Asthma is a chronic disease of the airways that leads to breathing difficulty and sometimes death: the condition affects about 235 million people worldwide, especially children. Scientists still do not know exactly what causes asthma, but studies in Europe and North America suggest that individuals born or raised in rural areas are less likely to be affected. However, few studies have examined asthma in African countries, where urbanization is often quickly increasing. Examining the factors associated with the disease as more people move to cities may provide new clues about how asthma emerges, and how to prevent it.

To this end, Mpairwe et al. conducted a study with over 1,670 schoolchildren in Uganda. Those born or raised in rural areas were least likely to have asthma, but the risk doubled among children from small towns, and tripled in those born or who grew up in the city. Children whose parents had a higher education and socioeconomic status had the highest asthma risk, but more work is required to understand why this is the case.

The study by Mpairwe et al. is the first step towards identifying environmental and lifestyle factors associated with increased asthma risk in Africa. Further studies may help scientists to understand how beginning life in a more urban area plays a role in the development of the disease.

Asthma is estimated to affect more than 235 million people globally, and is the most common non-communicable condition among children (World Health Organisation, 2017). In Africa, the prevalence of asthma appears to be increasing (Asher et al., 2006; Addo-Yobo et al., 2007; van Gemert et al., 2011; Zar et al., 2007; Lawson et al., 2017), particularly in urban areas (Addo-Yobo et al., 2007; Morgan et al., 2018), but the causes of this increase are not fully understood. Moreover, asthma has various phenotypes which may have different aetiologies (Lötvall et al., 2011). Asthma risk factors appear to vary internationally, and to differ between high-income countries (HICs) and low-and-middle income countries (LMICs) (Douwes and Pearce, 2002).

There is little previously published data on asthma risk factors from Africa. The few studies reported have suggested that current residence in urban areas is associated with a higher risk of asthma than rural residence in Africa (Botha et al., 2019; Addo-Yobo et al., 2001) and other LMICs (Robinson et al., 2011; Gaviola et al., 2016). The association between helminth infections and asthma has been investigated in Africa and other LMICs, but the findings have been inconsistent across studies (Leonardi-Bee et al., 2006; Mpairwe and Amoah, 2019). Other risk factors for asthma in Africa and other LMICs, similar to those in HICs, include maternal smoking (Ayuk et al., 2018; Arrais et al., 2019), maternal history of asthma (Nantanda et al., 2013), childhood atopic sensitisation (Addo-Yobo et al., 2001; Nyembue et al., 2012) and history of allergy (Nantanda et al., 2013; Mehanna et al., 2018). Previous reports suggest no association between biomass fuels and asthma risk (Thacher et al., 2013; Oluwole et al., 2017a), but increased asthma symptoms (Oluwole et al., 2017a; Oluwole et al., 2017b). Unlike in HICs, higher parental education and socioeconomic status has been associated with asthma among children in Africa (Addo-Yobo et al., 2007; Nantanda et al., 2013; Wolff et al., 2012).

We undertook a case-control study among schoolchildren in an urban area in Uganda, to investigate the main risk factors for asthma and the patterns of allergic sensitisation.

We found a step-wise increase in asthma risk according to the child’s area of residence at the time of birth and in their first five years of life. Children born and raised in rural areas had the lowest risk, children born and raised in small towns had a 2-fold increase in risk, while children born and raised in the city had a 3-fold increase in asthma risk. This is the first study in Africa to show such a strong gradient in asthma risk by place of birth. Previous studies have been mostly cross-sectional and conducted in either rural or urban settings, and therefore focusing on current residence; these have shown that the prevalence of asthma is lower among rural residents compared to urban residents (Lawson et al., 2017; Morgan et al., 2018; Botha et al., 2019).

