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Effect of polyunsaturated fatty acids intake on the occurrence of current asthma among children and adolescents exposed to tobacco smoke: NHANES 2007–2018

Journal of Health, Population and Nutrition volume 43, Article number: 168 (2024) Cite this article

Abstract

Background

Asthma is an airway inflammatory disease driven by multiple factors with a high incidence in children and adolescents. Environmental tobacco smoke exposure (TSE) and diet are inducing factors for asthma. The potential of omega-3 polyunsaturated fatty acids (PUFAs) to alleviate asthma symptoms by their anti-inflammatory effects has been explored. However, to date, no studies have explored the effect of dietary PUFAs intake on the asthma in children and adolescents exposed to tobacco smoke.

Objective

We aimed to examine the effect of dietary PUFAs intake on the current asthma in children and adolescents exposed to tobacco smoke.

Methods

Data of this cross-sectional were extracted from the National Health and Nutrition Examination Survey (NHANES) 2007–2018. Children and adolescents with serum cotinine concentration ≥ 0.05 ng/mL were defined to exposed to tobacco smoke. Dietary PUFAs intake information were obtained from 24 h recall interview. The weighted univariate and multivariate were utilized to explore the effect of PUFAs on the association of asthma and TSE, with adjusted odds ratios (AORs) and 95% confidence intervals (CIs). These moderating effects were further explored based on the age, gender and body mass index (BMI) and sedentary time.

Results

Totally, 7981 eligible children and adolescents were included, with the mean age of 11.96 ± 0.06 years old. Of whom, 1.024 (12.83%) had current asthma. After adjusted all covariates, we found children and adolescents with TSE had high occurrence of current asthma (AOR = 1.2, 95% CI 1.03–1.63); We also found omega-3 PUFAs intake (P for interaction = 0.010), not omega-6 PUFAs (P for interaction = 0.546), has a moderating effect on the association of TSE and current asthma. Moreover, we further observed that children and adolescents with TSE and low omega-3 PUFAs intake had high occurrence of current asthma (AOR = 1.58, 95% CI 1.19–2.10), while no significant association was found in children and adolescents with high omega-3 PUFAs intake (all P > 0.05). This moderating effect was more prominent in children and adolescents aged ≤ 12 years old (AOR = 1.62, 95% CI 1.06–2.47), girls (AOR = 2.14, 95% CI 1.15–3.98), overweight (AOR = 1.87, 95% CI 1.01–3.47) and sedentary time > 6 h (AOR = 1.96, 95% CI 1.00–3.86).

Conclusion

We found dietary omega-3 PUFAs plays a moderating effect on the association of asthma and TSE in children and adolescents, especially in children and adolescents aged ≤ 12 years, girls, overweight or sedentary time > 6 h. This moderating effect suggested higher omega-3 intake has potential benefits in decreasing the occurrence of asthma in children and adolescents who exposed to tobacco smoke.

Introduction

Asthma, a condition featured by airway hyper-responsiveness and increased mucus secretion leading to airway obstruction, constitutes a significant disease burden on children and young individuals [1]. Globally, the prevalence of asthma in children have increased significantly in the past 40 years, with a prevalence of 9.6% and 10.5% in children aged 5–11 and 12–17 years, respectively [2, 3]. Inhaled glucocorticoids are the most commonly used treatment persistent asthma in clinical practice [4], but some of children still experience frequent and severe relapses, causing deterioration of lung function [5]. Exploring modifiable factors contributing to asthma and good health management of asthma are important to reduce the burden of asthma in the children and adolescents.

Asthma is an inflammatory disease driven by environment exposure. Tobacco smoke exposure (TSE) is a vital factor of environment pollution [6]. There is an abundance of evidence to suggest that children and adolescents exposed to environmental tobacco smoke may suffer adverse health consequences including reduced lung growth, increased susceptibility to respiratory infection and onset of childhood asthma [7].

