Associations of the planetary health diet index (PHDI) with asthma: the mediating role of body mass index | BMC Public Health

Associations of the planetary health diet index (PHDI) with asthma: the mediating role of body mass index | BMC Public Health

Based on the NHANES database, this study found that after adjusting for relevant covariates, there is a negative association between PHDI and the prevalence of asthma and that BMI mediated this relationship, thus validating our hypothesis. The results of the RCS and subgroup analyses reaffirmed that higher PHDI scores are beneficial in reducing the prevalence of asthma. Additionally, WQS analysis suggests that dietary components of the PHD, including fiber, vitamin C, and protein, play significant roles in the development of asthma.

An important pathogenic mechanism of asthma is airway hyperresponsiveness. Upon exposure to allergens, various inflammatory cells such as eosinophils, mast cells, T cells, neutrophils, airway epithelial cells, and macrophages release inflammatory mediators and cytokines. This release causes damage to airway epithelial cells and exposes epithelial nerve endings, leading to hyperresponsiveness. Studies [27] indicate that the underlying mechanisms of asthma are multifactorial, involving environmental factors, genetic predispositions, and lifestyle choices, with diet being a significant factor. Previous research [28] has found a positive correlation between asthma prevalence and gross domestic product (GDP). For instance, the prevalence of asthma in developed Western countries is typically around 10%, whereas in less developed countries, it is ≤ 1% [29].

The disparity in asthma prevalence between developed and developing countries can be attributed not only to underdiagnosis, high misdiagnosis rates, and inadequate treatment in low- and middle-income countries but also to differences in dietary patterns. Studies [30] have shown that Western dietary patterns emphasize animal-based foods while neglecting whole grains, fruits, vegetables, and legumes. For example, the intake of saturated fats in the U.S. population, which follows a predominantly Western diet, significantly exceeds recommended levels, while fruit and vegetable consumption falls below the norm. As dietary patterns westernize, the risk of asthma increases [31]. In contrast, diets that emphasize whole grains, fruits, vegetables, and legumes, and de-emphasize high-fat meats and dairy products, are beneficial in reducing asthma risk. A case-control study involving 287 children aged 9–19 in Lima, Peru [32], used a modified Mediterranean Diet Score (MDS) to analyze dietary patterns. Preliminary analysis showed a negative correlation between adherence to the Mediterranean diet and the incidence of asthma in children. Similar plant-based dietary patterns have also been shown to reduce asthma risk [33, 34]. A meta-analysis and systematic review of 31 studies evaluated asthma outcomes such as prevalence, asthma-related quality of life, symptoms, lung function, frequency of asthma attacks, asthma control, and inflammatory markers associated with asthma. The results indicated a significant association between dietary patterns and asthma in 12 of the studies, with protective dietary patterns including components like black bread, nuts, and wine [35]. Adhering to a plant-based dietary pattern can result in higher PHDI scores. A multicenter cohort study conducted in Brazil with 14,779 participants using a 114-item Food Frequency Questionnaire (FFQ) found that the PHDI was positively correlated with carbohydrates, plant proteins, polyunsaturated fats, fiber, and micronutrients from fruits, vegetables, oilseeds, and whole grains. In the PHDI, nuts and peanuts, legumes, fruits, total vegetables, and whole grains are defined as adequacy components. Recent research [36] showed that PHDI scores are positively correlated with plant protein, fiber, polyunsaturated fats, vitamins A, E, K, C, and folic acid (p < 0.001), and negatively correlated with animal protein, total fat, monounsaturated fats, and riboflavin (p < 0.001).

This study indicates that dietary fiber, vitamin C, and protein play significant roles in the development of asthma. Meta-analyses [37] have long shown that high consumption of fruits and vegetables is associated with a reduced risk of asthma in both children and adults. Retrospective studies [38] have demonstrated that a high intake of fruits and vegetables is correlated with higher forced expiratory volume in one second (FEV1), reducing the risk of asthma and the incidence of wheezing. Fruit and vegetable consumption can also effectively control and alleviate symptoms during asthma attacks. A cohort study involving 2,870 children [39] showed that habitual fruit consumption helps alleviate asthma symptoms (OR = 0.93, 95% CI 0.85-1.00), and long-term fruit intake was negatively correlated with the frequency of asthma symptoms (OR = 0.90, 95% CI 0.82–0.99) and allergen sensitization (OR = 0.90, 95% CI 0.82–0.99). However, Willers et al. further noted that increased consumption of certain foods, whether early or late in life or over extended periods, does not have a consistent impact on asthma and atopy in 8-year-old children [39]. Consequently, fruit intake may be inversely related to asthma. A prospective cohort study [40] observing 520 children found that fruit intake was inversely associated with the incidence of asthma, rhinitis, and allergy symptoms. The incidence of asthma symptoms decreased from 33.3 to 28.3% to 14.3% across groups with increasing fruit intake (P for trend = 0.01). Additionally, a Dutch study indicated a negative correlation between whole grain consumption and asthma incidence, which our study further supports.

