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Research Article| Volume 119, P122-129, October 2016

Ethnic and socio-economic differences in the prevalence of wheeze, severe wheeze, asthma, eczema and medication usage at 4 years of age: Findings from the Born in Bradford birth cohort

Open ArchivePublished:August 23, 2016DOI:https://doi.org/10.1016/j.rmed.2016.08.017

      Highlights

      • Comparison of ethnic differences wheeze, asthma eczema and medication usage.
      • Children of Other ethnic origin were less likely to have a doctor diagnosis of asthma.
      • Other outcomes including severe wheeze, wheeze in the past 12 months, eczema or medication usage did not differ by ethnicity.

      Abstract

      Background

      Asthma, wheeze and eczema are common in early childhood and cause considerable morbidity. Generally rates of these conditions are higher in high income compared to low income countries. Rates in developed nations are generally higher than in less developed countries. After migration to Western countries, differences in risks of developing these conditions may between migrant and non-migrant may diminish.

      Methods

      A convenience sample of 1648 children of White British, Pakistani or Other ethnicity aged between 4 and 5 years were recruited from the main Born in Bradford cohort. Children's parents or guardians were asked to report on a range of potential risk factors and their associations with wheeze, asthma and eczema. Relationships between ethnicity and disease outcomes were examined using logistic regression after adjustment for other relevant risk factors and confounders.

      Results

      Ethnic differences in doctor diagnosed asthma were evident, with children of other ethnic Origin being less likely and children of Pakistani origin more likely to have a diagnosis than White British or other origin children, although after adjustment for other risk factors this difference only remained significant for the Other Ethnic group. Ethnic differences were not observed in other outcomes including wheeze in the past 12 months, severe wheeze and taking medications for breathing problems.

      Conclusions

      In UK born children, traditional risk factors such as gender, family history, socio-economic status and child's medical history may be stronger risk factors than ethnicity or familial migration patterns.

      Keywords

      1. Background

      Asthma, wheeze and eczema are common in early childhood and cause considerable morbidity. Globally wheeze and asthma prevalence in children aged 6–7 is generally highest in high income countries, with the prevalence of current wheeze being lowest in the Indian subcontinent and highest in English-speaking countries such as the United Kingdom and New Zealand [
      • Lai C.K.W.
      • Beasley R.
      • Crane J.
      • et al.
      Global variation in the prevalence and severity of asthma symptoms: phase three of the International Study of Asthma and Allergies in Childhood (ISAAC).
      ]. Within Western countries, migrants generally have lower prevalence rates than native born populations [
      • Garcia-Marcos L.
      • Robertson C.F.
      • Ross Anderson H.
      • et al.
      Does migration affect asthma, rhinoconjunctivitis and eczema prevalence? Global findings from the international study of asthma and allergies in childhood.
      ]. However, the prevalence of wheeze and asthma symptoms may be higher in migrants compared to their peers in their countries of origin, and prevalence and severity increase with each additional year of residence in high-prevalence countries [
      • Garcia-Marcos L.
      • Robertson C.F.
      • Ross Anderson H.
      • et al.
      Does migration affect asthma, rhinoconjunctivitis and eczema prevalence? Global findings from the international study of asthma and allergies in childhood.
      ,
      • Whitrow M.J.
      • Harding S.
      Asthma in Black african, Black caribbean and South asian adolescents in the MRC DASH study: a cross sectional analysis.
      ,
      • Cabieses B.
      • Uphoff E.
      • Pinart M.
      • et al.
      A systematic review on the development of asthma and allergic diseases in relation to international immigration: the leading role of the environment confirmed.
      ]. The ethnic differences in eczema prevalence are not as consistent, with high prevalence observed in Western countries, such as the UK and NZ, but also high prevalence in some low and middle income countries in Africa and Latin America [
      • Odhiambo J.A.
      • Williams H.C.
      • Clayton T.O.
      • et al.
      Global variations in prevalence of eczema symptoms in children from ISAAC Phase Three.
      ]. Similar to the situation with asthma, recent migrants to affluent and Western countries experience lower eczema prevalence than populations already resident in host countries [
      • Garcia-Marcos L.
      • Robertson C.F.
      • Ross Anderson H.
      • et al.
      Does migration affect asthma, rhinoconjunctivitis and eczema prevalence? Global findings from the international study of asthma and allergies in childhood.
      ].
      The prevalence of physician-diagnosed asthma in childhood has been reported to differ by ethnicity in UK and other western populations. In the UK, highest rates have been reported in children of Black ethnicity followed by those of White and South Asian ethnicity [
      • Davidson E.
      • Liu J.J.
      • Sheikh A.
      The impact of ethnicity on asthma care.
      ]. Phenotypes of asthma, wheeze and atopy may also differ by ethnicity [
      • Kelley C.F.
      • Mannino D.M.
      • Homa D.M.
      • et al.
      Asthma phenotypes, risk factors, and measures of severity in a national sample of US children.
      ]. Atopy has also been shown to vary by ethnicity, with South Asian children having higher rates than their White British peers [
      • Carey O.J.
      • Cookson J.B.
      • Britton J.
      • et al.
      The effect of lifestyle on wheeze, atopy, and bronchial hyperreactivity in Asian and white children.
      ], although it is being increasingly recognised that not all persons who experience asthma, wheeze and/or eczema are also atopic [
      • Brown S.
      • Reynolds N.J.
      Atopic and non-atopic eczema.
      ,
      • Court C.S.
      • Cook D.G.
      • Strachan D.P.
      Comparative epidemiology of atopic and non-atopic wheeze and diagnosed asthma in a national sample of English adults.
      ]. Despite persons of South Asian origin resident in the UK being less likely to experience symptoms of wheeze and asthma, there are reports of poorer outcomes, with higher risks of exacerbations and hospitalisations [
      • Davidson E.
      • Liu J.J.
      • Sheikh A.
      The impact of ethnicity on asthma care.
      ,

      Netuveli G, Hurwitz B, Levy M, et al. Ethnic variations in UK asthma frequency, morbidity, and health-service use: a systematic review and meta-analysis. Lancet (London, Engl.;365:312–317, http://dx.doi.org/10.1016/S0140-6736(05)17785-X.

