Original article

Risk factors for asthma among children in Maputo (Mozambique)

Asthma is the most common chronic pulmonary diseaseof children (1, 2). Its severity ranges from intermittentasthma to severe persistent asthma (1). The prevalence ofasthma and allergies in general has considerably increasedover the last two decades, particularly among children(1). The prevalence of asthma worldwide is very variable.For example, in 6- and 7-year olds the prevalence ofwheezing is 4.1% in Indonesia and 32.1% in Costa Rica(3). In Brazil, the prevalence of asthma is 7.3% in boysand 4.9% in girls aged 6 or 7 years and 9.8% and 10.2%in 13–14-year olds (4). There have been fewer studiesestimating the prevalence of asthma in Africa than inother continents. Although the prevalence of asthma islower in Africa, it has increased over the last few years(5, 6). The available data concern exercise-inducedasthma, the prevalence of which is between 5 and10.5% in school-aged African children (7–9). The preval-ence of wheezing in the previous 12 months is higher,between 10 and 18.2% (10–12).

The causes of asthma and the reasons for its increasingprevalence are not fully understood (13). Few studieshave looked at the role of risk factors for asthma inpopulations of African children (5, 10, 14, 15). It has notbeen demonstrated that the risk factors are identicalto those in Western countries, or that their relativeimportance is the same. Indeed, the available evidence

tends to indicate the converse for some environmentalelements (5). No studies have been carried out inMozambique. The capital of Mozambique, Maputo, hasa population of about one million inhabitants (16). Theclimate is tropical with a very hot and dry season betweenDecember and March. In 1999, asthma was the secondmost common cause of hospitalization, after infectiouspulmonary diseases, in the Pediatric Pneumology Depart-ment of Maputo Central Hospital.

The identification of risk factors is essential for theadaptation of preventive measures and the optimizationof asthma patient management. We aimed to identify therisk factors associated with asthma in children recruitedfrom the Pediatrics Department of Maputo CentralHospital.

Patients and methods

This case–control study included 199 age-matched children whoattended the Pediatrics Department of Maputo Central Hospitalbetween January 1999 and July 2000. The patient group comprised100 asthmatic children and the control group, 99 nonasthmaticchildren.

The inclusion criteria for the patients were: (i) medically diag-nosed asthma based on clinical history, physical examination, achest X-ray and the improvement of symptoms on treatment with

Background: Few studies have looked at risk factors for asthma in Africanchildren. We aimed to identify the risk factors associated with childhood asthmain Maputo (Mozambique).Methods: This case–control study included 199 age-matched children (100asthmatic and 99 nonasthmatic) who attended Maputo Central Hospitalbetween January 1999 and July 2000. We collected information concerningtheir familial history of atopy, birth weight, environment and breast-feeding.Detailed information about morbidity and treatment was obtained for eachasthmatic child.Results: The children were aged between 18 months and 8 years; 60% were male.The asthmatic children were hospitalized more frequently than the nonasthmaticchildren (P < 0.0001). Most of the asthmatic children lived in the urban area ofMaputo [odd ratio (OR) ¼ 6.73, CI ¼ 3.1–14.0, P < 0.0001], had a parentalhistory of asthma (OR ¼ 26.8, CI ¼ 10.8–68.2, P < 0.0001) or rhinitis(OR ¼ 4, CI ¼ 1.2–13.3, P ¼ 0.005), had at least parent who smoked and wereweaned earlier than the nonasthmatic children (OR ¼ 2.4, CI ¼ 1.3–4.4,P < 0.001).Conclusion: Childhood asthma was strongly associated with a family history ofasthma and rhinitis, the place of residence, having smokers as parents and earlyweaning from maternal breast milk. These results highlight the need to reassessthe management of asthmatic children in Maputo.

S. Mavale-Manuel1, F. Alexandre1,N. Duarte1, O. Albuquerque1,P. Scheinmann2, A. S. Poisson-Salomon2, J. de Blic21Department of Pediatrics, Maputo Central Hospital,Maputo, Mozambique; 2Service de Pneumologie etd'Allergologie P!diatriques, H"pital Necker, EnfantsMalades, Paris, France

Key words: asthma/epidemiology; child; environmentalexposure; Mozambique/epidemiology; risk factors.

Prof. Jacques de BlicService de Pneumologie etd'Allergologie P!diatriquesH"pital Necker-Enfants Malades149, rue de s4vres 75743Paris Cedex 15France

Accepted for publication 23 June 2003

Allergy 2004: 59: 388–393Printed in UK. All rights reserved

Copyright � Blackwell Munksgaard 2004

ALLERGY

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b2-mimetics; (ii) age between 18 months and 8 years; (iii) at leasttwo previous episodes of wheezing.