Whole grains are essential components of a healthy diet, providing dietary fiber, B vitamins, minerals, and other nutrients. Early epidemiological studies have linked asthma prevalence to dietary habits. A study using questionnaires and clinical data to define asthma [41] found a negative correlation between whole grain intake and asthma (OR = 0.46, 95% CI 0.19-10), suggesting that high consumption of whole grain products may reduce asthma attacks in children. A Danish study [42] used a disease-death multi-state model to evaluate the correlation between whole grain intake and life expectancy (defined as 20 years of follow-up without cancer, asthma, chronic obstructive pulmonary disease, etc.). It found that for every doubling of whole grain intake, the difference in disease-free life expectancy (without cancer, type 2 diabetes, ischemic heart disease, stroke, asthma, chronic obstructive pulmonary disease or dementia or with disease (any of the listed)) increased by 0.43 (95% CI: 0.33–0.52) in men and 0.15 (95% CI: 0.06–0.24) in women over an average follow-up period of 13.8 and 17.5 years for 22,606 men and 25,468 women, respectively. Furthermore, studies have shown that dietary fiber intake is positively correlated with improved lung function. Higher fiber intake was associated with higher average FEV1 and FVC measurements, with those consuming the most fiber having average FEV1 and FVC values that were 82 ml and 129 ml higher than those consuming the least fiber (P = 0.05 and 0.01, respectively). Therefore, a fiber-rich diet may also play a role in improving asthma [43].

Current observational and clinical research evidence suggests that plant-based dietary patterns (primarily consisting of fruits, vegetables, and whole grains) are valuable in preventing asthma, whereas Western dietary patterns (emphasizing red meat, processed meats, refined grains, and added sugars) appear to increase asthma risk [44]. As a modifiable factor affecting lung health [45], the protective effects of a plant-based dietary model (corresponding to higher PHDI scores) may be associated with oxidative stress, inflammation, and gut microbiota. In contrast, the exacerbation of asthma by a Western dietary model (corresponding to lower PHDI scores) is likely linked to inflammation.

Oxidative stress and inflammation are key mechanisms by which diet influences asthma. Oxidative stress occurs when the balance between the production and elimination of free radicals is disrupted, leading to neutrophilic inflammatory infiltration and increased secretion of proteases, resulting in the production of a large amount of reactive oxygen species (ROS). Excessive ROS can also increase the expression of NLRP3, triggering the release of pro-inflammatory cytokines and inducing inflammation. During inflammation, mast cells and leukocytes accumulate at the damaged site, increasing oxygen intake and subsequently the release and accumulation of ROS at the site, thereby exacerbating oxidative stress. Oxidative stress and inflammation are associated with poor asthma outcomes. When the lungs are exposed to oxidative stress and an inflammatory environment, it can lead to pulmonary dysfunction such as asthma. Research by Wood LG et al. [46, 47]. confirmed that a diet rich in plant-based foods (high PHDI scores) can reduce inflammatory responses and enhance anti-inflammatory factors. Early studies [48] have shown that adopting a plant-based diet provides antioxidants and unsaturated fatty acids, which can alleviate oxidative stress and inflammation, thus mitigating asthma. Increased intake of fruits and vegetables is negatively correlated with the number of pro-inflammatory cytokines and airway neutrophils in asthma patients [49]. Whole grains also have antioxidant and anti-inflammatory properties. Studies [50] have shown that higher consumption of whole grains is associated with lower levels of serum C-reactive protein and tumor necrosis factor-α receptor-2. Conversely, Western dietary patterns exacerbate oxidative stress and inflammation. Research [51] indicates that dairy consumption is positively correlated with the concentration of pro-inflammatory interleukin (IL)-17 F (P < 0.05), suggesting that the IL-17 F-dependent inflammatory pathway may mediate asthma development. Kim et al. [52]. found that a high-fat diet induces the production of numerous pulmonary cytokines, increasing airway hyperresponsiveness and inflammation, as evidenced by elevated IL-6 and IL-8 expression in sputum samples. A diet high in mixed fats not only increases the release of TNF-α and IL-6 but also activates Toll-like receptors, triggering immune responses [53].

The composition and function of respiratory and gut microbiota interact, known as the “gut-lung axis,” and are related to airway immune function. Dysfunction of the airway epithelial barrier and increased permeability contribute to antigen sensitization and the progression of asthma. Concurrently, gut microbiota dysbiosis can increase the risk of asthma. Gut microbiota is closely related to dietary patterns, with different diets influencing the production of various metabolites by gut microbiota, thereby affecting immune responses and modulating pulmonary pro-inflammatory reactions [54]. Studies have shown that plant-based diets (with high PHDI scores) can modulate gut immune responses to improve airway inflammation [55]. Intake of dietary fiber can lead to the production of short-chain fatty acids by gut microbiota, which have a regulatory effect on immune responses. Consuming yogurt can supplement the body with prebiotics, which are dietary supplements that regulate gut microbiota, affect blood lipid levels, and enhance immune system function. Research [56] indicates that women who take prebiotics during pregnancy and lactation may reduce the risk of allergen sensitization.