In addition to TSE, dietary is an important wellness factor associated with asthma [8]. Polyunsaturated fatty acids (PUFAs) are essential fatty acids acquired mainly via fish and vegetable oils, consisting of two subtypes, omega-3 PUFAs and omega-6 PUFAs [9]. These fatty acids are a source of biologically active molecules, in the lung and provide biologic rationale for respiratory effects [10]. Among these fatty acids, omega-3 has been demonstrated to exhibit anti-inflammatory effects on airway and may modify the influence of TSE on the onset of asthma in children [11]. Brigham et al. [12] reported that high omega-3 PUFAs intake was associated with reduced effect of indoor particulate matter (PM) ≤ 2.5 μm in aerodynamic diameter on asthma symptoms. To date, there are no relevant reports on the association of dietary PUFAs intake and the risk of asthma among children and adolescents exposed to tobacco smoke. We speculate that high dietary PUFAs intake, especially omega-3 PUFAs, may play a moderating effect on the risk of asthma in these populations.

This study aims to explore the effect of dietary PUFAs intake on the risk of asthma in children and adolescents exposed to tobacco smoke, and further discuss this effect in age, gender, body mass index (BMI) and sedentary time subgroups.

Methods

Study design and population

Data of present cross-sectional study were extracted from the National Health and Nutrition Examination Surveys (NHANES) database 2007–2018. In NHANES, data of approximately 5000 representative and non-institutionalized samples were collected annually through a multistage sampling design since 1999 to assess the health and nutrition of the U.S. household population. The interview of NHANES includes demographic, socioeconomic, dietary, and health-related questions and the examination of NHANES consists of medical, dental, physiological measurements, and laboratory tests [13]. All examinations were administered by highly trained medical personnel to ensure the stability and completeness of the data. The detailed information of the NHANES survey can be found on the website (NHANES—National Health and Nutrition Examination Survey Homepage (cdc.gov). The requirement of ethical approval for this was waived by the Institutional Review Board of Changzhi Maternal and Child Health Care Hospital, because the data was accessed from NHANES (a publicly available database). All methods were performed in accordance with the relevant guidelines and regulations.

In current study, 10,902 children and adolescents aged 6–17 years old were initially included. Among them, 2131 without the complete intake data of omega-3 PUFAs or omega-6 PUFAs, 37 without the BMI data and 753 without the assessment information of current asthma were exclude. Current asthma of children and adolescents was defined by self-reported questionnaire responses. If subjects responded to the question “Has a doctor or other health professional ever told you that you have asthma?” and “Do you still have asthma?” both “yes”, then they were diagnosed as having current asthma. Subjects only answered “yes” to the former question while answered “no” to latter question were diagnosed as not having current asthma, and these subjects were excluded from our study [13].

Finally, 7981 eligible children and adolescents were included for further analysis. The entire process of study subjects was shown in Fig. 1.

Fig. 1
figure 1

The flow chart of population screening

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Assessment of dietary PUFAs intake

Dietary PUFAs intake data were obtained from two 24-h dietary recall interviews. The first 24-h recall interview was performed in-person by experienced interviewers at the Mobile Examination Center (MEC). The second interview was conducted via telephone or mail between 3 and 10 days after the MEC interview. Participants were required to recall all the type and quantity of food and beverages consumed in the 24 h prior to the interviews. This data was utilized to calculate the consumption of energy, nutrients, and other food components [14]. Then, these consumption data were converted to United States Department of Agriculture (USDA) standard reference codes, and the dietary intake was linked to the USDA’S Food and Nutrient Database for Dietary Studies (FNDDS). The PUFAs intake information of subjects aged 6–11 years old were accompanied by their guardian to assist in responding, while subjects aged 12–17 years old were responded by themselves. In this study, the average value of the two 24-h dietary intake data of omega-3 PUFAs or omega-6 PUFAs was used, and dichotomized these PUFAs according to the upper tertiles of intake in the study children and adolescents. Thus, the cut-off values for omega-3 PUFAs and omega-6 PUFAs intake were 1.57 and 16.03, respectively.

