This study sought to identify the most important risk factors for atopy from a variety of self-reported environmental and lifestyle exposures among children and adults residing in a rural community in Zimbabwe. The overall prevalence of atopic sensitisation was 31.17% with a higher prevalence among adults (33.33%) compared to children (23.53%) (p = 0.059). Self-reported nasal and skin allergies were more prevalent in adults than in children. The prevalence of allergic sensitisation in this study population was within the range (21.5–42.8%) of the prevalence of positive SPTs reported in studies from other African countries (Ghana, Uganda, Cameroon, and South Africa) that included children and adults from urban areas, rural areas or a combination of both communities (40–45).
Demographic and lifestyle characteristics
While there were no differences in age between atopic and non-atopic children, girls were significantly more likely to be atopic than boys (p = 0.04). Studies have reported that after puberty, girls seem to be at higher risk of developing atopic diseases than boys due to hormonal influences or sex-specific factors (46). Among adults, atopic individuals tended to be older than non-atopic individuals (p = 0.005), contrary to observations from studies in developed countries where atopy decreased with age (47). The likelihood of atopic sensitisation increased with increasing age among adults (OR = 1.02, 95%CI = 1.01–1.03). In addition to being older than the non-atopic adults, atopic adults were predominantly middle aged, with mean ages of 48.71 years (± 20.03 years) and 46.10 years (± 17.04 years) among men and women, respectively. There is relatively limited representation of middle-aged and advanced-aged individuals in the current body of work related to atopy and allergic diseases. Available data are mainly from studies in children, adolescents and young adults. As a steady increase in allergies has been noted in older adults and elderly individuals, future research should focus on this population group (48, 49). We also noted generational differences in demographic characteristics between the adults and children. For instance, adults were raised in larger families than were children, as reported by the significantly greater median number of siblings reported by adults (6, IQR = 4–8) than by children (4, IQR = 3–6) (p < 0.05). There is substantial epidemiological evidence for the sibling effect, indicating the inverse relationship between the number of siblings and the risk of allergic sensitisation and disease among adults and children in various developing countries (50). However, there was no evidence of such a relationship in this study population.
There were 77 (20.16%) adults who reported consuming a predominantly traditional diet when asked to recall and describe their childhood dietary habits. However, a follow-up question to describe the type of food consumed over the last 12 months revealed that dietary habits have changed to reflect a more modern or processed diet. None of the children and only 9 (2.36%) adults said they currently consume a predominantly traditional diet. Another Zimbabwean study similarly reported low levels of daily traditional food consumption (9.3%) among adults, and the reasons cited included weak value chains, difficult and time-consuming cooking procedures for some food types, misconceptions about quality and safety, and aggressive commercial advertising of modern foods (39). Modern diets, characterised by the intake of highly processed foods with high energy, high saturated fat, high protein, low fibre and low levels of vitamins and minerals, have been implicated in increasing susceptibility to allergic diseases (51). Subsequently, the protective effects of nutrients such as antioxidants, oligosaccharides, polyunsaturated fatty acids, folate and other vitamins are an area of increasing research interest as a strategy for the prevention of allergic diseases (52, 53). Alcohol also appeared to increase the likelihood of atopy among adults in this study (OR = 1.88, 95% CI = 0.93–3.78), a finding that has been reported in other studies in Europe and Asia (54, 55). Although variables related to diet were not significant enough for inclusion in the current multivariate analysis, the ongoing nutrition transition in Sub Saharan Africa will likely continue to influence the development of allergic diseases and other non-communicable diseases (NCDs) (56). In Zimbabwe, there is renewed interest in traditional foods due to their perceived health benefits (39). Leveraging this attention to traditional foods in Zimbabwe to promote their consumption and to address the current barriers to access may be an important intervention for allergic disease prevention and control. A study in rural Crete found that a high level of adherence to the Mediterranean diet had a beneficial effect on allergic rhinitis, asthma-like symptoms and atopy. They concluded that a diet high in antioxidants may prevent the expression of allergic diseases in this population (57). It is plausible that a typical traditional Southern African diet could offer similar levels of protection, as there is evidence, though sparse, indicating high levels of bioactive compounds in indigenous fruits (58) and leafy vegetables (59).
Air quality
The relationship between air quality and allergy has received considerable attention. Therefore, various sources of both indoor and outdoor air pollutants, known to be important risk factors for allergic diseases, were considered in this study (60). Reports of dampness and mould inside the home were common, and these variables were included in the final models for both adults and children. Although not statistically significant, dampness and mould, as measured by self-reported history of water damage or roof leakage and the presence of visible mould on walls, appeared to increase the risk of allergic sensitisation among both children and adults. Housing conditions in low-income communities, if not properly maintained, may encourage the proliferation of microorganisms due to dampness and inadequate ventilation (61). In addition, 83% of participants reported that they practice indoor cooking using firewood, further compromising the indoor air quality (62). In Zimbabwe, women and children in rural communities have been reported to be particularly vulnerable to air pollutants from biomass combustion (63).
With an overall prevalence of passive smoking of 47.54%, exposure to environmental tobacco smoke (ETS) was quite common in this study population. Among children, passive smoking almost doubled the odds of atopic sensitisation (OR = 1.93, 95% CI = 0.70–5.30). In adults, parental smoking increased the odds of atopic sensitisation (OR = 1.54, 95% CI = 0.95–2.50). Exposure to environmental tobacco smoke (ETS), particularly among children and adolescents, has been associated with asthma and allergic rhinitis and influences sensitisation to both food and aeroallergens (64–67). Our results support the existing body of evidence against tobacco smoke, further emphasising the need for tobacco control interventions in the community to minimise exposure.