      ,
      • Sheikh A.
      • Steiner M.F.C.
      • Cezard G.
      • et al.
      Ethnic variations in asthma hospital admission, readmission and death: a retrospective, national cohort study of 4.62 million people in Scotland.
      ]. South Asian populations resident in the United Kingdom (UK) are heterogeneous, originating from different countries including India, Pakistan and Bangladesh, experiencing differing cultural and socio-economic profiles.
      Few studies of ethnic differences in childhood eczema have been reported. Lower eczema prevalence in children of Indian, Pakistani and Bangladeshi origin compared to children of White British origin has been reported in a London based study [
      • Whitrow M.J.
      • Harding S.
      Asthma in Black african, Black caribbean and South asian adolescents in the MRC DASH study: a cross sectional analysis.
      ], whilst another prevalence study conducted in Leicester found no differences between White and Asian children [
      • Neame R.L.
      • Berth-Jones J.
      • Kurinczuk J.J.
      • et al.
      Prevalence of atopic dermatitis in Leicester: a study of methodology and examination of possible ethnic variation.
      ].
      The current study therefore examines the risks of wheeze, severe wheeze, doctor diagnosed asthma and eczema, and treatment provision for breathing problems, in an early childhood population that is UK born and predominantly of White British and Pakistani ethnic origin [
      • Wright J.
      • Small N.
      • Raynor P.
      • et al.
      Cohort profile: the born in bradford multi-ethnic family cohort study.
      ]. We also examine the comparability of these results to studies that have included heterogeneous South Asian populations with differing migration profiles [
      • Lai C.K.W.
      • Beasley R.
      • Crane J.
      • et al.
      Global variation in the prevalence and severity of asthma symptoms: phase three of the International Study of Asthma and Allergies in Childhood (ISAAC).
      ,
      • Whitrow M.J.
      • Harding S.
      Asthma in Black african, Black caribbean and South asian adolescents in the MRC DASH study: a cross sectional analysis.
      ,
      • Netuveli G.
      • Hurwitz B.
      • Sheikh A.
      Ethnic variations in incidence of asthma episodes in England & Wales: national study of 502,482 patients in primary care.
      ].

      2. Methods

      A sub-cohort of children from the Born in Bradford cohort study were recruited to participate in this study of asthma and allergy; this work was conducted as part of a larger EU FP7 project entitled Mechanisms of the Development of ALLergy (MeDALL) [
      • Bousquet J.
      • Anto J.
      • Auffray C.
      • et al.
      MeDALL (Mechanisms of the Development of ALLergy): an integrated approach from phenotypes to systems medicine.
      ]. This subcohort consisted of a convenience sample of 1648 children aged between 4 and 5 years recruited between 22nd October 2012 and 24th April 2014 whose parented consented for participation. Full details of the main Born in Bradford study and recruitment processes have been reported elsewhere [
      • Wright J.
      • Small N.
      • Raynor P.
      • et al.
      Cohort profile: the born in bradford multi-ethnic family cohort study.
      ].
      Children's parents or guardians were asked to report on a range of potential risk factors and their associations with wheeze, asthma and atopy. Children's ethnicity was assigned based on maternal self-reported ethnicity and classified as White British, Pakistani and Other. We excluded responses from cases where maternal ethnicity was missing (excluded n = 2), resulting in an eligible study population of 1646 children and their carers; which was predominantly their mother (n = 1621) or father (n = 22).

      2.1 Clinical outcomes

      Wheeze: defined as self-reported wheeze in the past 12 months.
      Severe wheeze: defined as reported wheeze on four or more occasions in the past year.
      Asthma: defined as a positive report of doctor diagnosis of asthma ever.
      Eczema: defined as a positive report of ever been diagnosed by a physician with having eczema/atopic dermatitis.
      Medication use: defined as a positive response to question asking if child had received medication for asthma or other breathing problems during the previous 12 months.

      2.2 Statistical analysis

      The variables included in the analysis were based on previous literature, and in the case of socio-economic variables, were selected to ensure that a wide range were considered as our previous work in the cohort has shown that socio-economic measures and health behaviours may differ between different ethnic groups [
      • Fairley L.
      • Cabieses B.
      • Small N.
      • et al.
      Using latent class analysis to develop a model of the relationship between socioeconomic position and ethnicity: cross-sectional analyses from a multi-ethnic birth cohort study.
      ,
      • West J.
      • Lawlor D.A.
      • Fairley L.
      • et al.
      Differences in socioeconomic position, lifestyle and health-related pregnancy characteristics between Pakistani and White British women in the Born in Bradford prospective cohort study: the influence of the woman's, her partner's and their parents' place.
      ]. In particular, we considered adjusting for variables that have previously been shown to be associated with wheeze, asthma, eczema or medication usage in childhood. These included mothers age at delivery, maternal history of asthma or atopy (yes vs no), paternal history of asthma or atopy (yes vs no), maternal smoking during pregnancy (yes vs no), child currently exposed to smoke (yes vs no), visible signs of mould or damp in the home (yes vs no), gas cooker used in the home (no, yes always use an extractor fan, yes sometimes use a fan, yes never use a fan) mother born abroad (yes vs no), father born abroad (yes vs no), child seen doctor for chest infection in the past 12 months (yes vs no), born at term (yes vs no), gender of child (male vs female), ever breastfed (yes vs no), older sibling (yes vs no), birthweight (<2500g, 2500–2999g, 3000–3499g, 3500–3999g, >=4000g), mode of birth (vaginal vs caesarean), ever eczema ever (yes vs no), ever had a problem with sneezing, or a runny or blocked nose when s/he did not have a cold or the flu (yes vs no) and mother's BMI at first pregnancy appointment with a midwife (booking).
      We included three different socio-economic indicators: highest maternal education level reported in the baseline questionnaire; (categorised as less than 5 General Certificates of Secondary Education (GCSEs), >5 GCSEs, A level, Degree Level, Other, Foreign Unknown or Other); current home ownership (yes vs no); and subjective poverty (yes vs no). Subjective poverty was derived by asking women how they felt they were managing financially and were classified as subjectively poor if they responded that they were “finding it very difficult” or “finding it quite difficult” and not subjectively poor if they responded that they were “living comfortably”, “doing alright” or “just getting by”.
      Comparison of characteristics between study participants of different ethnic backgrounds was performed using Chi square tests to investigate differences in proportions and ANOVA or Kruskall-Wallis tests to compare continuous data items.
      Univariate associations between covariables and outcomes were estimated using logistic regression. The optimal inclusion of socio-economic variables into final mutually adjusted models was determined by creating models with different combinations of socio-economic variables and calculating the Bayesian Information Criterion (BIC) to determine the most parsimonious model. The model with the lowest BIC value for each clinical outcome was chosen as the final model. All logistic regression analyses used complete case analysis only. Output from models was expressed as odds ratios and 95% confidence intervals of the effect estimates and corresponding p values provided. Estimates were assumed to indicated statistically significant differences if p values < 0.05. All analyses were conducted using Stata SE 14.1 (Statacorp, Texas).