Assessment of tobacco smoke exposure

As a primary nicotine metabolite, serum cotinine concentration was used as a predictor to represent recent TSE levels for both exclusive consumed tobacco users and non-users of tobacco products [15, 16]. For laboratory measures, serum samples were stored at appropriate frozen conditions (below − 20 °C), and were transported to test at National Center for Environmental Health. Serum cotinine concentration was testing by isotope-dilution high-performance liquid chromatography/atmospheric pressure chemical ionization tandem mass spectrometric (ID HPLC-APCI MS/MS) method [17]. This method has good accuracy, with mean values within 9% of theoretical values at all levels expect the lower limit of quantification, where it was within 14% of the theoretical values. In present study, serum cotinine concentration ≥ 0.05 ng/mL were considered as TSE, while < 0.05 ng/mL were considered as non-TSE [18].

Potential covariates

Data of study children and adolescents’ demographic information, family background, physical examination, laboratory values and dietary intake were extracted from the NHANES database. Age, gender, race and educational level were self-reported demographic information. Sedentary time was assessed by the NHANES through the daily hours of watching TV or videos and computer for subjects aged 6–11 years old while subjects aged 12–17 years old were assessed by the time of sedentary time. Sedentary time was divided into two categories: > 6 h and ≤ 6 h [19]. Children and adolescents’ overweight were defined as BMI at or above the 85th and below 95th gender-specific percentile of the BMI-for-age growth chart from the Centers for Disease Control and Prevention (CDC) [20]. Close relative asthma history was defined by a positive response to the question “Including living and deceased, were any of your close biological ever told by a health professional that they had asthma?”. Hey fever was defined by the question “During the past 12 months, have you had an episode of hay fever?”. Household smoke was defined by the question “Does anyone smoke in the home?” in NHANES 2007–2012 while “How many people who live here smoke cigarettes, cigars or any other tobacco product?” and “Not counting decks, porches or detached garages, how many people who live here smoke cigarettes, cigars or any other tobacco product inside this home?” in NHANES 2013–2018. For children aged 6–11 years old, physical activity (PA) levels were assessed by the question “During the past 7 days, how many days was physical active for a total of least 60 min per day?” and PA on every day was considered as ideal PA. For adolescents aged 12–17 years old, PA was expressed as the metabolic equivalent task (MET) and calculate as follows: PA (met·min) = recommended MET × exercise time for corresponding activities (min/day) the number of exercise days per week day (day) [21]. Ideal PA for adolescents was ≥ 180 met·min/day. Then, all children and adolescents were divided into three categories: non-ideal PA, ideal PA and unknown.

Statistical analysis

Quantitative data were represented as mean and standard error (S.E.), and categorical data were represented as the number and percentage [N (%)]. We compared quantitative data and categorical data among different groups using the weighted t-test and chi-square test, respectively. Rank sum test was used for ranked data. Sensitivity analyses were performed to compare whether the results were different before and after imputation of missing covariates (Table S1). The weighted univariate logistic regression model was used to screen for covariates related to children and adolescents’ asthma (Table S2). The collinearity test was used to explore whether there was collinearity between each variable with the evaluation index of variance inflation factor (VIF) (Table S3). The weighted multivariate logistic regression models were utilized to evaluate the association of serum cotinine concentration, omega-3 PUFAs, omega-6 PUFAs and their moderating effect on the odds of asthma among children and adolescents, with adjusted odds ratios (AORs) and 95% confidence intervals (CIs). Subgroup analyses were performed to further evaluate whether these moderating effects remain robust based on age, gender, overweight, and sedentary time. All analyzes were performed using R (version 4.20, Foundation for Statistical Computing, Vienna, Austria) and SAS 9.4 (SAS Institute Inc., Cary, NC, USA). Two-sided P < 0.05 was considered statistically significant.

