prevalence of self-reported hay fever from
prevalence in urban areas was 10 times higher than in           1977-1978 to 1989-1990 [22] nor in the degree of skin-
rural areas (1-2% vs 0-13%). A similar survey carried out       prick positivity among adults over a similar period [23].
in 1985 found a much higher prevalence (10-0%) and
little evidence of urban-rural variation (8-0% vs 10-5%).
                                                                Geographical variations
    The substantial increase in prevalence in Switzerland
parallels that described in serial surveys of American          Estimates of the prevalence of hay fever in different
college students [15], Swedish army recruits [16] and           countries vary widely, from 0-5% to 28% for children
British teenagers [6,7], which suggest a long-standing          and from 0-5% to 15% for adults [24]. Much of this
and continuing rise in hay fever prevalence. There is           variation may be attributable to the methods of sample
also evidence of a rise in the prevalence of eczema in          selection and case definition, but there is also evidence of
Britain [6,7,17] and Denmark [18]; skin-prick reactions         real differences, notably between former east and west
to common aeroallergens in Britain [19] and USA [20];           Germany [25]. Regional differences are also apparent
300     D. P. Strachan
 within Australia [22], perhaps related to a higher aero-      groups was evaluated in a study of adults in south
 allergen burden in drier inland districts.                    London [32] which found little difference in the preva-
    The marked geographical variation in the prevalence        lence of symptoms or skin-prick reactions by social class,
 of hay fever in the British 1958 cohort appears to relate     but a greater use of the hay fever label by doctors among
 more closely to region of birth than region of residence at   patients from more privileged social classes.
 23. This may reflect the distribution of the atopic              The socioeconomic gradient in self-reported hay fever
 genotype, or variations in lifestyle or environmental         in the British 1958 cohort parallels that seen for eczema
 exposures (including aeroallergens) in early life. A          as reported by parents and examined by school medical
 study of the birthplace of the parents of children with       officers at ages 7, 11 and 16 [4], and for skin-prick
 and without hay fever would help to distinguish between       positivity to common aeroallergens measured at age
 these alternative explanations.                               34-35 [Strachan DP, unpublished observations]. This
    Studies of urban-rural variation within countries are      suggests that it is unlikely to be a reporting artifact and
 inconsistent. In Tecumseh, USA, probable allergic             probably reflects an association of aflluence with the
 rhinitis was found three times more commonly in city          underlying atopic tendency. Socioeconomic variations
 residents than in the surrounding rural areas (75% vs         in sensitization to common aeroallergens in two large
 25%) [26], whereas in Switzerland no urban-rural              American surveys [33,34] are consistent with this
 variation was evident in recent surveys [14]. The 1958        interpretation.
 cohort were born at a time when all cities and most major
 towns in Britain experienced winter pollution by coal
 smoke and sulphur dioxide at levels comparable to those       Family structure
 in east German cities in the mid-1980s [27]. The absence       The strongest association which emerged in this analysis
 of substantial urban-rural variation in hay fever pre-         was between hay fever and the number of older children
valence in this large cohort and the low prevalence of hay      in the household. This appeared to be largely independent
fever and allergic sensitization in previously highly           of maternal age and parity, suggesting that postnatal
polluted east German cities [25] are evidence against           influences were more important than the intrauterine
the hypothesis that irritant air pollution resulting from       environment. This would be consistent with the weaker,
industrialization was a major influence in the emergence        but independent, trend by numbers of younger children
of hay fever as a 'post industrial revolution epidemic' in     in the household.
Britain and elsewhere [28].                                        A similar pattern of decreasing prevalence of hay fever
   There has been concern that the continuing rise in          with increasing numbers of older siblings was found in a
prevalence of allergic disease in recent decades may have      later British birth cohort born in 1970. When studied at
been due to increased exposure to vehicle-related pollu-       the age of 5 years, 6-0% of the flrstborn children suffered
tants such as nitrogen dioxide, ozone and diesel particu-      from hay fever compared with 1-3% of children with
lates [29]. Two studies have suggested a higher                four or more older siblings [35]. In a recent survey of over
prevalence of nasal allergy in areas with high traflic          18000 teenage school children in SheflSeld, the preva-
density [30,31]. In modern Britain, ozone levels are           lence declined from 18-4% among flrstborns to 11-8%
generally higher in urban areas, whereas nitrogen              among children with three or more older siblings
oxides and diesel particulates are urban pollutants. The       [Strachan DP, unpublished observations]. Total family
lack of urban-rural variation in the prevalence of hay         size is inversely related to the prevalence of skin-
fever may thus conceal subtle but counterbalancing             prick positivity among German children [36], but this
influences of different air pollutants. Nevertheless, it is    study did not distinguish between older and younger
clear that exposure to outdoor air pollution cannot            siblings.
