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Association between serum albumin and pulmonary function in adolescents: analyses of NHANES 2007–2012

BMC Pulmonary Medicine volume 24, Article number: 554 (2024) Cite this article

Abstract

Background

Pulmonary function tests (PFTs) are an important tool for assessing pulmonary diseases, although clinicians often find it challenging to accurately evaluate the pulmonary function of children.

Methods

We intend to investigate the association between serum albumin (SA) and lung function among U.S. adolescents. This cross-sectional study included 3,072 adolescents (aged 12 to 19) from 2007 to 2012National Health and Nutrition Examination Survey (NHANES). PFTs, including forced vital capacity (FVC)%predicted, forced expiratory volume in 1 s (FEV1)%predicted, FEV1/FVC%predicted, and maximum mid-expiratory flow (FEF25-75) % predicted, were utilized to assess the association between serum albumin levels and lung function. To explore the potential associations between SA and pulmonary function, we employed multivariate linear regression, subgroup analysis, smoothing curve fitting and threshold effect.

Results

A positive correlation was observed between serum albumin levels and pulmonary function. In the model with a fully adjusted, each 1 g/dL serum albumin increase in SA corresponded to an increase of 2.69% in FVC%pred, 5.8% in FEV1%pred, 10.99% in FEF25–75%pred and 2.98% in FEV1/FVC%pred. This association between SA and FEV1%pred differed across gender subgroups. A non-linear relationship was observed between SA and FEV1/FVC%pred.

Conclusion

Our results demonstrated a positive correlation between SA and lung function, suggesting a novel modality for evaluating pulmonary function, specifically in children.

Clinical trial number

Not applicable.

Peer Review reports

Introduction

Pulmonary function tests (PFTs) are fundamental examination methods for assessing general respiratory health [1]. PFTs enable to determine many lung conditions and help physicians to identify a lot of non-pulmonary disease processes by detecting respiratory gas flow quantity, volume and other indicators [2]. Currently, the common clinical indices assessed by PFTs are forced vital capacity (FVC), forced expiratory volume in 1s (FEV1), the FEV1/FVC ratio, and forced expiratory flow 25–75% (FEF25-75%). It has been demonstrated that lung growth ends at about 18 years for females and 20 years for males, and lung function will peak at these ages, then reduce thereafter [3]. However, conducting PFTs in children presents significant challenges and exhibits greater variability compared to adults. This is largely attributed to the differences in the physiology of chest wall muscles and the cognitive development of pediatric patients [4].

Serum albumin (SA), the most prevalent protein, maintains around 80% of the colloidal plasma osmotic pressure [5]. It also has many other biological functions. It binds and transports many endogenous compounds, such as unconjugated bilirubin [6], cholesterol [7] and thyroxine [8]. As the circulating antioxidant, it can scavenge oxygen as well as nitrogen-reactive species [9, 10]. Moreover, serum albumin levels may affect the efficacy and toxicity of drugs and disease progression [11]. A large study in about 8,750 acute myocardial infarction showed that the risk of cardiovascular prevalence and early mortality increased as serum albumin concentrations decreased [12]. It is utilized in chronic and critically ill patients as a biomarker for nutritional status and disease severity [13,14,15]. In cystic fibrosis (CF) pediatric patients, A 0.1 mg increase in serum albumin was linked to a 2.7% increase in FEV1% [16]. Relative to CKD5 patients and healthy controls, patients undergoing continuous ambulatory peritoneal dialysis had Lower vital capacity, furthermore the lung function was positively associated with albumin level [17]. Previous research among the U.S. population reported a linear and positive relationship between SA levels and FVC in the general population during the years 2013 to 2014 [18]. However, the relationship between these two important indicators in children remains unclear.

National Health and Nutrition Examination Survey (NHANES) obtains continuous data from representative samples across every state in U.S., providing comprehensive and reliable support for cross-sectional studies [19]. The diverse population samples enhance the rigor and reliability of this study. Therefore, we will use NHANES data to examine if SA levels affect pulmonary function and provide a new way of assessing pulmonary function specifically for children.

Methods

Study population

The cross-sectional data from NHANES, a nationally representative study conducted by the National Center for Health Statistics (NCHS). Individuals gave informed consent, and the review was conducted and approved by the NCHS Ethics Review Board. The complete study design and data can be accessed by the public on the website of the NCHS (https://www.cdc.gov/nchs/nhanes/index.htm). Our research subjects is based on NHANES data from 2007 to 2012. In our analysis, participants with complete data about SA and lung function were enrolled. In this study, after excluding lacking serum albumin (n = 11,229), lung function metrics data (n = 3,496), and participants>19 years old (n = 12,645). Ultimately, the analysis encompassed a total of 3,072 participants (Fig. 1).