      3. Results

      The baseline characteristics of the participating mother-child pairs, by ethnicity, are shown in Table 1 below.
      Table 1Characteristics of study participants.
      White BritishPakistaniOtherTotalP value
      n = 495n = 961n = 190n = 1646
      Family history
      Maternal history of asthma or atopy287 (58.0)277 (28.8)69 (36.3)633 (38.5)<0.001
      Paternal history of asthma or atopy204 (41.2)264 (27.5)61 (32.1)529 (32.1)<0.001
      Socio-demographic factors
      Maternal age at child's birth29.2 (6.2)28.6 (5.3)29.1 (5.2)28.8 (5.5)0.13
      Maternal BMI at booking
      Underweight3 (0.6)59 (6.1)4 (2.1)66 (4.0)
      Normal210 (42.4)429 (44.6)92 (48.4)731 (44.4)
      Overweight129 (26.1)271 (28.2)53 (27.9)453 (27.5)
      Obese123 (24.9)150 (15.6)31 (16.3)304 (18.5)
      Missing30 (6.1)52 (5.4)10 (5.3)92 (5.6)<0.001
      Maternal education (baseline)
      <5 GCSEs84 (17.0)290 (30.2)26 (13.7)400 (24.3)
      5 GCSEs150 (30.3)290 (30.2)44 (23.2)484 (29.4)
      A level81 (16.4)101 (10.5)25 (13.2)207 (12.6)
      Degree level127 (25.7)247 (25.7)65 (34.2)439 (26.7)
      Other47 (9.5)17 (1.8)9 (4.7)73 (4.4)
      Foreign unknown/Don't know6 (1.2)12 (1.3)20 (10.5)38 (2.3)<0.001
      Housing tenure (current)
      Owns house291 (58.8)716 (74.5)110 (57.8)1117 (67.9)>0.001
      Subjectively poor (current)34 (6.87)49 (5.10)15 (7.89)98 (5.95)0.188
      Mother born abroad (baseline)

      Yes
      9 (1.8)645 (67.1)121 (63.7)775 (47.1)<0.001
      Father born abroad (baseline)