This study found that BMI mediates the association between PHDI and asthma, potentially through the following mechanisms: (1) The dietary patterns within PHDI may influence asthma risk through their impact on BMI. For instance, diets rich in vegetables, fruits, and whole grains help maintain a healthy BMI [57], potentially reducing asthma risk. Conversely, high-fat and high-sugar diets may increase BMI [58], thereby elevating asthma risk. (2) The gut microbiota in obese individuals typically differs significantly from that of healthy individuals, often characterized by a reduction in beneficial bacteria and an increase in harmful bacteria [59]. This dysbiosis can affect lung health via the “gut-lung axis,” increasing airway susceptibility [54]. Elevated BMI may mediate the relationship between PHDI and asthma indirectly by altering gut microbiota composition, particularly when high-fat and high-sugar diets further disrupt the gut microbiome. (3) Increased BMI may influence immune system function [60], potentially affecting how certain dietary components in PHDI (such as high sugar or high fat) impact asthma risk through BMI’s effects on the immune system. (4) Individuals with higher BMI are more likely to experience airway narrowing and airflow limitation [61], which may increase susceptibility to asthma or exacerbate asthma symptoms during an attack. The mechanical pressure of obesity on the airways could amplify the effects of unhealthy diets within PHDI. (5) Expansion of adipose tissue in obese individuals leads to macrophage infiltration and elevated levels of pro-inflammatory cytokines (e.g., TNF-α, IL-6, and CRP) [62]. These inflammatory markers can affect the lungs via the bloodstream, increasing airway inflammation and thereby worsening or triggering asthma symptoms [63]. Elevated BMI may enhance or accelerate the negative impact of unhealthy dietary components in PHDI on asthma risk through this systemic inflammation pathway.

In summary, the PHDI is a dietary metric representing both planetary and human dietary health. Asthma, beyond its genetic predispositions, is closely associated with diet and environmental factors. Current research predominantly focuses on the relationships between dietary patterns, dietary fiber, and nutrients with asthma. There has been no previous research on the association between PHDI and asthma risk in adults. This study is the first to investigate the role of BMI in the relationship between PHDI and asthma prevalence using the NHANES database. First, a multivariable logistic regression model demonstrated a negative correlation between PHDI and asthma. Smooth curve fitting assessed the relationship, confirming a negative and linear correlation (nonlinearity = 0.138). Subgroup analyses adjusting for age, gender, education level, marital status, income, race, energy intake, smoking, alcohol consumption, hypertension, diabetes, and hypercholesterolemia showed no significant interaction between PHDI and these stratified variables (p > 0.05), indicating a very stable relationship. Finally, the mediation analysis results indicate that BMI serves as a mediator in the association between PHDI and asthma. Literature review reveals that plant-based dietary patterns correspond to higher PHDI scores, while Western and high-fat dietary patterns correspond to lower PHDI scores. Previous studies have found that a high intake of fruits, vegetables, and grains can reduce the risk of asthma [37, 38], whereas a high intake of red meat, eggs, fish, saturated fats trans fats, added sugars and fruit juices increases the risk of asthma. The underlying mechanisms are closely related to oxidative stress, inflammation, and gut microbiota.

Additionally, this study has limitations: (1) The cross-sectional nature of the data limits causal inference, and although PHDI may have an impact on asthma through BMI, more comprehensive prospective cohort studies, randomized controlled trials, or animal studies are required in the future to determine the precise pathogenic processes. (2) The constraints of the NHANES database preclude us from eliminating the potential confounding factors’ ultimate impact on the study results, even though we included a reasonably high number of covariates based on prior research to improve the robustness of our study results. As a result, it is important to interpret the study’s findings carefully and impartially. (3) Given that the analysis of the relationship between dietary components and disease risk should adhere to the isocaloric principle, incorporating all macronutrients, micronutrients, and energy within the same model may introduce bias [64]. Consequently, the WQS analysis results in this study should be interpreted with caution. (4) The development of the PHDI is based on the Food Frequency Questionnaire (FFQ). Although the FFQ is the most used method in epidemiological studies to investigate the relationship between diet and health outcomes, it has its limitations. These include the incompleteness of the food list and the potential for recall bias in the reports provided [65]. (5) It is well known that asthma is associated with socioeconomic status, urbanization, and local air pollution levels, all of which play a significant role in the pathogenesis of asthma [66]. In the future, we plan to pursue multicenter studies with larger sample sizes or explore alternative study designs to address this limitation.

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