Use of Biomass Fuel in Households Within Limpopo Province of South Africaand Its Association with Asthma Among School Children Aged Thirteen and Fourteen Years of Age

Biomass fuel is energy generated from burnt coal, wood, paraffin, dried animal dung and other agricultural waste. Each one of these energy sources when burnt produces unique toxic substances, some of which the Environmental Protection Agency lists as criteria pollutants. Singly or in combination these substances are associated with asthma. In this study 742 children aged 13and 14 years taken from 10 schools in 5 education districts in areas around the City of Polok- wane were investigated to determine the association of biomass fuel and asthma. A cross sectional study design was used to test the association. The prevalence of asthma among the exposed group was 33%. The odds ratio for the exposed and un- exposed was 1.50, p < 0.001, C.I. 1.34, 4.98.Meaning the exposed group was 1.50 times more at risk of asthma. Testing for potential confounders showed that use of biomass fuel remained resilient in predicting asthma. The study suggests that complete electrification of areas in Limpopo Province to prevent use of alternative unclean energy sources, can help reduce exposure to energy-related asthma agents. For purposes of control, asthma should be made a priority disease; and that an asthma surveillance system is established in Limpopo Province.


Introduction
This study investigatedthe association of asthma and use of biomass fuel in a sample of 742 children drawn from ten schools in five education districts in the province of Limpopo in South Africa.
The National Heart, Lung and Blood Institute [1] defines Asthma as 'a chronic inflammatory disorder of the airways in which many cells and cellular elements play a role in particular, mast cells, eosinophil, T lymphocytes, macrophages, neutrophils, and epithelial cells. In susceptible individuals, this inflammation causes recurrent episodes of wheezing, breathlessness, chest tightness, coughing, and abundant mucous production, particularly at night or in early morning. These episodes are usually associated with widespread but variable airflow obstruction that is often reversible either spontaneously or with treatment. The inflammation also causes an associated increase in anexisting bronchial hyper-responsiveness to a variety of stimuli.
Reversibility of airflow limitation may be incomplete in some patients with asthma'.
According to this definition, asthma results from the interaction of inflamed airways, obstructed air flow, and bronchial hyperresponsivesness to many stimuli; and that these interactions determine clinical expression of asthma such as wheezing, tight chest and cough [1].
In this study asthma was measured using theAsthma Core Questionnaire of the ISAAC protocol. The questionnaire uses presence of selected symptoms to diagnose presence of the disease. A questionnaire that had questions on use of biomass fuel, to which respondents answered "Yes" or "No" was used to measure the predictor variable.
Asthma is associated with factors broadlyclassifiedinto host and environmental factors. Host factors include age, sex, atopy and genetics. Environmental factors include air pollution emitted from a wide variety of sources such as smoking, use of biomass fuel, automobile transport emissions, emissions from power generation etc. Environmental factors are defined as triggers, suggesting that inherited potential to develop asthma is a necessary condition. Variable susceptibility of individuals to asthma explains why people evenly exposed to triggers do not simultaneouslydevelop asthma. South Africa and Its Association with Asthma Among School Children Aged Thirteen and Fourteen Years of Age This study examines an environmental factor, exposure to use of biomass fuel for energy indoors and asthma.
As used here biomass fuel refers to energy generated from burnt coal, wood, paraffin, dried animal dung and agricultural waste. These energy sources, singly or in combination produce toxic substances, some of them adverse enough to be classified under the Environmental Protection Agency's (EPA) list of criteria pollutants. Table 1 lists air pollutants and their concentrations emitted from biomass fuel, and known to be detrimental to respiratory health. Children are known to be highly susceptible to asthma because of their level of biophysical development [2]. This study used children aged 13 and 14 years to test the association of asthma and use of biomass fuel in households in Limpopo province of South Africa. These age groups are selected in line with the research protocol of the International Study of Asthma and Allergies among Children (ISAAC) which uses two age classifications of 6-7years and 13-14 years. In this study the older age group was selected for convenience.

