Asthma in South African adolescents: a time trend and risk factor analysis over two decades

Discussion

This study is amongst the first globally to use the GAN methodology to investigate changes in asthma prevalence in adolescents in a LMIC over an extended period. A key finding was the increasing prevalence of severe asthma. While asthma prevalence did not change substantially over this period on the written questionnaire, all measures of symptoms of severity increased on the written and video questionnaires. The proportion of children diagnosed with asthma increased, but only a third of those with current or severe symptoms had been diagnosed with asthma. Key environmental exposures associated with asthma or with severe disease were outdoor pollution, participant smoking, pets and poor housing.

The rising prevalence and severity of asthma from 1995 to 2002 has previously been reported amongst adolescents from the same area [9]. These trends were consistent with ISAAC data from other African countries, such as Kenya and Nigeria, which showed an increasing prevalence of asthma compared to a stabilising or decreasing trend in some higher-income countries [5]. In addition, bronchial hyper-responsiveness studies have shown comparable increases in asthma prevalence amongst rural and urban South African children from 1979 and through to 2020 [17–21]. The current study extends these findings by showing a striking increase in disease severity across all measures.

Several factors may account for the greater severity of asthma. Poor living conditions was a key risk factor, as was self-reported smoking, pet ownership and outdoor pollution. Consistent with ISAAC III data from Cape Town, children from higher SES backgrounds (as measured by parental employment or private schooling) had a higher risk of current asthma; however, asthma severity was higher amongst those from a lower SES [22]. In another South African study using self-reported questionnaires amongst 6002 children from both rural and urban settings to investigate socioeconomic risk factors for childhood asthma, asthma severity increased with socioeconomic deprivation [23]. This association may be attributable to both the inequitable distribution of health care, poor access to diagnosis and care and environmental factors, such as increased exposure to indoor pollution and smoking [22, 23].

Self-reported smoking was an important risk factor, with almost 9% of participants self-reporting smoking at a relatively young age. While self-reported smoking is an imperfect measure, this probably represents the lowest estimate of adolescents who are currently smoking in this population. Exposure to tobacco smoke is a well-established risk factor for asthma [10, 24, 25]. Amongst 6–7-year-old children from a different part of South Africa, exposure to tobacco smoke increased the likelihood of wheeze by 77% [10]. South Africa's Tobacco Products Control Amendment Act (2008) prohibits children younger than 18 years from smoking, regulates the advertisement of cigarettes and cigarette tax, and makes designated smoking areas a legal requirement [26]. Our data suggest the need for more effective enforcement of this legislature as well as improved educational programmes aimed at children and adolescents, to prevent initiation of smoking and to strengthen smoking cessation initiatives for school-going children.

Outdoor pollution, as measured by frequency of trucks passing by the respondent's home, was associated with an increased risk of severe asthma. Outdoor pollution is a well-established risk factor for current and severe asthma [27]. However, data from Sub-Saharan Africa on the strength of the association are limited, with only a few recent studies describing an association between air pollution and wheeze in this region [27, 28]. With increasing industrialisation, levels of pollution are expected to continue to rise, particularly in urban areas [27]. Further research is therefore needed to accurately describe this relationship in LMICs such as South Africa, and to promote strategies to reduce exposure.

Consistent with ISAAC and other global data, female sex was found to be a significant risk factor for current wheeze amongst adolescents [4, 29, 30]. In pre-pubertal children the prevalence and severity of asthma is higher amongst males. The switch in asthma prevalence at the onset of puberty may be related to the effects of female sex hormones on airway inflammation and hyper-reactivity. Other factors thought to contribute to the gender differences in asthma prevalence include differences in airway growth and function between sexes, a tendency for girls to over-report asthma symptoms, as well as differences in environmental exposures, such as smoking [29, 30].

Lack of asthma diagnosis for adolescents with asthma or with severe disease was common, with two-thirds of cases undiagnosed. This proportion has remained relatively unchanged over this period; in ISAAC III, undiagnosed asthma was most common in African countries, with 40% of children undiagnosed [9, 31]. The results from our study suggest that ongoing underdiagnosis and undertreatment of childhood asthma remains a key concern. This may be particularly challenging in LMICs, where access to care may be limited, and illnesses such as lower respiratory infections are more likely to be diagnosed [8]. Adolescents may also deny symptoms and underestimate the severity of disease [30]. Improved access to primary health care for diagnosis and affordable essential asthma medication, including inhaled corticosteroids or short-acting beta agonists, can reduce hospitalisations, mortality and costs [32, 33]. Our data highlight the need for urgent public healthcare interventions to address underdiagnosis in these settings.

A limitation of the study is the lack of generalisability to rural areas; however, the study is relevant to peri-urban and urbanising landscapes of LMICs [17, 18]. Further, the study was done in Cape Town, an urban area of South Africa, the same area in which ISAAC phase I and III were done. However, South Africa has experienced profound social and economic changes over this period, with increased urbanisation and increased numbers of people living in informal homes [34–36]. An estimated 53% of the population resided in urban or peri-urban areas in 1994 compared to 78% in 2013 [37, 38]. A further limitation is reliance on self-reported symptoms as a proxy for disease, rather than a confirmed diagnosis or lung function testing. Self-report may over- or underdiagnose asthma symptoms [39]. However, the ISAAC self-report methodology has been widely used globally and validated against physician assessments [14, 40]. Furthermore, the use of identical methodology at all three time points makes a valid comparison over time possible [9].

Although questionnaires have been translated and the study was conducted in the language appropriate for each individual, the translations may be limited in their ability to capture the scope of disease as the interpretation of terms such as “wheezing” and “asthma” may not be specific enough in each language. However, the video questionnaire was used to obviate any language issues. Both the video and the written questionnaires confirmed an increase in severe asthma while the prevalence of asthma, as measured by wheeze in the last 12 months, was remarkably consistent between the two (21.3% on the written and 18.7% on the video questionnaire). Further, these adolescents are all school-going, with a relatively high level of literacy. Lastly, the same questionnaires were used in ISAAC and in GAN, making comparison of responses valid.

The study highlights the emerging undiagnosed and increasing burden of asthma, including severe asthma, which is the commonest non-communicable disease in adolescents in LMICs. The key environmental factors associated with disease and disease severity, including smoking, poor housing and poverty, are amenable to public health interventions. Further study of the determinants of disease and long-term impact is needed in LMIC settings. Strategies to improve asthma diagnosis and management in these settings must be strengthened.