Home exposure to Arabian incense (bakhour) and asthma symptoms in children: a community survey in two regions in Oman

Asthma is a worldwide major health problem with significant variations in its prevalence and severity in different parts of the world [1, 2]. As a participating center in the International Study of Asthma and Allergies in Children (ISAAC), we have previously shown that asthma is common in Omani children with prevalence rates of 10.5% and 20.7% in 6–7 and 13–14 years old children respectively) [3]. In addition, Oman ranked among the top countries in ISAAC global ranking of symptoms taken to indicate severe asthma [2, 3]. For example, the prevalence of waking one or more nights per week in the past 12 months in 6–7-year-old children was 3.5% (nearly 50% of all children with current wheeze), putting Oman in the top five countries for this severe symptom. Similarly, the 13–14-year-old group ranked among the top for the prevalence of severe asthma symptoms such as sleep disturbing wheeze and speech-limiting wheeze. We also found a significant variation in the prevalence of asthma diagnosis and symptoms among children from different geographical regions of the country [4, 5].

As no information is available on the prevalence of asthma risk factors in Oman, we postulated that these findings may be due to differences in locally prevailing factors such as family history, sensitization to pollen and house dust mite, respiratory infections, and dietary habits, in addition to outdoor and indoor air pollutants including incense smoke. These factors may influence the pathogenesis and severity of asthma and require investigation not only to contribute to the understanding of asthma etiology, but also to plan measures for its control. [6]. In particular, it is important to explore the less characterized risk factors related to life style, culture and home environment which may be peculiar to different populations [7–9].

In Oman and other Gulf countries, Arabian incense (bakhour) is one of the common indoor smoke sources to which individuals are frequently exposed, and may be an important contributory factor to the observed high prevalence and severity of asthma in children of this region [10]. A wide variety of substances are used to produce bakhour including frankincense, aromatic wood, herbs, flowers, essential oils, and perfumes burned using charcoal burner [10]. Frankincense is a resin produced by oozing from incisions in the trunks of trees of the genus Boswellia that grow in the south of Oman (Dhofar) [11]. Other forms of incense are derived from sandalwood and are usually mixed with ingredients such as natural oils and perfumes [10].

Due to its slow and incomplete combustion, incense burning produces continuous smoke, generating pollutants such as toxic gases and chemicals particles including polycyclic aromatic hydrocarbons, carbon monoxide, benzene, and isoprene that easily accumulate indoors, especially under inadequate ventilation [12]. Exposure to incense smoke has been linked to several illnesses, including respiratory symptoms, asthma, elevated cord blood IgE levels, contact dermatitis and cancer [10, 12–14]. In addition, it has been demonstrated that exposure to bakhour induced significant morphological changes in rats pneumocytes. [15]. The widespread use of bakhour in Oman, has prompted the need to explore whether exposure to bakhour contributes to the prevalence of asthma and/or triggers its symptoms in Omani children by comparing two Omani regions with different prevalence of asthma.

A total of 2535 questionnaires were distributed and 2441 (1241 from Muscat) were returned and available for analysis (96% response rate; 95% in Muscat and 97% in South Sharqiyah). The mean age (SD) of children was 10.7 (0.9) years, and was slightly higher in South Sharqiyah; 10.8 (0.9) years compared to Muscat; 10.6 (0.9) years (p < 0.001). The gender distribution was similar in the two regions (males constituted 54.3% and 51.3% in Muscat and Sharqiyah respectively, p = 0.141). The prevalence of current asthma diagnosis in the study sample was 15.4%.

Figure 1 shows the frequency of triggers of wheeze among children with current asthma stratified by region. Although, there was a trend for higher frequency of various wheeze triggers in Sharqiyah region, the difference was not statistically significant except for fumes (p = 0.042). Bakhour was reported as a cause of worsening wheeze in 33.1% and 40.7% (p = 0.144) of children with current asthma in Muscat and Sharqiyah respectively, making it the fourth most common factor for worsening wheeze after dust, weather and viral upper respiratory tract infections in both regions.

This study builds on our prior work as participating center in the ISAAC phases one and three by confirming the previous findings in another age group (10 year old children) using ISAAC phase II protocols. Consistent with our previous finding in ISAAC phase one (1995) and phase three (2001) surveys conducted on 6–7 and 13–14 year old children, the prevalence rates of asthma symptoms and diagnosis in these 10 year old children were significantly higher in South Sharqiyah region [4, 5]. More importantly, this study explores the role of the Arabian incense burning "bakhour" which is commonly used in Oman and other Gulf countries, as a potential indoor environmental risk factor for asthma symptoms. In this study, we evaluated the relationship between the frequency of bakhour use and asthma symptoms and its interaction with other potentially relevant factors.

After controlling for potential confounding factors in multivariate analysis (Table 2), we found a significant dose-response association between the frequency of bakhour use and its effect on these children breathing especially asthmatics. Parents who reported regular use (more than twice per week) of bakhour at home were three times more likely to report that their child breathing was affected by bakhour compared to parents who rarely used bakhour, and this was more 2.5 times higher in children with current asthma. The effect of bakhour was also significantly higher in girls and in children from Sharqiyah. In addition, bakhour was reported (Figure 1) as a cause of worsening wheeze in nearly 40% of children with current asthma, making it the fourth most common precipitating factor of wheeze (after dust, weather and viral upper respiratory tract infections). However, we found no significant association between bakhour use and the prevalence of current asthma (Table 3). There was also no significant difference between bakhour users and non users in the prevalence of any of the surveyed respiratory symptoms (Table 4). These findings suggest that bakhour is a common trigger factor of respiratory symptoms among Omani school children especially asthmatics and females. However, it is not be associated with higher prevalence of current asthma.