      Yes
      22 (4.4)572 (59.5)112 (59.0)706 (42.9)<0.001
      Environmental exposures
      Currently exposed to smoke
      Includes smoke exposure from mother, father or others in the home.
      50 (10.1)108 (11.2)16 (8.4)174 (10.6)0.473
      Maternal smoked during pregnancy125 (25.3)33 (3.4)21 (9.3)179 (10.9)<0.001
      Gas cooker in the home
      No92 (18.6)12 (1.3)21 (11.1)125 (7.6)
      Yes always use a fan138 (27.9)498 (51.9)70 (36.8)706 (42.9)
      Yes sometimes use a fan122 (24.7)221 (23.0)52 (27.4)395 (24.0)
      Yes never use a fan143 (28.9)230 (23.9)47 (24.7)420 (25.5)<0.001
      Visible signs of dampness or mould99 (20.0)206 (21.4)41 (21.6)346 (21.0)0.800
      Child characteristics
      Female gender234 (47.2)497 (51.7)96 (50.5)827 (50.2)0.274
      Ever breastfed, yes336 (67.9)730 (76.0)162 (85.3)1228 (74.6)<0.001
      Seen doctor for chest infection past 12 months52 (10.9)155 (16.9)22 (12.0)230 (14.5)0.029
      Older sibling261 (52.7)627 (65.2)108 (55.8)996 (60.5)<0.001
      Eczema ever177 (35.8)227 (23.6)49 (25.8)453 (27.5)<0.001
      Ever sneezing, runny or blocked nose when no cold106 (21.4)178 (18.5)42 (22.1)326 (19.8)0.287
      Birth weight
      <250027 (5.5)104 (10.8)17 (9.0)148 (9.0)
      2500–299974 (15.0.)277 (28.8)46 (24.2)397 (24.1)
      3000–3499170 (34.3)342 (35.6)80 (42.1)592 (36.0)
      3500–3999145 (29.3)184 (19.2)35 (18.4)364 (22.1)
      >400079 (16.0)54 (5.6)12 (6.3)145 (8.8)<0.001
      Term pregnancy, yes437 (88.3)833 (86.7)166 (87.4)1436 (87.2)0.735
      Mode of birth
      Vaginal379 (76.6)755 (78.6)141 (74.2)1275 (77.5)
      Caesarean110 (22.2)193 (20.1)47 (24.7)350 (21.3)0.276
      Childs BMI z score, mean (SD)0.32 (0.97)0.03 (1.23)0.09 (1.12)0.09 (1.15)<0.001
      a Includes smoke exposure from mother, father or others in the home.
      Maternal and paternal history of asthma or atopy was more common in children of White British origin compared to Pakistani and Other ethnic groups. The Other ethnic group consisted of 60 Indian, 29 Bangladeshi, 25 White Other, 24 Black, 12 Mixed White and Black, 8 Mixed White and South Asian and 32 of Other ethnic background which included Arab and other Asian backgrounds which included Chinese and Philippino.
      Maternal smoking during pregnancy was higher in the White British group compared to the Other ethnic group and lowest in the Pakistani group. Current exposure to smoke in the home was higher in the Pakistani group compared to White British and lowest in the Other group. Women of Pakistani ethnicity were most likely to be in the normal weight category at booking.
      Socio-demographic characteristics differed between the different ethnic groups. Mother's age at delivery was youngest for mothers of Pakistani origin followed by mothers of Other ethnicity and of White British origin. Women in the Other ethnic group were more likely to have a degree or an A level education (or equivalent) followed by White British and Pakistani women. Mothers of Other ethnic origin were most likely to report that they were managing financially whilst White British mothers were least likely to report this. Mothers of Other ethnic origin were most likely to be born abroad compared to mothers of White British and Pakistani ethnic groups, whereas fathers of Pakistani children were most likely to born abroad compared to fathers of White British and Other ethnic origin. Rates of home ownership were highest amongst Pakistani respondents.
      There were also ethnic differences in specific household environmental risk factors; White British families were most likely to have gas cookers and use them without an extractor fan or only sometimes use an extractor fan, whilst children of Other ethnicities were slightly more likely to have visible damp in their homes.
      Children of Pakistani origin were more likely to have been born low or very low birth weight, delivered vaginally rather than via caesarean, and have an older sibling compared to White British and Other ethnic groups. Children of Other ethnic origin were most likely to have ever been breastfed, followed by Pakistani and lowest in the White British group. Minimal ethnic differences were observed between the prevalence of term birth. Eczema prevalence was highest in children of White British origin compared to children of other ethnic groups.
      Table 2 below presents the patterns, by ethnicity, of all outcomes examined.
      Table 2Summary of asthma, wheeze, eczema and medication usage by ethnic group.
      White BritishPakistaniOtherTotalP value
      n = 495n = 961n = 190n = 1646
      Wheeze
      Wheeze in the last 12 months98 (19.8)217 (22.6)29 (15.3)344 (20.9)0.063
      Severe wheeze (>4 times in a year)
      Denominator participants that reported wheezing or whistling in the last 12 months.
      31 (6.3)39 (4.1)4 (2.1)74 (4.5)0.014
      Asthma diagnosis and management
      Ever diagnosed by doctor as having asthma42 (8.9)129 (13.4)6 (3.2)179 (10.9)<0.001
      Ever diagnosed by doctor as having eczema or atopic dermatitis161 (32.5)200 (20.8)42 (22.1)403 (24.5)<0.001
      Taken medicines for asthma or breathing difficulties in past 12 months94 (19.0)185 (19.3)23 (12.1)302 (18.3)0.065
      a Denominator participants that reported wheezing or whistling in the last 12 months.
      Wheeze in the last 12 months was highest in children of Pakistani ethnicity, followed by children of White British and Other ethnic groups. In contrast, severe wheeze and eczema was highest in the White British group followed by those of Pakistani and Other ethnic background. Doctor diagnosis of asthma and medication usage for asthma or breathing problems was consistently highest in children of Pakistani origin followed by children of White British and then children of Other ethnic background.
      All potential confounders were explored in two different models for each outcome of interest. The first model (Table 3) examined the univariate associations between the various measures of socioeconomic position and all five outcomes; the second model mutually adjusted for all variables (Table 4).
      Table 3Associations of socio-economic measures with outcomes.
      Wheeze in the last 12 monthsSevere wheezeDoctor diagnosed asthmaDoctor diagnosed eczemaMedications for asthma or breathing problems
      Maternal education
      <5 GCSEs0.90 (0.65–1.24)1.09 (0.57–2.10)1.13 (0.77–1.67)0.76 (0.55–1.04)0.91 (0.65–1.27)
      5+ GCSEs11111
      A level0.86 (0.58–1.28)1.05 (0.47–2.36)0.53 (0.29–0.96)*1.15 (0.80–1.67)0.89 (0.58–1.34)
      Degree level0.70 (0.51–0.97)*1.05 (0.55–1.99)0.52 (0.32–0.81)*1.08 (0.80–1.45)0.71 (0.51–1.01)
      Other1.07 (0.61–1.90)1.70 (0.62–4.70)0.96 (0.45–2.02)1.14 (0.66–1.99)1.20 (0.67–2.15)
      Foreign unknown/Don't know0.62 (0.25–1.51)1.29 (0.29–5.73)1.03 (0.39–2.74)0.94 (0.43–2.04)0.89 (0.38–2.08)
      Subjectively poor, yes2.21 (1.44–3.41)*1.15 (0.45–2.91)1.79 (1.03–3.09)*1.25 (0.79–1.96)1.56 (0.97–2.50)
      Housing tenure
      Owns house, yes0.65 (0.51–0.83)**0.45 (0.29–0.72)**0.66 (0.48–0.90)**0.94 (0.74–1.19)0.69 (0.53–0.89)**
      *p < 0.05, **p < 0.001, ***p < 0.0001.
      Table 4Unadjusted and Adjusted associations with study outcomes.
      For wheeze in the past 12 months subjective poverty increased the odds by 2.10 (1.20–3.66)**, owning compared to renting your house was associated with a reduced odds of severe wheeze OR 0.49 (0.27–0.89)*, doctor diagnosed asthma OR 0.62 (0.41–0.93)*. Housing tenure was not statistically significantly associated with medication for asthma or breathing problems OR 0.71 (0.51–1.00) whilst for doctor diagnosed eczema none of the socio-economic measures evaluated improved model fit so none were included in final models.
      Wheeze in the last 12 monthsSevere wheezeDoctor diagnosed asthmaDoctor diagnosed eczemaMedications for asthma or breathing problems
      UnadjustedAdjustedUnadjustedAdjustedUnadjustedAdjustedUnadjustedAdjustedUnadjustedAdjusted
      Ethnicity
      White British1111111111
      Pakistani1.18 (0.90–1.54)0.98 (0.60–1.61)0.63 (0.39–1.03)0.92 (0.39–2.16)1.59 (1.11–2.28)*1.84 (0.99–3.44)0.55 (0.43–0.70)***0.79 (0.52–1.22)1.02 (0.77–1.34)1.22 (0.73–2.01)
      Other0.73 (0.47–1.16)0.57 (0.30–1.09)0.32 (0.11–0.92)0.47 (0.14–1.60)0.33 (0.14–0.80)*0.35 (0.13–0.96)*0.59 (0.40–0.87)**0.68 (0.40–1.16)0.59 (0.36–0.97)*0.67 (0.35–1.29)
      Female gender0.77 (0.60–0.96)*0.75 (0.56–1.00)0.88 (0.55–1.41)0.96 (0.57–1.63)0.64 (0.46–0.87)**0.56 (0.39–0.81)**0.97 (0.77–1.21)1.01 (0.78–1.29)0.67 (0.52–0.86)**0.66 (0.49–0.89)**
      Eczema ever1.96 (1.53–2.52)*1.71 (1.25–2.34)***1.85 (1.49–2.98)*1.35 (0.77–2.38)2.43 (1.77–3.34)***2.08 (1.43–3.02)***2.26 (1.75–2.94)***1.82 (1.33–2.50)***
      Ever sneezing, runny or blocked nose when no cold2.76 (2.11–3.60)*2.60 (1.88–3.61)***3.51 (2.18–5.64)***3.97 (2.28–6.92)***2.42 (1.73–3.39)***2.02 (1.37–2.99)***2.06 (1.59–2.67)***1.83 (1.36–2.46)***2.89 (2.19–3.81)***2.58 (1.86–3.59)***
      Older sibling0.80 (0.62–1.02)0.78 (0.55–1.10)0.56 (0.35–0.89)*0.82 (0.44–1.53)0.87 (0.63–1.20)1.01 (0.66–1.54)0.61 (0.49–0.77)***0.60 (0.45–0.80)***0.72 (0.56–0.93)*0.72 (0.51–1.02)
      Maternal age at child's birth
      15–191.07 (0.57–2.01)0.93 (0.42–2.07)2.51 (1.09–5.77)1.32 (0.46–3.82)1.72 (0.85–3.48)1.52 (0.62–3.73)1.05 (0.59–1.90)0.76 (0.38–1.52)1.19 (0.63–2.24)0.90 (0.41–2.00)
      20–241.13 (0.82–1.56)1.13 (0.75–1.70)0.88 (0.48–1.62)0.65 (0.32–1.33)1.21 (0.81–1.83)1.18 (0.72–1.93)0.99 (0.73–1.34)0.88 (0.62–1.26)1.04 (0.75–1.46)0.87 (0.57–1.32)
      25–291111111111
      30–341.01 (0.73–1.39)1.19 (0.79–1.77)0.54 (0.27–1.07)0.53 (0.23–1.20)0.77 (0.49–1.20)0.85 (0.51–1.41)0.88 (0.64–1.18)0.98 (0.69–1.39)0.84 (0.59–1.18)0.84 (0.56–1.27)
      35 or greater0.97 (0.67–1.41)1.23 (0.78–1.93)0.57 (0.26–1.26)0.70 (0.29–1.70)1.10 (0.69–1.76)1.27 (0.73–2.22)0.99 (0.70–1.40)1.01 (0.68–1.50)1.00 (0.69–1.47)1.07 (0.68–1.70)
      Family history
      Maternal history of asthma or atopy1.43 (1.13–1.82)*1.11 (0.81–1.52)1.94 (1.22–3.10)*1.12 (0.64–1.96)1.72 (1.26–2.35)**1.82 (1.25–2.65)**2.48 (1.97–3.12)***2.18 (1.67–2.84)***1.82 (1.41–2.34)***1.52 (1.11–2.08)**
      Paternal history of asthma or atopy1.09 (0.85–1.41)1.15 (0.84–1.57)1.08 (0.66–1.77)0.88 (0.48–1.58)1.34 (0.97–1.84)1.41 (0.96–2.05)1.52 (1.20–1.92)***1.25 (0.96–1.64)1.18 (0.90–1.53)1.16 (0.85–1.60)
      Maternal smoking during pregnancy1.23 (0.85–1.77)1.24 (0.75–2.04)1.29 (0.65–2.57)0.51 (0.22–1.21)0.90 (0.54–1.51)0.93 (0.48–1.80)1.08 (0.76–1.54)0.75 (0.48–1.18)1.05 (0.70–1.55)0.81 (0.48–1.38)
      Currently exposed to smoke1.19 (0.82–1.72)1.14 (0.73–1.79)1.87 (1.00–3.47)*1.93 (0.92–4.06)1.21 (0.75–1.95)1.14 (0.66–1.94)1.09 (0.76–1.56)1.12 (0.75–1.68)1.00 (0.67–1.50)0.89 (0.55–1.44)
      Mother born abroad (baseline)