account for the major epidemiological features of hay             Within the 1958 cohort, the influence of older siblings
fever which emerge from comparisons within popula-             is apparent for hay fever or allergic rhinitis ascertained
tions, by socioeconomic status and family structure.           by parental interview at age 11, and for eczematous
                                                               rashes occurring in the first year of life [2]. Skin-prick
Socioeconomic variations                                       tests performed on a sub-sample of the cohort at age
                                                               34-35 show a strong, graded and statistically significant
Hay fever has been recognized as a complaint of the            inverse association between number of older siblings and
wealthier classes since the 19th century [5], and several      the prevalence of positive reactions to each of three
studies suggest that this pattern persists in developed        common aeroallergens (mixed grass pollen, house
countries [22,26]. The possibility of differential reporting   dust mite and cat fur) [37]. These observations
and labelling of nasal symptoms in different social            effectively exclude reporting artifacts and suggest
                                                                                         Epidemiology of hay fever         301
that the relationship between hay fever and house-              of its risk factors are shared by infant eczema and skin-
hold size reflects the distribution of atopy in general,        prick positivity to common aeroallergens, suggesting
rather than organ-specific effects on the nasal                 that epidemiological variations in each of these three
mucosa.                                                         outcomes reflect the underlying distribution of atopy.
                                                                The strongest risk factor to emerge is position in the
                                                                household as a child. The apparent protective influence
Infant feeding                                                  of older siblings emerges within a few months of birth
There has been considerable interest in the possibility         (infant eczema) and persists at least to age 35 (skin-prick
that infant feeding may modulate the development of             responses). This may be seen as an example of biological
allergy, in particular that breastfeeding may have a            'programming' [41].
protective effect [38]. This debate emerged some years             The precise nature of the programming influence
after the 1958 cohort were born, so it is unlikely that their   remains uncertain. A working hypothesis is that allergic
mothers had selectively altered their feeding practice          sensitization can be prevented by infections acquired
because of a family history of allergy. As in a later           during early childhood [2]. Evidence is emerging from
national cohort studied at 5 years of age [35], breastfeed-     in vitro studies that bacterial or viral infections may
ing was actually associated (albeit weakly) with a higher       stimulate the development of TH-1 lymphocytes and
prevalence of hay fever. However, these findings from           thus prevent the proliferation of TH-2 cell populations
general population samples do not exclude a possible            [42]. Early childhood infections are commonly trans-
protective influence of prolonged exclusive breastfeeding       mitted by household contact, particularly with older
in a small subgroup of infants at particularly high risk of     siblings attending schools and playgroups, but later
allergic diseases.                                              infection or reinfection from younger siblings might
                                                                have some additional protective effect. The low
                                                                prevalence of hay fever among the offspring of poorer
Smoking                                                         families living in rented housing and sharing household
Cigarette smoking has been implicated as a cause of             amenities may reflect unhygienic lifestyles or household
increased serum IgE levels but is associated with a lower       conditions which promote the spread of infection. Wide-
prevalence of cutaneous reactivity to common aeroaller-         spread use of day nurseries from an early age will
gens. This discrepancy has been attributed to a lower           promote cross-infection and may explain the unusually
uptake of smoking and a higher rate of smoking cessa-           low prevalence of allergic sensitization in former east
tion among allergic individuals [39]. In the 1958 cohort,       Germany [36]. The slightly increased risk of subsequent
smoking was less common among respondents with hay              hay fever and eczema [17] among breastfed infants may
fever at 23 only if hay fever or allergic rhinitis was          reflect a reduced incidence of gastrointestinal infection
reported at age 11 or 16 [Strachan DP, unpublished              during breastfeeding, or more hygienic child rearing
analyses]. This suggests that adolescents and young             practice in a broader sense.
adults who suffer from hay fever may indeed be less
likely to take up regular cigarette smoking. However, the
similar rates of hay fever among lifelong non-smokers           Community prognosis
and former smokers suggest that affected individuals are        The hypothesis that early infection may protect against
not more likely to give up smoking once they have               atopic disease offers a coherent explanation for both the
started.                                                        past and present epidemiological patterns of hay fever.
   Higher levels of cord blood IgE in the have been             Over the past 200 years, reductions in average family
reported in the offspring of mothers who smoked                 size, improved household amenities and higher standards
during pregnancy [40], but skin-prick positivity was less       of personal cleanliness have reduced the opportunity for
common among German children whose mothers                      cross-infection within young families. This may have
smoked [36]. There is no evidence in the British birth          resulted in more widespread expression of atopy and
cohorts that maternal smoking during pregnancy or               the emergence of a 'post industrial revolution epidemic'
childhood is an important determinant of symptomatic            of allergic disease, affecting to a greater extent the more
nasal allergy.                                                  affluent classes and areas of the country.
                                                                   If the prevalence of hay fever is increasing as a result of
                                                                changes in biological programming in early childhood,
Community diagnosis
                                                                then the generations who have been found to be at high
Hay fever displays a remarkable degree of variation             risk of allergic disease while young may carry that
within and between families in modern Britain. Most             increased susceptibility for much of their lives. Evidence
302     D. P. Strachan
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