Our findings confirm that the area where a child is born (usually the same as the area where the mother was resident during pregnancy) is important for asthma risk. Indeed, we found that when children moved to other environments, they carried with them the asthma risk related to their area of residence in pregnancy: children born in urban areas who were subsequently raised in rural areas still had a 2-fold increase in asthma risk, similar to their counterparts born and raised in urban areas. These findings are comparable to observations from Europe showing that children born on a farm (usually in rural areas) have a lower risk of asthma in later life, even when they subsequently moved to urban areas (Leynaert et al., 2001), and that children who migrated to Europe after age five had a lower prevalence of asthma, similar to their country of origin, than children who were either born in Europe or migrated before the age of five (Migliore et al., 2007; Kuehni et al., 2007). However, there are also studies that show increased risk of wheezing and allergy among children following migration (Rodriguez et al., 2017; Stein et al., 2016). Unlike studies from Europe and North America which have reported a lower risk of asthma for children born or raised on farms (Genuneit, 2012; Timm et al., 2015), our study found no association between asthma risk and exposure to farm animals either during pregnancy or in early life. We hypothesise that this may be due to ubiquitous farm animal exposure due to subsistence farming, a widespread practice in Uganda, even in towns.

Our observation that children with asthma were more likely to have parents with tertiary education and to use gas or electricity for indoor cooking (as opposed to charcoal stoves) has been made by an earlier study in Uganda (Nantanda et al., 2013). Similarly, our finding that children with asthma reported the highest frequency of ‘trucks passing on the street near their home’ has been reported elsewhere (Sharma and Banga, 2007; Shirinde et al., 2014; Venn et al., 2005). We suggest that these factors are proxy measures of a higher socio-economic status of asthma cases and of urbanicity, consistent with findings from other LMICs that have found a higher prevalence of asthma among children (and adults) in urban than rural areas (Morgan et al., 2018; Robinson et al., 2011; Gaviola et al., 2016). However, our findings contradict those from HICs in which asthma is associated with lower parental education (Lewis et al., 2017) and socio-economic status (Akinbami et al., 2011). This suggests that there may be similarities in lifestyle and environmental factors between the highly educated and high socio-economic status families in LMICs with the low educated and low socio-economic status families in HICs, which increase asthma risk, and therefore require further investigation.

Although children with asthma were more likely to be sensitised to allergens than controls, the pattern of allergic sensitisation was similar among cases and controls; majorly sensitised to house-dust mites and cockroach, and least sensitised to peanut, cat, pollen and mould. This SPT response pattern was similar to other studies from Africa (Nyembue et al., 2012; Mbatchou Ngahane et al., 2016), but different from Europe where the main allergens are dust mite, cat and pollen (Bousquet et al., 2007).

Although maternal smoking is a known risk factor for childhood asthma (Silvestri et al., 2015), our study found no association between maternal smoking and asthma. We attribute this to the low prevalence of smoking in this population, by the mothers during pregnancy (2.5%) and by any household members currently (11%). The lack of association between asthma and indoor cooking with biomass fuels in this study is consistent with other studies from Africa (Thacher et al., 2013; Oluwole et al., 2017a). Indeed, this is consistent with the general pattern of lower risk of asthma in rural areas (where biomass fuel use is highest) than urban areas.

We found an inverse association between asthma and current infection with any helminths, particularly T. trichuria. However, the association between asthma and current infections in Africa has been inconsistent across studies (Mpairwe and Amoah, 2019). What was novel in this study is that we also collected data on history of using de-worming medication in the last 12 months. We found that children with asthma were more likely to have used de-worming medication more than twice in the last 12 months compared to controls, and this was de-worming with albendazole (for geo-helminths) not with praziquantel (for schistosomiasis). This implies that the inverse association we noted between asthma and helminths may be partly explained by increased de-worming among children with asthma. The current de-worming schedule in this age-group in Uganda includes mass-deworming in schools, bi-annually for albendazole and once a year for praziquantel. We did not establish whether the additional de-worming was self-medicated or prescribed by medical workers.

We found that children with asthma were less likely to have a BCG scar, but there was no association with tuberculin skin test at enrolment. In Uganda, BCG vaccination is routinely given at birth. A lack of BCG scar does not mean the vaccine was not administered, but may indicate differences in immune responses among children who will eventually develop asthma. Alternatively, BCG vaccination may be protective against asthma, as suggested by previous studies (El-Zein et al., 2010).