Study area
Limpopo Province is one of the poorest provinces of South Africa [4].It is predominantly rural. Rural villages and agricultural farming communities comprise the bulk of the provincial land and theseare areaswhere the larger population proportion lives. Table2 gives details of the rural /urban distribution of the population of Limpopo province.
The study area lays within a radius of 60kilometresaround the capital City of Polokwane. The sampled areas are ten schools and five education districts. Schools and districts are distributed variably within a 60 kilometre radius, the majority being located in rural villages. Informal/ traditional housing structures, absence of waterborne sanitation systems, absence of bulk water supplies, and lack of proper road infrastructures and absence of bulk electricity supplies characterize rural villages of Limpopo. This is more so as one move further away from the City of Polokwane.  Table 3 gives details of proportions of various uses of electricity within Limpopo Province compared to South Africa as a whole. Table 3 shows that since1996 up to and including 2007 (year of study), Limpopo Province had lower rates of electricity use in both absolute, and in comparative terms with South Africa as a whole.
Children whom, during the study year (2007), were aged 14 and13 were born in 1993 and 1994 respectively. At the time of the 1996 Census (when thefirst survey on electricity was done), they were aged 3 and 2 respectively. It is therefore likelythat studychildren could have been in the group that was exposed toindoor use of biomass fuels at early ages of three and two, when the risk of respiratory diseases in children could have been higher due to incomplete biological development as suggested [2].

Study Design
Author used a cross sectional design with a weighted andprobability sample of students selected in the study without due regard to exposure or disease status. A multi-stage cluster sampling technique was used for selecting eligible children from the population of study. First, eligible educational districts in Polokwanewere selected on the basis of convenience. Second, eligible schools within selected districts were chosen based on maximum variability, convenience and relevance to the study. Third, eligible classrooms within eligible schools were selected. Finally, eligible students taken from eligible classrooms were selected using the probability proportional to sample (PPS) technique. At each classroom, children who met the criteria for inclusion, namely being aged 13 or 14 years, of unknown exposure status and free from the disease,were selected. Children in the sample were mostly in Grades 7 and 8.Schools for children with special needs were excluded from sampling, so were those whose parents refused to give informed consent.

Data Collection
The Research and Ethics Committee of the University of Pretoria on the 30 th November 2006gavepermission for the study, as did the department of Education in Limpopo by allowing access to different schools. In each school, children aged 13 and 14 were called into the school hall where the study was explained to them. Consent forms attached to questionnaires were given to each child to obtain consent to participate in the study fromparents or legal guardians. After parental consent was obtained, assent was obtained from the children. Children who did not return the forms to school were considered to have been refused to participate in the study. Before interviews commenced, consent and assent forms were separated from the questionnaire to remove all identifiers.
Research assistants interviewed the participants and recorded thedata using structured questionnaires. The completed questionnaires were collected at the various schools, serially numbered and captured. Data validation and verification were done in collaboration with interviewers at the various schools prior to data analysis.

Data Analysis
The objective of the analysis was to determine the association of asthma and use of biomass fuel within households. Exposure to smoke emitted from burnt biomass is one among important predictors of asthma in this study. Others were absence of waterborne toilet, persistent coughand (to a moderate extent), exposure to hyper allergenic diets.
Pearson's Chi-square tests of association, binary logistic regression and multi-level analyses were used for data analysis. Multilevel analysis used for quantifying variability of asthma at the levels of districts and schools will not be explored in this paper. Data entry and analysis were performed using the statistical package, Stata version 10. Table 4 presents demographic and other characteristics of children in the study.

Findings
Fifty-six per cent (56.06%) or 416 children in the study were females. Sixty-five per cent (65%) or 486 were aged 14 years. The overwhelming majority of the sample, 97.17% came from villages, but residence did not significantly predict asthma in this study.
The prevalence of asthma in the sample was 27.63%. This is more than what was previously observed in the same area [7]. Mankweng district which is semi-urban had the lowest prevalence of 17%. Maraba being the farthest and more rural had higher prevalence of 35%.
Prevalence of asthma and odds ratios in various demographic groups:

Age category
In the sub-group of children aged 13 years (n=256) the prevalence of asthma was 25.39% or 65/256. In the sub-group aged 14 years (n=486) prevalence was 29% or 140/486. The asthma odds ratio for the two groups was 0.84, p = 0.323, CI 0.60; 1.19. This findings show that older age was protective of asthma.

Prevalence by sex
In a sub-group of males (n=326), 80 were diagnosed with asthma and the prevalence was 25.0%. Among the sub-group of females (n=416) 125 were diagnosed with asthma and the prevalence was 30.0%. The male-female odds ratio was 1.32, p = 0.06, CI 0.98; 1.99. The finding shows that females were 1.32 times more likely to have asthma than males.