Fig. 1
figure 1

Flow chart of participants selection. NHANES, National Health and Nutrition Examination Survey

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Exposure and outcomes

SA (g/dL)

The LX20 and DcX800 techniques were employed for the determination of albumin levels, by tracking the absorbance variation at 600 nm, correlating linearly with the albumin content in the specimens.

Pulmonary function

Pulmonary function data were available only in the NHANES cycles for 2007–2008, 2009–2010, and 2011–2012. Testing procedures compliance the recommendations of the American Thoracic Society (ATS). NHANES spirometry training and quality control consultants were served by the NIOSH Division of Respiratory Disease Studies. Pulmonary function was assessed using FVC, FEV1, FEV1/FVC, and FEF25–75% as the primary outcome indicators. Measured values were transformed into predicted percentages using Global race-neutral reference Eq. [4].

Description of confounding variables

The confounding variables were incorporated: age (years), sex (male/female), race (Mexican American/other Hispanic/non-Hispanic White/non-Hispanic Black/other race), PIR (ratio of family income to poverty), waist (cm), height (cm), alanine transaminase (ALT, U/L), Creatinine (mmol/L), serum globulin(g/dl), total calcium (mmol/L), Cholesterol (mmol/L), thoracic/abdominal surgery (yes/no), smoking status (yes/no) and second-hand smoke (yes/no), presence of respiratory disease (yes/no) and asthma (yes/no). The body mass index (BMI, kg/m2) is categorized into ranges of < 25, 25–30, and > 30 kg/m2, representing normal, overweight, and obese, in that order. Individuals were classified as smokers if their blood cotinine levels exceeded 1 ng/ml. Survey participants are asked about exposure to second hand smoke exposure at work or inside home. The history of asthma was determined through respiratory a questionnaire survey.

Statistical analysis

Data analysis was conducted using R software (version 4.2) and EmpowerStats package (version 5.0), with all computations weighted in alignment with the guidelines of the NHANES. During the demographic analysis phase, categorized by serum albumin concentration. Categorical data were analysed by Chi-square, while continuous data by t-tests. Multivariate logistic regression analyses were employed to address the association between serum albumin and pulmonary function. In Model 1, we did not incorporate any covariates for adjustment. In Model 2, adjustment variables included age, gender and race. All factors were taken into account and adjusted for in Model 3. We employed a weighted generalized additive model, incorporating smooth curve fitting. In cases where a non-linear association was identified, we deployed a segmented linear regression model to delve deeper into potential threshold effects. Additionally, further stratified analyses and interaction tests were implemented to ascertain the association between serum albumin and pulmonary function. P < 0.05 was deemed to be significant.

Results

The baseline characteristics of the subjects are displayed in Table 1. Following rigorous screening, our study included 3,072 adolescents aged 12–19 years, with a median age of 15.50 years, and 47.17% of them were female. The mean serum albumin was 4.43 g/dl, and the averages for tertile 1–3 were 4.03 ± 0.21, 4.40 ± 0.08, and 4.75 ± 0.16, respectively. Compared to tertile 1–2, participants in tertile 3 had higher pulmonary function. The analysis revealed that age, gender, race/ethnicity, PIR, BMI, waist circumference, height, ALT, total calcium, serum globulin, creatinine, cholesterol, respiratory disease, asthma, smoking status, and exposure to second-hand smoke were all statistically significant covariates (P < 0.05). In contrast, thoracic/abdominal surgery showed no statistical significance (P > 0.05). Subjects with higher pulmonary function (tertile 3) were predominantly older males from Mexican American, other Hispanic, or non-Hispanic White backgrounds, and they belonged to other racial groups. This group typically did not smoke, had no respiratory diseases or asthma, exhibited lower BMI, serum globulin levels, and household income, and had higher levels of height, total calcium, creatinine, ALT, and cholesterol.

Table 1 Baseline characteristics of participants stratified by SA tri-sectional quantiles
Full size table

Table 2 presents the findings from multiple linear regression analyses examining the relationship between SA levels and pulmonary function. In model 1, there was a strong positive correlation between SA and pulmonary function, with effect values notably higher than in the other models. In model 3, for each 1 g/dL increase in SA, there was a corresponding 2.69% rise in FVC%pred [2.69(0.87, 4.50)], 5.8% increase in FEV1%pred [5.80(3.91, 7.69)], 10.99% increase in FEF25–75%pred [10.99(7.31, 14.66)] and 2.98% increase in FEV1/FVC%pred [2.98(1.87,4.08)]. The group with high concentration exhibited markedly higher lung function values than the group with medium concentration, when the low-concentration group was used as a reference.