The other important risk factors for asthma, that have been previously described, included parental history of allergic disease (Lim et al., 2010), a child’s atopy status and concomitant other allergic disease (Bao et al., 2017). The strength of this study was to demonstrate that having a combination of any two of these known risk factors for asthma had an additive effect on asthma risk, and that this risk also increased in relation to area of residence in early life, with an increasing rural-town-city gradient. This gradient and independent effects of parental education provide strong evidence for the role of environmental and lifestyle factors associated with urbanisation that are responsible for the increasing asthma risk in urban areas. More investigations are required to identify the specific factors, in order to design interventions to modify them so as to prevent the establishment of asthma risk in early life.

This study had limitations inherent to all case-control studies, such as potential recall bias, selection bias and confounding. We minimised recall bias by focusing on major early life events that a parent was likely to remember. It was re-assuring to note a strong correlation between the recalled events and objective measures such as SPT. We minimised the selection bias for controls by randomly selecting controls from the same class register where the cases were obtained, and by randomly selecting the 400 participants for the asIgE assay. We minimised confounding by adjusting for measured confounders in all our analyses, but cannot rule out the possible role of unmeasured confounders. Finally, a large number of potential participants were not included in this study, mostly because they were in the boarding school section and were unable to contact their parents/guardians in time to attend the parents’ meeting (to provide consent). We do not have information on whether these parents were more likely to reside in rural areas or the city, where the asthma risk is either lower or higher than the town where this study was conducted, respectively. Our results may or may not be generalisable to similar urban areas in Uganda and Sub-sahara Africa.

Our findings support the concept that environmental factors during early life may influence the risk of development of NCDs in later life (Fleming et al., 2018). However, our study does not involve information sufficiently detailed to identify whether exposures in utero or in early life are most relevant. Further research in this setting is required to investigate these hypotheses, and this would have important implications for the life course approach in the prevention of asthma globally.

Data is available on request via https://datacompass.lshtm.ac.uk/1369/. To gain access to the data please complete the application process via the website. Requests will be reviewed and assessed by the corresponding author, in consultation with the LSHTM's Research Data Manager and relevant LSHTM staff members responsible for research governance and data protection. Applications will be evaluated on the basis of their compatibility with the study's research objectives and the ability to provide de-identified data sufficient to meet the intended purpose, without breaching participant confidentiality or the study's ethical and legal commitments. Successful applicants will be asked to sign a Data Transfer Agreement prior to being provided with the data.

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Author details

1. Harriet Mpairwe

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Conceptualization, Formal analysis, Funding acquisition, Investigation, Visualization, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   Harriet.Mpairwe@mrcuganda.org

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-1199-4859

2. Milly Namutebi

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

3. Gyaviira Nkurunungi

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-4062-9105

4. Pius Tumwesige

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

5. Irene Nambuya

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

6. Mike Mukasa

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

7. Caroline Onen

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

8. Marble Nnaluwooza

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

9. Barbara Apule

   Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

   Contribution

   Investigation, Writing—review and editing

   Competing interests

   No competing interests declared

10. Tonny Katongole

    Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

    Contribution

    Investigation, Writing—review and editing

    Competing interests

    No competing interests declared

11. Gloria Oduru

    Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

    Contribution

    Investigation, Writing—review and editing

    Competing interests

    No competing interests declared

12. Joseph Kahwa

    Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

    Contribution

    Data curation, Writing—review and editing

    Competing interests

    No competing interests declared

13. Emily L Webb

    London School of Hygiene and Tropical Medicine, London, United Kingdom

    Contribution

    Formal analysis, Writing—review and editing

    Competing interests

    No competing interests declared

14. Lawrence Lubyayi

    Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda

    Contribution

    Formal analysis, Writing—review and editing

    Competing interests

    No competing interests declared

15. Neil Pearce

    London School of Hygiene and Tropical Medicine, London, United Kingdom

    Contribution

    Supervision, Funding acquisition, Writing—review and editing

    Competing interests

    No competing interests declared

16. Alison M Elliott

    1. Medical Research Council/Uganda Virus Research Institute and London School of Hygiene and Tropical Medicine Uganda Research Unit, Entebbe, Uganda
    2. London School of Hygiene and Tropical Medicine, London, United Kingdom

    Contribution

    Conceptualization, Supervision, Funding acquisition, Writing—review and editing

    Competing interests

    No competing interests declared

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