Prevalence by category of residence
In the sub-group coming from rural villages (n=721) 196 or 27.18 were diagnosed with asthma. In the sub-group coming from suburbs, townships and inner city (n=21) 9 were diagnosed with asthma making a prevalence of 43%. Though numerically smaller, prevalence in this latter group was very high indicating the likelihood of exposure to higher concentrations of multiple, particularly environmental agents.
However if we take the total number of asthmatics (n=205) in the whole sample (n=742), only 9 (9/205) or 0.0439% lived in other areas other than villages. But the majority 196/205 (96%) lived in rural villages indicating effects of village life on asthma occurrence. The odds ratio for the two groups was 0.51 showing that not coming from rural villages was protective of asthma.
Prevalence among children who did not live in villages was 0.012%. The odds ratio for the two groups was 0.50 p 0.120 CI 0.21, 1.20. This finding suggests asthma was negatively associated with residential category.
The prevalence of asthma was higher in a group that lived in the area since birth i.e. 47.80% followed by the group that lived in the area from three years onwards with 31%. This finding supports the theory that duration of exposure to air pollutants of certain concentrations is effective in causing asthmaas Klepeis [8] suggests in his exposure model.

Prevalence according to use of biomass fuel
In the total sample (n=742) 270 used biomass fuel for energy within their homes, making a prevalence of 36.40%. The prevalence of asthma in this subgroup (n=270) was 32.96% or 89/270.
Among the 205 subjects with asthma in the whole sample (n=742) 89 or 43.40 % were exposed to use of biomass fuel within their homes.

Use of biomass fuel and asthma
To test whether asthma was associated with use of biomass fuel, a logistic regression analysis was done. This analysis revealed that use of biomass fuel significantly predicted asthma, with odds ratio 1.50 p 0.014 CI 1.085; 2.097, suggesting that children who came from a household using biomass fuel for energy were 1.50 times more likely to have asthma than those who came from households not using biomass fuel for energy.
To test the effects of significant other predictors on the magnitude of the odds ratio of asthma and use of biomass fuel, a logistic regression analysis was done. Results are shown in Table 5.
Results in Table 5 show that the main predictor retained its resilience in the presence of other significant predictors. In a model of asthma and use of biomass fuel, the odds ratio was 1.50, p value 0.014, CI 1.085; 2.097. In a model with significant predictors the odds ratio was 1.43, p 0.047, CI 1.00; 2.04. The difference between the two odds ratios is small showing that the variables in Table 5 are not confounders of the relationship of asthma and use of biomass fuel. Theory suggests that the magnitude of the odds ratio of the predictor and outcome variable depends upon the prevalence of the magnitudes of other variables in the model. Author tested the magnitude of the odds ratio of asthma and biomass fuel ina modelwith all predictors with significant findings. Table 6 gives details.
The predictor variable remained persistent in its significance, odds ratio 1.43, p 0.047, CI 1.00; 2.04.  Tables 5 and 6 shows that the predictor variable was resilient in predicting asthma

Adjustment for Confounding
A review of literature shows that variables such as age, gender, place of residence are potential confounding variables [9]. As a result, the odds ratio estimated from logistic regression analysis were adjusted for age, gender and place of residence. The adjusted odds ratio of asthma and use of biomass fuel was 1.54 p 0.01 CI 1.10; 2.15.When comparing the unadjusted odds ratio of 1.50 p 0.014 and an adjusted odds ratio of 1.54, p =0.01 the difference is not significant, suggesting that these variables were not confound-ers of the association of asthma and use of biomass fuel.

Discussion of Findings
The prevalence of asthma in the sample was 27.63 or 205/742. The findings on age, sexand use of biomass fuel, as far as they relate to susceptibility to asthma, support what is currently known.