Table 2 The associations between SA (g/dL) and FVC%pred, FEV1%pred, FEF25–75%pred, FEV1/FVC%pred
Full size table

Based on our results, we examined the relationship between SA and pulmonary function through subgroup analysis (Table 3). The subgroup variables included gender, race, BMI, thoracic/abdominal surgery, respiratory disease, asthma, smoking status, and exposure to second-hand smoke. We did not find significant interactions for race, BMI, thoracic/abdominal surgery, respiratory disease, asthma, smoking status, or second-hand smoke (all P for interaction > 0.05). Nonetheless, a statistically significant difference was observed for gender (P for interaction = 0.0169).

Table 3 Subgroup analysis of the association between SA (g/dL) and FVC%pred, FEV1%pred, FEF25–75%pred
Full size table

A non-linear relationship was revealed between SA and FEV1/FVC%pred with turning point observed at 4.8 g/dL (Table 4; Fig. 2). A significant positive relationship exists on both sides of the turning point. We further addressed the non-linearity for gender, while it exhibited a non-linear relationship between SA and FEV1%pred in female participants with a turning point calculated at 4.5 g/dL (Table 5; Fig. 3). When albumin was < 4.5 g/dL, FEV1%pred (β = 5.93, CI: 2.73, 9.13) displayed a positive association with increasing SA levels. However, when albumin was > 4.5 g/dL, no statistically significant link was observed. For males, FEV1%pred exhibited no non-linear association with SA.

Table 4 Analysis of threshold and saturation effects
Full size table
Fig. 2
figure 2

The relationship between SA (g/dL) and FVC%pred, FEV1%pred, FEF25–75%pred, FEV1/FVC%pred. The solid red line represents the smooth curve fit between variables. Blue bands represent the 95% of confidence interval from the fit. (A) SA and FVC%pred; (B) SA andFEV1%pred; (C) SA FEF25-75%pred and (D) SA and FEV1/FVC%pred

Full size image
Table 5 Analysis of threshold and saturation effects between SA and FEV1%pred stratified by gender
Full size table
Fig. 3
figure 3

The relationship between SA (g/dL) and FEV1%pred stratified by gender

Full size image

Discussion

Our cross-sectional study findings indicate that serum albumin concentration is significantly associated with improved lung function in adolescents aged 12 to 19 years, even after adjusting for all potential confounding factors. Furthermore, this relationship exhibits gender heterogeneity, suggesting that the impact of serum albumin on lung function may differ between males and females.

Impaired lung development during adolescence is associated with an increased risk of chronic lung diseases such as COPD in the future. Approximately 85% of individuals who develop COPD in early adulthood exhibit impaired lung function during childhood and adolescence [20]. Spirometry is an important tool for assessing chronic lung diseases. However, there are many contraindications for pulmonary function testing in children, such as pneumothorax, active infections (including tuberculosis), hemoptysis, and severe arrhythmias [1]. Therefore, finding alternative indicators to spirometry is significant. Serum albumin (SA) is a common diagnostic marker [21,22,23] and has become an outcome indicator for various diseases, including coronary artery disease [24], liver disease [25], and kidney injury [26]. Additionally, a previous study involving 85 patients aged 6 to 18 with cystic fibrosis indicated that albumin levels of 4.1 mg/dL or lower were associated with declines in FEV1 [27]. Ju et al. reported that bronchiectasis patients with low SA had lower FEV1 compared to those with normal SA levels [28]. Our results are consistent with these previous findings, indicating that higher SA levels are associated with better lung function.

Although the exact mechanism by which serum albumin affects lung function is not well understood, several studies have demonstrated an association between them. Numerous investigations have demonstrated a link between reduced albumin levels and diminished muscular strength [29, 30]. Reduced serum albumin levels could be a contributing risk factor for sarcopenia [31], and low pulmonary function is closely related to sarcopenia in older population samples [32]. Additionally, the improvement in lung function associated with high serum albumin levels may be attributed to the anti-inflammatory properties of albumin. Albumin has been shown to make a significant contribution to systemic antioxidant capacity and possesses anti-inflammatory functions [33]. Glutathione, a vital protective antioxidant in the lung, plays a key role in buffering antioxidant potential and inhibiting oxidant-mediated inflammatory responses [34]. Enteral and parenteral nutrition support has been demonstrated to effectively increase SA levels and lung function in patients with COPD and respiratory failure while also reducing inflammatory factors and oxidative stress markers [35]. Persistently low albumin levels may indicate ongoing inflammation and are associated with progressive fibrotic interstitial lung disease [36]. When an inflammatory response occurs, interleukin-6 released by granulocytes and monocytes inhibits albumin synthesis and promotes lung fibroblast proliferation, leading to idiopathic pulmonary fibrosis [37,38,39].