Results

Characteristics of study children and adolescents

Finally, 7981 eligible children and adolescents were included for analysis, with the weighted frequency of 185,390,379. Among them, 1024 (12.83%) had current asthma. The baseline characteristics of study children and adolescents were depicted in Table 1. The proportion of children and adolescents with high serum cotinine concentration in current asthma group was significantly high than in non-current asthma group (48.19% vs. 37.04%). The differences were found in age, race, household smokers, the level of poverty-to-income ratio (PIR), sedentary time, BMI and education, and the history of hay fever and asthma in close relative between current asthma group and non-current asthma group (all P < 0.05).

Table 1 Characteristics of study children and adolescents
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Association of TSE, omega-3 PUFAs or omega-6 PUFAs with current asthma

The association of single TSE, omega-3 PUFAs or omega-6 PUFAs with current asthma in children and adolescents were evaluated by three logistics regression models, as depicted in Table 2. Model 3 adjusted age, gender, race, sedentary time, overweight, asthma in close relative and hay fever and the collinearity test shown that there is no collinearity between each covariates (VIF < 10) (Table S3). We observed that children and adolescents with TSE (serum cotinine concentration ≥ 0.05 ng/mL) had a 29% increased occurrence of current asthma (AOR = 1.29, 95% CI 1.03–1.63, P = 0.030). However, no significant statistically association between omega-3 PUFAs and omega-6 PUFAs with current asthma were observed (all P > 0.05).

Table 2 Association of TSE, dietary PUFAs intake and current asthma
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Moderating effects of dietary PUFAs intake on the association of TSE and current asthma

Moderating effects of dietary omge-3 PUFAs or omega-6 PUFAs intake on the association of serum cotinine concentration and current asthma were validated by three logistic regression models. In fully adjusted model, we observed that omega-3 PUFAs intake may have a moderating effect on the association of TSE and current asthma (P-value for interaction = 0.01) (Table 3), while no significant moderating effect were observed on the omega-6 PUFAs on the association of TSE and current asthma (P-value for interaction = 0.546) (Table 4).

Table 3 Moderating effect of omega-3 PUFAs on the association of TSE and current asthma
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Table 4 Moderating effect of omega-6 PUFAs on the association of TSE and current asthma
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The association of different omega-3 PUFAs intake, TSE and current asthma

Since the moderating effect on the association of TSE and current asthma was observed in omega-3 PUFAs, but not omega-6 PUFAs, then, the moderating effects of different levels of omega-3 PUFAs intake on the association of TSE and current asthma were further explored, as depicted in Table 5 and Fig. 2. In low omega-3 PUFAs intake group (≤ 1.57 g), children and adolescents with TSE were associated with high occurrence of current asthma (AOR = 1.58, 95% CI 1.19–2.10, P = 0.002), however, this association was not observed in high omega-3 intake group (P = 0.394). That was, omega-3 PUFAs may have a moderating effect on the association of TSE and current asthma in children and adolescents.

Table 5 Association of TSE and current asthma based on different omega-3 PUFAs intake
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Fig. 2
figure 2

The moderating effect of dietary omega-3 PUFAs on the association of asthma and serum cotinine concentration

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Moderating effect of omega-3 PUIFAs intake on the association of TSE and current asthma based on age, gender, overweight and sedentary time

Subgroup analysis was performed to verify this moderating effect based on age, gender, overweight and sedentary time. We found the moderating of omega-3 PUFAs intake on the association of TSE and current asthma was more prominent in children and adolescents aged ≤ 12 years old (AOR = 1.62, 95% CI 1.06–2.47, P = 0.027), girls (AOR = 2.14, 95% CI 1.15–3.98, P = 0.017), overweight (AOR = 1.87, 95% CI 1.01–3.47, P = 0.047) and sedentary time > 6 h (AOR = 1.96, 95% CI 1.00–3.86, P = 0.050) (Table 6).

