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Background: In high-income countries, allergy-related diseases (ARDs) follow a typical sequence, the ‘Atopic March’. Little is known about the life-course of ARDs in the markedly different, low-income, tropical environment. We describe ARDs in a tropical, African birth cohort. Methods: Ugandan children were followed from birth to 9 years. ISAAC questionnaires were completed at intervals; doctor-diagnosed ARDs were recorded throughout follow-up. Skin prick tests (SPTs) were performed at 3 and 9 years. Atopy was defined as ≥1 positive SPT. Results: Of the 2345 live-born children, 1214 (52%) were seen at 9 years. Wheeze and eczema were common in infancy, but by 9 years, only 4% reported recent wheeze, 5% eczema and 5% rhinitis. Between 3 and 9 years, atopy prevalence increased from 19% to 25%. Atopy at 3 or 9 years was associated with reported ARD events at 9 years, for example OR = 5.2 (95% CI 2.9–10.7) for atopy and recent wheeze at 9 years. Reported or doctor-diagnosed ARD events in early childhood were associated with the same events in later childhood, for example OR = 4.4 (2.3–8.4) for the association between reported wheeze before 3 years with reported recent wheeze at 9 years, but progression from early eczema to later rhinitis or asthma was not observed. Conclusion: Allergen sensitization started early in childhood and increased with age. Eczema and wheeze were common in infancy and declined with age. Atopy was strongly associated with ARD among the few affected children. The typical Atopic March did not occur. Environmental exposures during childhood may dissociate atopy and ARD.
The EMaBS is based in Entebbe municipality and Katabi subcounty, Wakiso district, Uganda: a peninsula on Lake Victoria, comprising urban, rural and fishing communities. Between 2003 and 2005, pregnant women were recruited into a randomized, double‐blind, placebo‐controlled trial of anthelminthic treatment in pregnancy and early childhood, and followed up as previously described [ISRCTN32849447] 9. The Research and Ethics Committee of the Uganda Virus Research Institute, the Uganda National Council for Science and Technology, and the London School of Hygiene and Tropical Medicine granted ethical approval. At ages 1, 2, 3, 5 and 9 years, caregivers were interviewed (in the child’s presence) on ARD symptoms using questions from the International Study on Allergy and Asthma in Children (ISAAC) questionnaire 15 and data on urticaria were also collected. For data collected at age 3 years, these questions were included in the questionnaire from November 2007 onwards; hence, only responses from children attending their age 3 visit from that date onwards were collected. Reported recent events were wheeze, eczema (a recurrent pruritic rash with typical infant or child distribution), allergic rhinitis (sneezing or runny nose or blocked nose, with itchy and watery eyes, without having a cold or ‘flu’) and urticaria (pruritic rash with wheals, ‘ebilogologo’ in the vernacular), occurring in the preceding 12 months. At 9 years, the questionnaire was supplemented with (i) the ISAAC video questionnaire (VQ; shown after the oral questionnaire [OQ]), and (ii) questions from the UK diagnostic criteria (UKDC) for atopic eczema 15. The VQ contained five short sequences of asthma symptoms (audible wheezing without breathlessness, exercise‐induced wheezing, waking at night with breathlessness, nocturnal coughing, a severe asthma attack). Each sequence was followed by questions asking whether the child’s breathing had ‘ever’ or ‘in the last 12 months’ been like the person’s in the video. Children were examined for visible flexural dermatitis by team members trained in the standardized approach 16. The UKDC defines eczema as a recent pruritic rash with at least three of the following: history of flexural involvement, history of generally dry skin, personal history of asthma or allergic rhinitis, visible flexural dermatitis and onset below age 2 years. Doctor‐diagnosed ARD events were identified when sick children presented to the study clinic. Wheezing episodes below the age of 5 years were documented. Asthma was diagnosed after the age of 5 years as an episode of wheezing or, a dry nocturnal cough, with a previous asthma‐like episode, after excluding other possible causes. Eczema was a recurrent pruritic rash lasting more than 6 months, with typical infant or child distributions. Skin prick testing was performed in a subset of three‐year‐olds (those who attained 3 years of age from November 2007 onwards, when SPT was added to the procedures performed at this visit) and in nine‐year‐olds, on the volar surface of the arm using standard methods 17 with allergens likely to elicit a response in this setting 18. At 3 years 12, dust mites (Dermatophagoides, Blomia tropicalis), cow’s milk and egg white were used; and at 9 years, the dust mites, German cockroach (Blattella germanica), peanut, Bermuda grass, cat, pollen and mould were used (ALK‐Abelló, Laboratory Specialities (Pty) Ltd, Randburg, South Africa). Wheals were measured after 15 min, positive being a mean diameter ≥3 mm. The primary definition of atopy was SPT positivity to at least one allergen (further categorized as monosensitivity [sensitive to one allergen] and polysensitivity [≥2 allergens]). At 9 years, plasma stored at −80°C was assessed for Dermatophagoides‐specific (Der‐p) IgE response using an in‐house ELISA as previously described 13. The lower detection limit was 312 ng/ml. A secondary definition of atopy was detectable Der‐p IgE >312 ng/ml. Data were double‐entered in Microsoft Access and analysed with Stata 14 (College Station, TX, USA). Chi‐square tests were used to compare maternal baseline (age, education, marital status, any worm infection, body mass index, anaemia) and child (sex, atopy at 3 years and infantile eczema diagnosis) characteristics between children seen and not seen at age 9 years. Agreement between OQ and VQ was determined by kappa statistic (κ) 19. Cross‐sectional associations between atopy and reported recent ARD events at 9 years were estimated using logistic regression and population‐attributable fraction (PAF) calculated. Longitudinal inter‐relationships between atopy or reported ARDs in the first 3 years of life (reported ARD event at 1, 2 or 3 years) and atopy or reported ARDs at 9 years were examined using logistic regression. Poisson regression with random effects was used to assess whether reported ARDs or doctor‐diagnosed ARD events in early childhood (0–5 years) or atopy at 3 years were associated with doctor‐diagnosed ARD events between 5 and 9 years.