      Yes
      0.98 (0.78–1.25)0.84 (0.59–1.21)0.32 (0.18–0.56)***0.24 (0.11–0.49)***1.25 (0.91–1.70)1.22 (0.78–1.90)0.65 (0.51–0.81)***0.88 (0.63–1.22)0.88 (0.68–1.13)0.84 (0.58–1.22)
      Father born abroad vs UK born (baseline)1.19 (0.94–1.51)1.38 (0.97–1.95)0.85 (0.52–1.37)1.16 (0.57–2.35)1.33 (0.97–1.81)1.39 (0.91–2.12)0.71 (0.56–0.90)**0.93 (0.68–1.27)1.13 (0.88–1.45)1.26 (0.88–1.81)
      Seen doctor for chest infection past 12 months7.77 (5.77–10.45)***7.29 (5.20–10.20)***4.22 (2.59–6.89)***3.73 (2.10–6.61)***4.03 (2.89–5.70)***2.92 (1.97–4.34)***1.56 (1.16–2.11)**1.38 (0.98–1.95)5.74 (4.27–7.73)***4.98 (3.55–7.00)***
      Visible signs of dampness or mould1.18 (0.89–1.57)1.11 (0.78–1.58)1.13 (0.65–1.96)0.82 (0.45–1.50)0.98 (0.67–1.44)0.80 (0.51–1.24)1.34 (1.03–1.74)*1.37 (1.02–1.85)*1.23 (0.91–1.65)0.77 (0.54–1.09)
      Gas cooker in the home
      No1111111111
      Yes always use a fan1.98 (1.14–3.44)*3.26 (1.48–7.19)**1.21 (0.47–3.17)2.46 (0.73–8.30)1.58 (0.77–3.24)1.92 (0.72–5.11)0.66 (0.44–1.00)0.76 (0.46–1.26)1.58 (0.91–2.76)2.52 (1.18–5.38)*
      Yes sometimes use a fan1.70 (0.95–3.04)3.09 (1.38–6.92)**1.28 (0.47–3.48)3.25 (0.92–11.5)1.37 (0.64–2.92)2.15 (0.79–5.87)0.67 (0.43–1.04)0.68 (0.40–1.14)1.52 (0.85–2.72)2.83 (1.30–6.15)**
      Yes never use a fan1.86 (1.05–3.31)*2.72 (1.23–6.01)*0.89 (0.31–2.50)1.21 (0.34–4.27)1.95 (0.93–4.06)2.51 (0.95–6.66)0.77 (0.50–1.20)0.81 (0.49–1.35)1.63 (0.92–2.91)2.40 (1.12–5.17)*
      Child characteristics
      Birth weight
      <25001.63 (1.09–2.44)*2.08 (1.17–3.69)*2.18 (1.09–4.38)2.07 (0.79–5.46)1.39 (0.81–2.38)1.77 (0.88–3.56)0.79 (0.51–1.23)0.48 (0.27–0.85)*1.58 (1.03–2.43)*1.52 (0.84–2.73)
      2500–29991.02 (0.75–1.40)1.02 (0.69–1.51)0.77 (0.39–1.52)0.83 (0.37–1.84)1.05 (0.69–1.60)1.05 (0.65–1.70)0.87 (0.64–1.17)0.88 (0.63–1.23)0.93 (0.66–1.31)0.90 (0.60–1.36)
      3000–34991111111111
      3500–39990.90 (0.65–1.25)0.80 (0.54–1.19)1.18 (0.63–2.19)1.33 (0.66–2.69)1.19 (0.78–1.80)1.20 (0.75–1.92)1.03 (0.76–1.39)0.90 (0.64–1.27)1.05 (0.75–1.48)1.09 (0.73–1.62)
      >40000.84 (0.53–1.35)0.69 (0.37–1.30)0.81 (0.30–2.15)0.98 (0.32–2.95)0.95 (0.51–1.75)0.87 (0.39–1.97)1.22 (0.82–1.83)1.16 (0.71–1.90)1.29 (0.82–2.03)1.44 (0.80–2.58)
      Child BMI z score1.04