Table 6 Subgroup analysis of the moderating effect of dietary omega-3 PUFAs intake on the association of TSE and current asthma
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Discussion

In present study, the effect of dietary PUFAs intake on the association of serum cotinine concentration with current asthma in U.S. children and adolescents were explored. The results were as follows: (1) subjects with high serum cotinine concentration were associated with high risk of current asthma; (2) high dietary omega-3 PUFAs intake may have a moderating effect on the association of serum cotinine and current asthma, while no significant moderating effect was found in the omega-6 on the association of serum cotinine and current asthma; (3) subgroup analysis suggested that this moderating effect of omega-3 PUFAs was more prominent in the children and adolescents with aged ≤ 12 years old, girls, overweight and sedentary time > 6 h.

Although the driving factor of asthma have not yet been completely understood, a plenty of hazard factors deemed to trigger asthma have been elucidated. Cotinine, a major metabolite of nicotine, is a valuable marker of exposure to tobacco smoke due to its high specificity and sensitivity [22]. Cotinine has relatively prolonged half-life which ranges from 16 to 20 h in children. Cotinine collected from plasma or serum is not influenced by renal function and flow rate, and serum cotinine has become the most widely used biomarker of TSE among children and adolescents [23]. Several epidemiological studies have demonstrated the association of serum cotinine concentration and childhood asthma [24,25,26,27]. Our study found children with high serum cotinine concentration had a 29% increased risk of asthma, which adds new evidence to the association and TSE with childhood asthma. In a vitro study, cigarette smoking induces cytotoxicity, partly through Akt (a serine/threonine kinase, suppresses apoptosis and regulates the cell cycle) degradation via the ubiquitin–proteasome system [28]. Thus, TSE would impact the initiation of chronic lung disease in childhood.

Diet is another driving factor of childhood asthma [29]. In in western countries, the prevalence of asthma is increasing as the popularity of westernized diet featured by high intake of processed food in contrast to a healthy diet high in fruit, vegetable and fish intake [29]. This unhealthy dietary pattern may lead to a decrease in the intake of antioxidants and micronutrients, thereby increasing the risk of inflammatory diseases. Omega-3, as a type of PUFAs, is proven to be associated with asthma in different populations due to anti-inflammatory effects. The Ryukyus Child Health Study included 25,033 schoolchildren aged 6–15 years examined the association of fatty acid intake and asthma and reported that consumption of both omega-3 PUFAs and omega-6 PUFAs may be associated with the risk of asthma [30]. In our study, only the association of omega-3 PUFAs and the childhood asthma were found. The different between our study and that study may be that study using a self-administered brief dietary history to obtain dietary intake data, which can be explain the bias among two studies. A cross-sectional of Zhang et al. [31] to investigate the dietary omega-3 intake and asthma in subjects aged less than 20 years old. The study found that dietary omega-3 PUFAs intake exhibited an L-shaped relationship with childhood asthma. However, a systematic review and meta-analysis of Muley et al. [32] included several observational studies and multicenter randomized controlled trials reported the different results. In that study, they found there is no significant association between omega-3 PUFAs supplementation in infants and children and asthma, allergic exacerbations, or wheeze. It is important to consider differences in population, age distribution as well as study outcomes, which may explain the differences in that study and our study.

Omega-3 PUFAs are naturally present in fish oil, which are the vital components of cell membranes and have a significant effect on cell signaling and gene expression, thereby affecting immune cell activity. It can effectively reduce the synthesis of prostaglandins and leukotrienes, thus reducing the inflammatory response [33, 34]. D-series catabolites and E-series catabolites, the anti-inflammatory metabolites of omega-3 PUFAs, can exert powerful anti-inflammatory effects, which may improve asthma symptoms and promote bronchodilation [35]. In addition, omega-3 PUFAs can suppress the inflammatory response by enhancing antioxidative function and inhibiting the omega-3 PUFAs cascade involving NF-kB and pro-inflammatory cytokines [36]. All in all, adequate intake of omega-3 PUFAs in children and adolescents has a protective effect on the prevention and management of asthma.