The anatomical and physiological differences in the respiratory system between genders have been extensively documented. Research indicates that female with COPD experience distinct disease burdens, symptoms, and clinical trajectories compared to their male counterparts [40, 41]. A meta-analysis of 11 longitudinal studies demonstrated that, after adjusting for smoking exposure, the rate of decline in lung function is significantly faster in females than in males [42]. This disparity may be attributed to women’s production of lower levels of reactive oxygen species, slower telomere shortening, and inherently longer telomeres compared to men, thereby affording them some protection against age-related biological processes [43, 44]. Furthermore, the growth patterns of airways and lung parenchyma also exhibit pronounced gender differences. Males typically experience an increase in smooth muscle mass and thickening of the airway walls, which contribute to a reduced forced expiratory flow relative to females [45, 46]. In neonatal intensive care settings, male infants face a higher risk of respiratory distress syndrome and subsequent bronchopulmonary dysplasia, a phenomenon likely linked to the earlier surfactant production in female fetuses, increased oral motor activity, larger airway development, lower reactivity to stimuli, and more mature parenchymal development [47]. Our findings extend these existing theories by revealing significant gender disparities in the association between SA levels and lung function. These differences underscore the necessity for gender-specific approaches in the assessment and management of pulmonary conditions.

There are a number of shortcomings in our study. First, a variety of relevant variables affect serum albumin levels, such as infectious diseases, chronic renal failure, malnutrition, cacotrophy, and cancer, We cannot adjust all potential factors. Secondly, it was unable to explain the causal inference between two factors and requires more prospective validations in the future. Despite these constraints, our research presents numerous strengths. Our research marks the initial investigation into the relationship between SA and pulmonary function in adolescents. In addition, our study incorporated a more extensive and nationally representative sample, thereby lending greater credibility to our results.

Conclusion

Serum albumin level is positively correlated with pulmonary function in adolescents aged 12 to 19 years. Serum albumin may be used as a new tool of assessing pulmonary function for children. In the future, multicenter, prospective large-scale clinical studies are needed to validate the robustness of our results.

Data availability

The survey data are publicly available on the internet for data users and researchers throughout the world http://www.cdc.gov/nchs/nhanes/.

Abbreviations

NHANES:

National Health and Nutrition Examination Survey

PFTs:

Pulmonary function tests

FVC:

Forced Vital Capacity

FEV1:

Forced Expiratory Volume in one second

FEF25:

75%-Forced Expiratory Flow 25-75%

NCHS:

National Center for Health Statistics

PIR:

Income-to-Poverty Ratio

BMI:

Body mass index

ALT:

Alanine aminotransferase

AST:

Asparate aminotransferase

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Acknowledgements

We would like to thank the staff and the participants of the NHANES study.

Funding

This work did not receive any specific grant from any funding agency in the public, commercial, or not-for-profit sector.

Author information

Authors and Affiliations

  1. Department of Pulmonology, Heyuan Hospital of Traditional Chinese Medicine, Heyuan, China

    Qiao Liu & Yuling Luo

  2. The 4rd Department of Orthopaedics and Traumatology, Heyuan Hospital of Traditional Chinese Medicine, Heyuan, China

    Biao Wu

  3. Department of Hand & Microsurgery, The Affiliated Nanhua Hospital, Hengyang Medical school, University of South China, Hengyang, China

    Ruijie Xie

  4. Department of Encephalopathy, Heyuan Hospital of Traditional Chinese Medicine, Heyuan, China

    Du Zheng

  5. The 2rd Department of Orthopaedics and Traumatology, Heyuan Hospital of Traditional Chinese Medicine, Heyuan, China

    Guang Liu

  6. Department of Critical Care Medicine, Heyuan Hospital of Traditional Chinese Medicine, Heyuan, China

    Huihai Zhang

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Contributions

Q.L., B.W. and R.X. designed the research. Q.L., Y.L., and D.Z. collected and analysed the data. G.L. and H.Z. prepared Figs. 1, 2 and 3; Tables 1, 2, 3, 4 and 5. Q.L. and B.W. drafted the manuscript. Q.L. and R.X. revised the manuscript. All authors contributed to the article and approved the submitted version.

Corresponding author

Correspondence to Qiao Liu.

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The studies involving human participants, human materials, or human data were reviewed and approved by the National Center for Health Statistics. The patients/ participants provided their written informed consent to participate in this study.

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Liu, Q., Wu, B., Xie, R. et al. Association between serum albumin and pulmonary function in adolescents: analyses of NHANES 2007–2012. BMC Pulm Med 24, 554 (2024). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12890-024-03341-x

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  • DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12890-024-03341-x

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BMC Pulmonary Medicine

ISSN: 1471-2466

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