      (0.94–1.16)
      1.06

      (0.93–1.22)
      1.02

      (0.83–1.25)
      0.99 (0.77–1.28)1.05

      (0.92, 1.20)
      1.09

      (0.93–1.28)
      1.03

      (0.93–1.13)
      0.95 (0.85–1.08)1.03

      (0.92–1.15)
      1.04

      (0.90–1.19)
      Term pregnancy0.56 (0.40–0.79)**0.91 (0.56–1.49)0.45 (0.26–0.81)*0.59 (0.26–1.35)0.81 (0.51–1.28)1.00 (0.54–1.83)0.81 (0.58–1.14)0.65 (0.41–1.03)0.54 (0.38–0.77)**0.70 (0.43–1.15)
      Ever breastfed0.93 (0.71–1.22)0.97 (0.69–1.38)0.74 (0.45–1.23)0.84 (0.46–1.54)0.86 (0.61–1.22)0.86 (0.57–1.30)1.18 (0.91–1.54)0.77 (0.54–1.09)0.90 (0.68–1.19)0.77 (0.54–1.09)
      Mode of birth
      Vaginal1111111111
      Caesarean1.11 (0.83–1.47)1.00 (0.70–1.43)1.10 (0.58–2.10)1.08 (0.56–2.05)1.05 (0.72–1.54)1.00 (0.64–1.55)1.54 (1.19–2.00)1.59 (1.17–2.15)**1.21 (0.90–1.63)1.09 (0.76–1.56)
      Maternal BMI at booking
      Underweight1.31 (0.71–2.40)1.35 (0.64–2.86)2.62 (0.82–8.37)2.68 (0.84–8.55)0.96 (0.43–2.18)0.66 (0.25–1.73)0.93 (0.52–1.67)1.24 (0.65–2.37)1.20 (0.63–2.27)0.98 (0.45–2.16)
      Normal1111111111
      Overweight1.34 (1.01–1.79)*1.44 (1.01–2.05)*1.17 (0.60–2.28)1.16 (0.60–2.25)0.99 (0.68–1.44)0.93 (0.60–1.44)0.89 (0.68–1.17)0.86 (0.63–1.17)1.13 (0.83–1.53)1.19 (0.83–1.71)
      Obese1.33 (0.96–1.84)1.39 (0.92–2.09)0.96 (0.45–2.05)0.96 (0.46–2.04)0.99 (0.64–1.52)0.95 (0.57–1.57)0.90 (0.66–1.23)0.79 (0.55–1.14)1.23 (0.87–1.72)1.12 (0.74–1.70)
      *p < 0.05, **p < 0.001, ***p < 0.0001.
      a For wheeze in the past 12 months subjective poverty increased the odds by 2.10 (1.20–3.66)**, owning compared to renting your house was associated with a reduced odds of severe wheeze OR 0.49 (0.27–0.89)*, doctor diagnosed asthma OR 0.62 (0.41–0.93)*. Housing tenure was not statistically significantly associated with medication for asthma or breathing problems OR 0.71 (0.51–1.00) whilst for doctor diagnosed eczema none of the socio-economic measures evaluated improved model fit so none were included in final models.