As there is no data on the contribution of incense burning to indoor air pollution in Oman, it is reasonable to assume that a higher frequency of incense burning produces a higher concentration of incense smoke pollutants. In general, most people spend approximately 90% of their time indoors [18]. Due to the very hot weather in Oman, it is expected the time spent indoors to be even higher especially for women and children. This may explain the observed greater susceptibility of girls to the effect of bakhour. The cause of the higher effect of bakhour on children from Sharqiyah region is not clear. Possible explanations include greater susceptibility [7], presence of other confounding factors not controlled for in the present analysis [5] and/or the difference in the composition of bakhour which is known to vary between regions within Oman. Further studies are necessary to determine the factors which influence the susceptibility to bakhour.

In the three studies that looked at the relationship between bakhour and asthma in the Arabian Gulf region, exposure to different types of Arabian incense was also reported as a significant precipitating factor of asthma symptoms in children [10, 13, 14]. However, none of these studies evaluated the relationship between bakhour and the prevalence of asthma. In Qatar, a case control study, found history of exposure to bakhour in 80% of asthmatic children compared to 66% of normal controls, [10] and in another study, bakhour was reported as precipitating factor of asthma symptoms in 19% of children with asthma [13]. Exposure to bakhour was also reported as trigger for asthma in 26% of 135 consecutive asthmatics attending a pediatric asthma clinic in a tertiary referral centre in Kuwait [14].

Several other studies from Asian populations, where different types of incense are burnt for religious purposes, reported significant associations between exposure to incense smoke and respiratory symptoms [12, 19, 20]. In contrast, one large survey of school children, showed incense burning at home was negatively associated with the prevalence of asthma [21]. The authors suggested that incense use might have been decreased in families with asthmatic children. In another study of 346 primary school children, there was no association between exposure to incense burning and respiratory symptoms [22]. Likewise, a case control study of 50 non smoking Saudi women with chronic obstructive pulmonary disease, reported no significant difference in the use of bakhour between cases and control [23].

Similarly our study did not find any significant association between bakhour use and the prevalence of current asthma. In fact there was an inclination towards a negative association which was significant in simple regression analysis, but disappeared after adjusting for other factors in the multivariate analysis. There was also no significant difference between bakhour users and non users in the prevalence of core asthma symptoms or any of the surveyed respiratory symptoms. Since our study is a cross-sectional, it is possible that families with asthmatic children avoid the use of bakhour after learning that bakhour might worsen asthma symptoms. Such avoidance behavior may influence the relationship between the reported prevalence of asthma and exposure to bakhour leading to underestimation or even reversal of any association. In our study, this was supported by the finding that parent who reported that their children were affected by bakhour exposure were less likely to report its use in the presence of child or in the child room.

The mechanisms by which bakhour provokes respiratory symptoms are unknown. People who are exposed to incense smoke inhale a complex mixture that contains particulate matter, gas products and many organic compounds, making it difficult to single out the health effects contributed by a certain component in the smoke. Furthermore, there appears to no standardized constituents of different types of bakhour even within the same country [12]. Our study has its limitations. The use of symptoms questionnaire to distinguish asthmatics and non asthmatics has potential problems arising from subjective symptom recognition and recall. In addition, as they were new to the Arabic version of ISAAC phase II, bakhour questions needed to have more scrutinized measures of validity and reliability. In ISAAC studies, current asthma is defined by wheeze in the past 12 months (current wheeze), regardless of the response to "ever had asthma?" question [16]. In addition, we included children with positive response to "ever had asthma?" together with positive responses to exercise wheeze and/or night cough not related to cold in the past 12 months in current asthma category. Like any cross-sectional study, this report lacks clear temporal association between exposure and its effect. We tried to overcome this problem with the question "does exposure to bakhour affect your child breathing?" In addition, the finding of bakhour exposure as one of the most frequent triggers of wheeze in our children suggests a temporal association. Finally, because of our primary focus, only few of asthma risk factors were evaluated.

This study demonstrated that burning of Arabian incense (bakhour) is common practice in Omani households and is an important trigger of wheezing among children with asthma. However, there was no association between bakhour use and the prevalence asthma in these children. To obtain more conclusive information, detailed studies are needed to address the various characteristics of incense burning practice and its respiratory effects, including: identifying the most common types, their compositions and the temporal association with respiratory symptoms, in addition to lung function measurements in high exposure individuals. Furthermore, the effect of incense smoke on asthma and the respiratory system and its mechanism needs further studied in animal models. As bakhour use is very common in most Arab communities, our findings have important public health implications. With the currently available evidence, it is important to raise public awareness about the potential harmful effects of incense burning in order to take steps to reduce exposure such as reducing the frequency and duration of incense burning, keeping the room well ventilated when burning incense and avoiding such practice in the presence of children and susceptible individuals.