Age and asthma
Sixty five per cent of the sample was aged 14 years. The odds ratio of 0.84 suggests that higher age was protective of asthma. This finding supports several theories of children's susceptibility to asthma. One such theory suggests that incomplete biological development of small children(particularly their undeveloped immune defence systems and developing lungs) increase their susceptibility to asthma and other respiratory diseases [2,10].Another theory suggests exposure to inspirable toxic pollutants in early years of life leads to atopy and sensitization of the respiratory system [11]. Theories of asthma development also suggest that airway inflammation, whether inherited or acquired from the environment, if it happens before the age of three years, sets the stage for development of asthma by 6 years of age or later [1].Author is of the opinion that most 13 and 14 year old children in the study were exposed to toxic air pollutants during their early years and that this exposure may have been due to lower rates of electrification in Limpopo province as shown in Table 3.

Gender and asthma
Fifty six per cent (56.06%) or 416/742 respondents were females. The prevalence of asthma within this group was 30% or 125/416.Female asthmatics comprised 61% or 125/205 of the sub-sample of all asthmatics in the study. The odds ratio of female-male asthma was1.32, p 0.06, CI 0.98; 1.99. The finding shows that girls were 1.32 times more likely to have asthma than boys.
This finding is not consistent with the generally held perspective that boys aremore susceptible to asthma than girls. The National Heart, Lung and Blood Institute [1] suggested that at younger ages males are more at risk than females. Harwood [12] also suggested boys are susceptible to asthma before the age of 14 years. Some studies also showed rates of asthma, wheezing, and rhinitis and hay fever symptoms to be higher in boys than girls in cities with high humidity and in cities with low humidity [13].Another theory suggested that lungs of boys are smaller during younger ages when compared with those of girls at same ages, making boys more susceptible to asthma at younger ages [14].

Use of Biomass Fuel and Asthma
Thirty six per cent or 270/742 of the sample used biomass fuel for energy within their homes. The prevalence of asthma within this group was 32.96% (or 89/270).
A logistic regression of asthma and use of biomass fuel yielded an odds ratio of 1.50, p 0.014 CI 1.86; 2.97 suggesting that use of biomass fuel significantly predicted asthma in this sample.
When adjusted by age, gender, residence, the (robust) odds ratio for use of biomass fuel and asthma was 1.54 , p 0.010, CI 1.11; 2.15 suggesting that the crude and adjusted odds ratio did not differ much (1.50vs. 1.54).
Looking at the data above, it is clear that the main study variable predicted asthma significantly and that potential confounders age, gender and residence did not significantly affect the relationship of asthma and use of biomass fuel.
This finding supported what is already known about the effect of burnt biomass on respiratory health: Burnt wood, coal, paraffin, gas, dried animal waste and agricultural waste produce toxic substances. Burnt paraffin and wood emit methane, nitrogen dioxide, nitric acid; carbon monoxide and carbon dioxide are emitted as cooking fumes [15]. Burnt coal emits carbon dioxide and carbon monoxide, dozens of polycyclic hydrocarbons and particulate matter [16].Household cooking stoves with or without ventilation, produce enough pollutants to significantly affect local neighbourhoods [17]. Nitrogen oxide combines with water to form acids that damage lung tissue. It also combines with sulphur dioxide to form inspirable particulate matter (sulphates and nitrates) [18]. Nitrogen dioxide exacerbates asthma and causes death among asthmatics [19]. Sulphur dioxide irritates respiratory tracts and causes airways to close and disrupt lung function [20]. Ozone damages the lungs, causes coughing, and in asthmatic patients, causes exacerbations. It also compromises the immune system and causes shortness of breath and painful breathing [21]. Fossil and biomass fuel [wood and coal] inflame airways and cause them to constrict resulting in breathing difficulties [22]. Fine and ultra-fine inspirable particulate (PM 1.0, 2.5) lodge deeper into lungs and incur damage to lungs [23]. A mixture of toxic pollutants can cause allergic sensitization to healthy individuals and to those who have chronic obstructive diseases [24]. When inhaled, carbon monoxide reduces the ability of the blood to bring oxygen to body cells and tissues [25]. Carbon dioxide inflames airways and causes them to become constricted resulting in breathing difficulties. It also irritates respiratory mucosa and increases sensitization to allergens [26].
The evidence presented in this study suggests that if rural children continue to be exposed to substances that burnt biomass produces, the risk of asthma in Limpopo province will remain high. Given that sick children become sick adults, Limpopo province may confront a phenomenon of insufficient healthy manpower to carry out development tasks.

Recommendations
If findings of this study and that of Maritz [7], both having been done in the District Municipality of Capricorn, are taken together; and given that The District Municipality of