The controls were children of the same age, who attended thePediatrics Department of the hospital immediately after selection ofthe index case. The inclusion criteria for the controls were: (i) havingthe same age (±3 months) as the corresponding patient; (ii) absenceof respiratory disease; (iii) no previous episodes of wheezing. Oncethey had given consent for participation in the study, the parents wereasked to complete a questionnaire in Portuguese (the official languageof Mozambique). If the parents experienced difficulty in completingthis questionnaire, they were interviewed in their mother tongue andthe questionnaire was completed by a member of our team. We col-lected information concerning familial history of atopy, birth weight,current weight and height, environment (external and domesticpollution) and history of breast-feeding. Detailed informationabout morbidity (circumstances in which asthma attacks occurred,clinical signs, hospitalization) and management (treatments received,medical follow-up) was obtained for each asthmatic child.

Statistical analysis

We used Pearson’s chi-squared test or Fisher’s exact test to comparequalitative variables. A Wilcoxon test was used to analyze quanti-tative variables. Differences were considered to be significant ifP £ 0.05. The strength of the relationship between risk factors andasthma was evaluated by calculating odds ratios (OR) and theirconfidence intervals (CI) for all the factors tested. We did not usemultivariate analysis because of the low frequency of some of therisk factors in the study population.

The data were analyzed with Epi-Info 2000 version 1.1.2. software1 .

Results

Clinical characteristics of the patients

We studied a total of 199 patients: 100 asthmatic childrenand 99 nonasthmatic children. The children were agedbetween 18 months and 8 years [mean age ¼ 40.9 ±18.7 months for the asthmatic children and 41.1 ± 18.9

for the control group, median ¼ 37 months, range 26–50.52 , not significant (NS)]. Sixty percent of the childrenwere boys and 40% were girls. Of the asthmatic children,7.7% weighed less than 2500 g at birth, vs only 12.6% ofthe control children (NS). Only 41.1% of the childrenattended regular medical consultations for their asthma.At the time of the study, 56% of parents stated thattheir children used anti-asthma treatment as needed.The following drugs were used (in descending order offrequency): theophylline (43%), oral salbutamol (22%),traditional medicines (8%), prednisolone (4%), andketotifen (1%). Asthmatic children were hospitalizedmore frequently than the other children (mean 1.7 and 0.6respectively; P < 0.0001). For asthmatic children, themean number of previous hospitalizations was 1.3 (range0–9). None of the children was on long-term treatment.

Environmental risk factors (external and domestic pollution)

We found a significant relationship between place of birthand asthma (OR ¼ 3.3, CI ¼ 1.0–12.2, P < 0.05) andbetween place of residence and asthma (OR ¼ 6.73,CI ¼ 3.1–12, P < 0.0001). Just over half (51%) theasthmatic children, but only 13.4% of the control children,lived in inner city areas. Just over a quarter (28%) of theasthmatic children, but only 16% of nonasthmaticchildren, lived in homes with at least one carpet (OR ¼ 2,CI ¼ 0.9–4.4,P ¼ 0.06). The relationship between asthmaand maternal smoking or paternal smoking consideredseparately was at the limit of statistical significance(P ¼ 0.06). However, the link between asthma and thepresence of a smoker in the child’s home (mother, father, orboth)was significant (OR ¼ 2.2, CI ¼ 1.1–4.3,P < 0.05).The frequency of animals, notably cats and dogs, at homewas very similar for the two groups (Table 1).

Table 1. Risk factors associated with asthma

Factor Asthmatic children (%; n ¼ 100) Control group (%; n ¼ 99) P Odds ratio (95% CI)

Genetic susceptibility factorParental asthma 71 15 <0.0001 26.8 (10.8–68.2)Parental rhinitis 17 5 <0.01 4 (1.2–13.3)Parental atopic dermatitis 5 1 NS –

External pollutionBorn in inner city 93 85 <0.05 3.3 (1.0–12.2)Resident in inner city 50 13 <0.0001 6.7 (3.1–14.6)Conventional building/house 87 59 <0.0001 5 (2.3–11.1)

Domestic pollutionCarpets at home 25 15 NS 2 (0.9–4.4)Animals at home 26 28 NS 0.9 (0.4–1.8)Maternal smoking 9 3 0.06 3.2 (0.76–15.4)Paternal smoking 32 20 0.06 1.86 (0.93–3.73)Parental smoking 37 21 <0.05 2.2 (1.1–4.3)

Dietary factorsWeaning before 18 months 61 39 <0.01 2.4 (1.3–4.4)

NS, not significant.