Strengths

In the present study, utilizing data from six survey cycles to achieve a large sample size and adjusting as many as possible covariates that could affect asthma attacks, the moderating effects of dietary PUFAs intake on the association between TSE and asthma in children and adolescents were explored. The subgroup analysis of age, gender, BMI and sedentary time were conducted to further evaluate this moderating effect. We found this moderating effect was more prominent in the subjects were aged ≤ 12 yeas, female, overweight or sedentary time > 6 h. In such populations, high dietary omega-3 PUFAs and supplementation have the potential beneficial effects to reduce airway inflammation and asthma attack risk in children and adolescents exposed to tobacco smoke.

Limitations

However, several limitations need caution when interpreting our findings. First, the cross-sectional design of the study prevents establishing a causal relationship between dietary omega-3 PUFAs intake and asthma in children and adolescents exposed to tobacco smoke. Second, dietary PUFAs intake data were obtained from 24-h dietary interview, which has a certain recall bias. Moreover, the daily diet of individuals varies greatly, and the 24-h dietary recall interview can only represent the individual's short-term eating habits. Third, current asthma status was based on a patient’s recall and a physician’s diagnosis of asthma, which could also introduce recall bias. Further large-scale prospective studies employing more accurate methods of dietary intake assessment and asthma measurement are needed to validate and expand our results.

Conclusion

We included 7981 eligible children and adolescents from the NHANES 2007–2018 and found that dietary omega-3 PUFAs may play moderating effect on the association between current asthma and TSE. This result suggested that for children and adolescents exposed to tobacco smoke should pay more attention to the potential benefits of dietary and supplement of omega-3 PUFAs intake in reducing the occurrence of asthma, and more well-designed prospective studies are still needed.

Availability of data and materials

The datasets generated during and/or analyzed during the current study are available in the NHANES database, https://wwwn.cdc.gov/nchs/nhanes/.

Abbreviations

TSE:

Tobacco smoke exposure

PUFAs:

Polyunsaturated fatty acids

PM:

Particulate matter

BMI:

Body mass index

NHANES:

National Health and Nutrition Examination Surveys

MEC:

Mobile Examination Center

CDC:

Centers for Disease Control and Prevention

PA:

Physical activity

MET:

Metabolic equivalent task

S.E.:

Standard error

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Authors and Affiliations

  1. Department of Emergency, Changzhi Maternal and Child Health Care Hospital, No.48 Weiyuanmen Middle Road, Luzhou District, Changzhi, 046000, Shanxi Province, People’s Republic of China

    Chunyan Wang & Guoqiang Hou

  2. Department of Neonatology, Changzhi Maternal and Child Health Care Hospital, Changzhi, 046000, Shanxi Province, People’s Republic of China

    Li Wang

  3. Department of Pediatric Respiratory, Changzhi Maternal and Child Health Care Hospital, Changzhi, 046000, Shanxi Province, People’s Republic of China

    Wanling Ding

  4. Department of Pediatric Digestive, Changzhi Maternal and Child Health Care Hospital, Changzhi, 046000, Shanxi Province, People’s Republic of China

    Feng Zhao

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  1. Chunyan Wang
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  3. Wanling Ding
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  4. Feng Zhao
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Contributions

Chunyan Wang designed the study. Li Wang wrote the manuscript. Wanling Ding, Feng Zhao and Guoqaing Hou collected, analyzed and interpreted the data. Chunyan Wang critically reviewed the manuscript. All authors read and approved the manuscript.

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Correspondence to Chunyan Wang.

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The requirement of ethical approval for this was waived by the Institutional Review Board of Changzhi Maternal and Child Health Care Hospital, because the data was accessed from NHANES (a publicly available database). The need for written informed consent was waived by the Institutional Review Board of Changzhi Maternal and Child Health Care Hospital due to retrospective nature of the study. All methods were performed in accordance with the relevant guidelines and regulations.

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Wang, C., Wang, L., Ding, W. et al. Effect of polyunsaturated fatty acids intake on the occurrence of current asthma among children and adolescents exposed to tobacco smoke: NHANES 2007–2018. J Health Popul Nutr 43, 168 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s41043-024-00663-8

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Keywords

Journal of Health, Population and Nutrition

ISSN: 2072-1315

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