      3.1 Wheeze in the past 12 months

      Mutual adjustment of variables showed that the odds of wheeze in the preceding 12 months was higher if the child had eczema ever OR 1.71 (1.25–2.34), had a history of sneezing, runny or blocked nose when no cold 2.60 (1.88–3.61), has seen a doctor for a chest infection in the previous 12 months OR 7.29 (5.20–10.20), had a birthweight of less than 2500 g OR 2.08 (1.17–3.69) or whether their mother had been overweight at the beginning of her pregnancy OR 1.44 (1.01–2.05). Additionally use of gas cooker was associated with elevated odds whether a gas cooker was used and also always used a fan OR 3.26 (1.48–7.19), sometimes used a fan OR 3.09 (1.38–6.92) or never used a fan OR 2.72 (1.23–6.01).

      4. Severe wheeze

      Mutually adjusted models showed that the odds of severe wheeze were higher in children who reported sneezing, runny or blocked nose when no cold OR 3.97 (2.28–6.92) and reported of a doctor visit for chest infection OR 3.73 (2.10–6.61). Only if mothers place of birth had been abroad was there a lower odds of severe wheeze OR 0.24 (0.11–0.49).

      4.1 Doctor diagnosed asthma

      Odds of doctor diagnosed asthma were shown to be higher in children who reported ever sneezing, runny or blocked nose when not had a cold OR 2.02 (1.37–2.99), seen a doctor for a chest infection in the past 12 months OR 2.92 (1.97–4.34) and having a maternal history of asthma or atopy OR 1.82 (1.25–2.65) and eczema ever OR 2.08 (1.43–3.02) were all associated with higher odds of doctor diagnosed asthma. Reduced odds of asthma were only observed in girls compared to boys OR 0.56 (0.39–0.81) and children of Other ethnic group compared to White British OR 0.35 (0.13–0.96). Pakistani ethnicity was not statistically significantly associated with increased odds of doctor diagnosed asthma.

      4.2 Doctor diagnosed eczema

      Odds of doctor diagnosed eczema were higher in children who had problems with sneezing when didn't have a cold OR 1.83 (1.36–2.46), had a maternal history of asthma or atopy OR 2.18 (1.67–2.84), were living in a home with visible signs of dampness or mould OR 1.37 (1.02–1.85) or had been born via caesarean section OR 1.59 (1.17–2.15). Lower odds were associated with having older siblings OR 0.60 (0.45–0.80) and being born <2500 g compared to 3000–3500 g OR 0.48 (0.27–0.85).

      4.3 Medications for asthma or breathing problems

      Having eczema ever OR 1.82 (1.33–2.50), ever sneezing or having a runny nose ever when not having a cold OR 2.58 (1.86–3.59), maternal history of asthma or atopy OR 1.52 (1.11–2.08), having seen a doctor a chest infection in the previous 12 months OR 4.98 (3.55–7.00) and use of a gas cooker in the home whether always using an extractor fan OR 2.52 (1.18–5.38), sometimes uses a fan OR 2.83 (1.30–6.15) or never uses a fan OR 2.40 (1.12–5.17) were all positively associated with medications for asthma or breathing problems. Female gender OR 0.66 (0.49–0.89) was however associated with a lower odds of receiving medications in line with the reduced risk of respiratory problems for girls.

      5. Discussion

      This study has found ethnic differences in the prevalence of doctor diagnosed asthma, with children of Other ethnicity less likely to receive a diagnosis than White British or Pakistani ethnicity children. However, no significant ethnic differences were observed for wheeze in the last 12 months, severe wheeze, doctor diagnosed eczema or taking medications for breathing problems or asthma, even after adjustment for other risk factors. For all five outcomes evaluated, one variable had consistent positive associations with outcomes: sneezing or having a runny nose ever when not having a cold and having whilst having seen a doctor for a chest infection in the previous 12 months was associated with higher odds of all outcomes with the exception of doctor diagnosed eczema. For most respiratory and respiratory medication usage outcomes, with the exception of severe wheeze, ever having eczema was associated with higher odds of these outcomes.
      Well established factors such as gender, family history, socio-economic status and child's medical history and chest infection were found to be stronger risk factors than ethnicity for the outcomes examined.

      5.1 Strengths and weaknesses

      The strengths of our studies include the large sample size, a homogenous UK born Pakistani comparator group with a rich collection of socio-demographic and clinical data which has allowed for adjustment for a wide range of potential confounding factors. We were also able to adjust for multiple measures of socio-economic status at different periods of the life-course, an approach that has been recommended when examining health inequalities within and between ethnic groups [
      • Krieger N.
      A glossary for social epidemiology.
      ,
      • Galobardes B.
      • Shaw M.
      • Lawlor D.A.
      • et al.
      Indicators of socioeconomic position (part 1).
      ,
      • Galobardes B.
      • Shaw M.
      • Lawlor D.A.
      • et al.
      Indicators of socioeconomic position (part 2).
      ]. We also adjusted for a wide range of factors relating to maternal and paternal migration in addition to ethnic background as well as other established risk factors for asthma and wheeze, although we were unable to adjust for pet ownership or day care attendance as this information was not collected.