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Genetic susceptibility factors

Asthmatic children were more likely to have a familyhistory of atopy. Asthmatic children were much morelikely to have a parental history of asthma (OR ¼ 26.8,CI ¼ 10.8–68.2, P < 0.0001) and rhinitis (OR ¼ 4,CI ¼ 1.2–13.3, P ¼ 0.005). The frequency of atopicdermatitis did not differ between the parents of the twogroups of children (Table 1).

Dietary factors

Of the asthmatic children, 61% were weaned before18 months of age (median ¼ 16 months, range 8–20), vs39%of the children in the control group (20 months, range15–24) (OR ¼ 2.4, CI ¼ 1.3–4.4, P < 0.01; Table 1).

Relationship between risk factors and hospitalization for asthma

The frequency of each of the risk factors was similar inchildren who had never been hospitalized and in thosewho had been hospitalized at least once before. Assumingthat children who are repeatedly hospitalized have moresevere asthma, this would imply that there is no linkbetween the severity of the disease and the risk factors.

Discussion

In this study population, there was a strong associationbetween childhood asthma and, in descending order ofimportance, having a family history of asthma andrhinitis, place of birth, living in an urban area, smokingby other family members and early weaning frommaternal breast milk. The role of the domestic environ-ment did not seem to be a major risk factor.

We recruited patients from a hospital, which may haveresulted in selection bias in favor of a more severelyaffected population. Patients only attend the hospitalwhen an attack continues or if there are serious clinicalrepercussions. However, there is no evidence that theassociation between asthma and any given risk factor islinked to asthma severity. Consequently, studying ahospital-based sample is unlikely to introduce significantbias into the analysis of associations between a givenfactor and disease. One of the limitations of our study isthe absence of an allergological study: no such study wasconducted because of practical difficulties. It was there-fore not possible to investigate in detail the relationshipbetween asthma and certain allergens specific to thelifestyle considered.

Genetic susceptibility factors are the main risk factors

Several studies have reported an association betweenchildhood asthma and parental asthma (5, 7, 17, 18). Ourresults confirm this finding. Maternal asthma is the main

risk factor for the development of persistent sensitizationin the child, which in turn increases the risk of asthma(18). Thus, asthma is at least partly caused by theinteraction between genetic susceptibility and exposure toallergens (19, 20).

The important role of environmental factors

Environmental factors are increasingly being implicatedin asthma (3, 14, 21–23). In Africa, asthma is morecommon in children who live in urban areas than in thosewho live in rural areas (5, 7–9, 24). Our results areconsistent with this finding. In contrast to what isobserved in rural areas, wheezing and exercise-inducedbronchospasm are closely linked to atopic sensitization inurban zones, as in Western countries (25). Children wholive on farms are protected against the development ofasthma and atopic diseases, probably by bacterial endo-toxins (18, 26). The role of place of residence, andtherefore lifestyle, is illustrated by the doubling or triplingof the prevalence of respiratory symptoms in childrenwho immigrated to Australia 5–14 years ago from coun-tries in which the prevalence of asthma is low (27).

Exposure to tobacco is a risk factor that is clearlyassociated with the development of asthma in the first fewyears of life (14, 19, 28, 29), by favoring persistentsensitization (18). This risk is higher in the case ofmaternal smoking, especially if the mother smokes duringpregnancy. In our study, this risk factor was found toplay a minor role. The association between asthma andpaternal or maternal smoking considered separately wasweak, at the limit of significance, due to a lack of power.By taking into account all the possible combinationscorresponding to ‘parental smoking’ (mother only, fatheronly, or both), we were able to show that the presence ofa smoker in the child’s immediate family was significantlyassociated with asthma.