Infectious diseases and atopy
We explored the relationship between infectious diseases and atopy due to reports of schistosomiasis-STH co-endemicity and high TB burden in Gwanda district (29, 36). A history of TB was reported by 34 (8.90%) adults and was also associated with atopic sensitisation among adults who had ever been employed (OR = 3.37, 95%CI = 1.08–10.52). There is evidence from observational studies of an inverse relationship between Mycobacterium tuberculosis infection and the presence of atopy or symptoms of allergic asthma (38, 68). This observation, however, is derived mostly from studies conducted in developed countries and among individuals with latent TB infection. On the other hand, our study participants had a previous history of active TB, which is immunologically different from latent infection (69). A study carried out in Peru to test whether a history of active TB was associated with atopy and allergic diseases found no evidence of a protective effect and concluded that the possibility of atopic disease in patients with a history of active tuberculosis could not be ignored (70).
Reports of history of bloody urine or schistosomiasis were also significantly more common in adults 32(8.38%) than in children 2(1.85%). Adults reporting a history of bloody urine or schistosomiasis were twice as likely to be sensitised to at least one allergen compared to those who did not (p = 0.056). Furthermore, a history of bloody urine or schistosomiasis diagnosis was an even more influential risk factor for atopy among adults who had previously been employed (OR = 4.36, 95% CI = 1.40-13.65). Although a history of helminth infection was positively associated with atopy in our study, there is conflicting epidemiological evidence for this relationship, which has been attributed to the genetic susceptibility of the host and type of parasite as well as the timing, duration and intensity of infection (71–75). A recent meta-analysis, which included 80 studies, revealed that Ascaris lumbricoides infections were associated with an increased risk of atopy among helminth-infected adults (76). According to a study of newly arrived Ethiopian immigrants to Israel, a greater incidence of SPT positivity was observed after one year of follow-up in individuals who either remained infected (with lower intensity) or became infection free after treatment than in individuals with no evidence of infection (p = 0.045). Their conclusion that a changing burden of helminth infection coupled with exposure to new environmental factors might increase the likelihood of allergic sensitisation is a reasonable explanation for our findings (37). Another explanation we considered was the possibility of cross-reactivity between allergen extracts from mopane worms, mites and cockroaches and helminth antigens due to the presence of proteins such as tropomyosin and myosin (77). These findings further highlight the potential challenges in allergy diagnosis that may need to be addressed in areas endemic for infectious diseases.
Occupational exposures
Adults with work experience reported a wide range of occupations, such as artisanal mining, domestic work, farming, cross-border trading and construction. A number of these occupations have been documented to offer very little protection from harmful exposures and to contribute to the growing burden of environmental pollution in African communities (45). This includes uncontrolled or unregulated exposure to many irritant pollutants, such as dust, smoke and pesticides (24, 78). The risk and intensity of exposure to these harmful factors among different vulnerable population groups continue to increase due to the lack of clear regulatory policies, particularly in informal occupational settings (79, 80). The most frequently reported occupation in this study was artisanal mining 37(24.34%). This was expected since mining is a major economic activity in Gwanda district because of the substantial mineral reserves (30). An increase in artisanal and small-scale miners in the area has had a significant negative effect on the environment and health of residents in the mining areas (30, 31). Having considered the potential vulnerability of this group, we carried out additional analysis to identify possible predictors of atopic sensitisation in the subpopulation of adults who reported having an occupation outside of the home in their lifetime. A history of TB and helminth infection were the most influential factors for atopy in this group. Infection with helminths and Mycobacterium tuberculosis in occupational settings is common in Zimbabwe and other sub-Saharan African countries (81–83). While infections have been found to have a protective effect according to the hygiene hypothesis, it seems that the environmental factors described in the Anthropocene might be more influential in promoting the development of atopy and allergic diseases in the presence of these infectious agents. In rural African communities, a steady increase in asthma and atopy has been observed despite the presence of protective factors associated with a rural lifestyle (84).
Strengths and limitations
A particular methodological strength of this study was the use of skin prick testing for the assessment of atopic sensitisation, for which the response rate was fairly high (93.15%). Additionally, a wide range of environmental exposures found in both childhood and adulthood were investigated using a collection of carefully selected questions that were a reflection of the study area’s environmental characteristics. A number of the factors reported, such as passive smoking, dampness and the presence of mould, are potentially modifiable; hence, these findings may be considered in the design and implementation of early public health interventions to prevent and control allergic diseases in the community. Nonetheless, our study is limited by its reliance on self-reports to collect environmental exposure information, which increases the vulnerability of the sample to recall bias. Every effort was made to ensure that most of the questions were extracted from validated questionnaires (34, 35, 85) and were sufficiently appropriate for children to minimise recall bias. In the questionnaire, we did not probe further about the duration of employment or the specific occupational exposures, thereby inherently introducing information bias. The use of non-probability sampling in the recruitment of participants could weaken the study as it potentially limits the generalizability of the study findings. This sampling approach was inevitable, as previously described in the feasibility study (13). Considering the ubiquitous nature of the environmental factors of interest in this study, we believe that the recruited participants provided a representative account of the community characteristics.