      5.2 Strengths and weakness compared to other studies

      Our findings are consistent with results from the Millennium cohort study in finding no difference in wheeze between children of White British and Pakistani or Indian ethnic origin children [
      • Panico L.
      • Bartley M.
      • Marmot M.
      • et al.
      Ethnic variation in childhood asthma and wheezing illnesses: findings from the Millennium Cohort Study.
      ] in the early years. Our findings of higher rates of doctor diagnosed asthma in Pakistani compared to White British children, although not achieving statistical significance, are similar to those of Panico et al. [
      • Panico L.
      • Bartley M.
      • Marmot M.
      • et al.
      Ethnic variation in childhood asthma and wheezing illnesses: findings from the Millennium Cohort Study.
      ] who had used a definition of asthma ever. Irrespective of the definition used, results for asthma both from ours and earlier studies should be interpreted with caution given the diagnostic uncertainty of asthma in the age groups under study. Our results are also based on a UK born Pakistani population which may also explain the similarity of some of our findings to those of Panico et al. [
      • Panico L.
      • Bartley M.
      • Marmot M.
      • et al.
      Ethnic variation in childhood asthma and wheezing illnesses: findings from the Millennium Cohort Study.
      ].
      With the exception of the current study and that of Panico et al. [
      • Panico L.
      • Bartley M.
      • Marmot M.
      • et al.
      Ethnic variation in childhood asthma and wheezing illnesses: findings from the Millennium Cohort Study.
      ], previous studies of ethnic differences in wheeze, asthma and asthma treatment in the UK including Pakistani participants, analysed their data as part of a homogenous grouping of South Asian participants. A previous systematic review and meta-analysis of ethnic variations in asthma frequency and morbidity concluded that the prevalence of asthma and wheeze was lower in South Asian populations than observed for White children; however these studies were limited by the heterogeneity of ethnic groups included, and the lack of adjustment for migration status [

      Netuveli G, Hurwitz B, Levy M, et al. Ethnic variations in UK asthma frequency, morbidity, and health-service use: a systematic review and meta-analysis. Lancet (London, Engl.;365:312–317, http://dx.doi.org/10.1016/S0140-6736(05)17785-X.

      ]. The other variable that is perhaps more likely to have influenced the lower prevalence results observed for South Asian children in the systematic review is the socio-economic profile of the included participants which will vary amongst and between different South Asian groups. South Asian women of Indian ethnic origin are more likely to be economically active compared to women of Pakistani and Bangladeshi ethnic backgrounds [
      • Dale A.A.
      Life-course perspective on ethnic differences in Women's economic activity in britain.
      ] and children of Bangladeshi and Pakistani origin are more likely to be economically deprived than Indian children [
      • Platt L.
      JRF Programme Paper: Poverty and Ethnicity, Inequality within Ethnic Groups.
      ].
      Our findings for eczema are consistent with earlier findings in showing lower rates of eczema in children of Pakistani origin compared to White British children. Lower rates of eczema in Pakistani children are likely related to the lower rates of familial history and higher likelihood of being in a low socio-economic group, given previous consistent findings showing higher rates of eczema in offspring born to parents with asthma and/or eczema and those of higher socio-economic status [
      • Cabieses B.
      • Uphoff E.
      • Pinart M.
      • et al.
      A systematic review on the development of asthma and allergic diseases in relation to international immigration: the leading role of the environment confirmed.
      ,
      • Bisgaard H.
      • Halkjaer L.B.
      • Hinge R.
      • et al.
      Risk analysis of early childhood eczema.
      ,
      • Purvis D.J.
      • Thompson J.M.D.
      • Clark P.M.
      • et al.
      Risk factors for atopic dermatitis in New Zealand children at 3.5 years of age.
      ].
      We selected children for inclusion in this study based on their age based on those already participating in the overall Born in Bradford study. Compared to the main Born in Bradford study population [
      • Wright J.
      • Small N.
      • Raynor P.
      • et al.
      Cohort profile: the born in bradford multi-ethnic family cohort study.
      ] we have oversampled children of Pakistani ethnicity in this current subgroup which has enabled examination of parental migration effects. Whilst our results are likely representative of the Bradford district they may not be representative childhood populations in other UK cities.

      6. Conclusion

      The finding of a higher prevalence of doctor diagnosed asthma for Pakistani children in this young age group, in contrast with the lack of ethnic difference in asthma symptoms, may suggest greater medicalization of wheeze and respiratory symptomology for these children.
      The findings of the current study confirm the conclusions of the Millennium Cohort study [
      • Panico L.
      • Bartley M.
      • Marmot M.
      • et al.
      Ethnic variation in childhood asthma and wheezing illnesses: findings from the Millennium Cohort Study.
      ], suggesting that associations between wheeze, asthma, eczema and medication usage for South Asian children are not homogenous. Authors of future studies should present results by different South Asian origin and report the migration status of the populations studied so that evidence generated will have greater validity and generalisability.

      Competing interest

      The authors declare that they have no conflicts of interest in relation to this work.

      Funding

      The data collection for this study was funded by the MeDALL project. MeDALL is a collaborative project funded by the Health Cooperation Work Programme of the 7th Framework programme (grant agreement No. 261357).
      The views expressed are those of the author (s). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

      Acknowledgements

      Born in Bradford is only possible because of the enthusiasm and commitment of the Children and Parents in BiB. We are grateful to all the participants, health professionals and researchers who have made Born in Bradford happen.

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