The relationship between asthma and the presence ofcarpets in the home was at the limit of statisticalsignificance (P ¼ 0.06). This is consistent with the resultsof studies on Western populations. Children sensitized atleast once in their first 3 years of life were found to havebeen exposed to significantly higher levels of dust miteallergen (18). Although exposure to indoor allergens isassociated with atopic sensitization to specific allergen, nolink with asthma was found (18). In most studies,sensitization to dust mites has been shown to increasethe risk of wheezing. Sensitization to dust mites isbecoming increasingly common among African asthmat-ics (Table 2). For example, in Ghana, asthmaticchildren are most frequently sensitized to dust mitesand cockroaches (5). In Kenyan children living in theurban area of Thika, the prevalence of atopy, particularlysensitization to dust mites, is significantly associatedwith exercise-induced bronchospasm (25). Palmer et al.performed a transverse study of 2164 children agedbetween 8 and 18 years and found that moderate

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infection with Ascaris lumbricoides was associated with anincreased risk of asthma, sensitization to pneumallergensand bronchial hyperreactivity to methacholine (30).Conversely, bacterial and viral infection during earlychildhood (18, 31) and chronic parasitic infection (4, 32)can reduce the risk of atopy and allergic diseases inchildren. In Ethiopia, sensitization to dust mites, withoutrespiratory symptoms, has been shown to be correlatedwith higher parasite density (33). Children living inMaputo city probably have fewer parasitic infection thanthose living in suburban areas. Given the frequency ofsuch infections in children living in Mozambique, itwould be interesting to carry out prospective studies thereto try to improve our understanding of this phenomenon.The presence of animals in the home does not seem to bea major risk factor for asthma in Africa, perhaps becausedomestic animals are less confined in the house (5). Ourresults confirm those of other African studies (5, 11, 12,14, 34).

The protective role of prolonged breast feeding

The relationship between breast feeding and asthmais unclear. The Tucson’s sturdy showed that therelationship between breast-feeding and repeated wheez-ing or asthma differs according to age, the presence orabsence of maternal asthma and the presence or absenceof atopy in the child. Thus, breast-feeding protected

against recurrent wheezing before the age of 2 years buthad the opposite effect in children over the age of 6 years,especially in those genetically at risk (35, 36). Accordingto Sears et al., breast-feeding does not protect childrenagainst atopy and asthma and may even increase the risk(37). Conversely, according to Haby et al. (13), breast-feeding reduces the risk of asthma in young children,regardless of its duration. In Australian children, exclu-sive breast-feeding for longer than four months wasfound to protect against asthma, wheezing and atopy(38). In Mozambique, the prevalence of breast-feeding isvery high (94.8%), and is highest in rural areas. Thenational mean duration of breast-feeding is 22.4 months(16). All of the children included in this study werebreastfed. However, the asthmatic children were weanedsignificantly earlier than the others.

Conclusion

Our results show that familial atopic background, placeof residence, passive smoking and early weaning areimportant risk factors for childhood asthma in Maputo.Some of the factors identified in various studies carriedout in Africa are consistent with the notion that thereis a relationship between asthma and ‘westernization’(domestic comfort, confinement, smoking among familymembers) (8, 34). Further studies are required to evaluate

Table 2. Summary of recent studies on the risk factors for asthma among African children

Reference Country Type of study N Age (y) Risk factor OR (95% CI)

Addo-Yobo 2001 (5) Ghana Case–control 50/50 9–16 Urban area 4.8 (1.5–5.2)Sensitization to dust mites 10.4 (3.5–30.9)Sensitization to cockroaches 4.9 (1.3–18.6)Order <5 in the family 6.3 (1.3–29.4)Domestic animals NS

Faniran 1999 (10) Nigeria Case–control 566 8–11 Sensitization to dust mites 2.4 (1.3–4.3)

Nriagu 1999 (11) South Africa Transverse 367 <17 Humidity NSCarpets NSDomestic animals NSUse of pesticides NS

Elrlich 1996 (14) South Africa Case–control 368/294 7–9 Hayfever 5.3 (3.1–8.8)Eczema 2.19 (1.3–3.6)Parental asthma 1.77 (1.1–2.8)Lack of paternal income 1.72 (1.1–2.5)Smoking in pregnancy 1.87 (1.2–8.1)Smoking in family 1.15 (1.0–1.3)Humidity/molds 1.48 (1.04–2.11)

Mohamed 1995 (15) Kenya Case–control 77/77 9–11 Humidity 4.9 (2.0–11.7)Domestic pollution 2.5 (2.0–6.4)Bedroom carpet 3.6 (1.5–8.5)

Fagbule 1994 (34) Nigeria Case–control 140/140 66 M Humidity 11.2; P < 0.001Domestic animals 116.8; P < 0.001Smoking in family 2.1; P < 0.01Mosquito coil 3.7; P < 0.001

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the precise role of the environment, parasitic infectionand atopic sensitization in particular. It would also beinteresting to compare these results with those obtained in

a population of asthmatic children with intermittent ormild persistent asthma, seen outside the hospital envi-ronment or during consultations.

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