Chronic obstructive pulmonary disease

Low household income increases risks for chronic obstructive pulmonary disease in young population: a nationwide retrospective cohort study in South Korea

Abstract

Background Low socioeconomic status is a risk factor for chronic obstructive pulmonary disease (COPD); however, the association between low household income and COPD in young populations remains unclear.

Methods We screened individuals aged 20–39 years who underwent the national health examination between 2009 and 2012 using the Korean National Health Information Database, which was searched until December 2019. We identified 5 965 366 eligible individuals, and 13 296 had newly developed COPD based on health insurance claims. We evaluated household income levels based on the health insurance premiums, categorised them into quartiles and ‘Medical aid’ (the lowest 3% income group), and assessed the annual income status from the preceding 4 years. Multivariate Cox proportional hazard models were used to estimate the adjusted HR (aHR) of risk factors for COPD.

Results In the Medical aid group, the incidence rate for developing COPD was 0.56/1000 person-years, with an aHR of 2.45 (95% CI 1.91 to 3.13) compared with that of the highest income quartile group. This association was prominent in consecutive recipients of Medical aid (aHR 2.37, 95% CI 1.80 to 3.11) compared with those who had never been Medical aid beneficiaries. Those who experienced a decline in household income between the previous (preceding 4 years) and baseline time points had an increased risk of developing COPD, regardless of previous income status.

Conclusion Low household income was associated with an increased risk of developing COPD in the young population. This risk was augmented by sustained low income and declining income status.

What is already known on this topic

  • Low socioeconomic status, including factors like low household income, is a risk factor for COPD.

What this study adds

  • Low household income was associated with an increased risk of developing COPD in young populations. These risks were augmented by sustained low income and declining income status.

How this study might affect research, practice or policy

  • Attending physicians and the national health examination programme should focus on respiratory symptoms and impairments among individuals with low household income, even young individuals.

Introduction

Chronic obstructive pulmonary disease (COPD) is a heterogeneous lung condition with chronic respiratory symptoms caused by abnormalities of the airways or alveoli, leading to persistent and progressive airflow limitation.1 Prolonged exposure to cigarette smoke and noxious gases has been recognised as a cause of COPD.2 3 Furthermore, the recently updated COPD classification in Global Initiative for Chronic Obstructive Lung Disease 2023 guidelines has drawn clinicians’ attention to other potential risk factors for this disease, including occupational exposures, biomass fuel, air pollution, genetic variants, low birth weight, childhood respiratory illness, low socioeconomic status, male sex, asthma and respiratory infections.1–3

As a risk factor for COPD, low socioeconomic status encompasses low household income, low educational level, poor living conditions, malnutrition, poor access to healthcare, indoor and outdoor air pollution and poor water sanitation.4–9 Among these, low household income is a significant risk factor for COPD progression and exacerbation,5 and substantial financial burden may further limit access to healthcare services,10 11 which may increase mortality risk.12 Previous epidemiological studies showed that the prevalence and mortality of COPD were higher in low-income countries than in high-income countries.4 13 Furthermore, a recent study estimated that up to 6% of the population aged ≥40 years had chronic airflow obstruction attributable to poverty.14

The prevalence of COPD increases with age, and it has traditionally been considered a disease of older adults.3 15 However, some individuals under 50 years of age were diagnosed with COPD,16 and these patients were classified as ‘young COPD’.1 16 Globally, 49.3 million people aged 30–39 years were estimated to have COPD in 2019, with a prevalence of approximately 4%.3 Current guidelines do not recommend routine screening for COPD in the general population (asymptomatic adults). However, given the substantial morbidity and mortality associated with COPD, screening strategies for the selected high-risk group could be beneficial for young adults, considering potential benefits from early treatment of COPD.17 18 Thus, recognising young individuals with modifiable risk factors for COPD is important for national healthcare plans.

However, previous studies on low household income in COPD had several limitations in their study design, such as small cohort size,9 19 cross-sectional analysis of household income,4 8 9 20 21 lack of smoking history20 and inclusion of individuals with smoking history only.5 Furthermore, most previous studies included individuals aged >40 years.5 8 9 20–22 A study in China, which included individuals aged 15–69 years, described a significant relationship between low income and COPD prevalence; however, this was a cross-sectional study, and the multivariate model was adjusted for limited covariates, including age, sex, smoking and geographic regions.23 Thus, the association between low household income and COPD in young individuals requires further investigation.

This study evaluated whether low household income was a considerable risk factor for developing COPD in young individuals (20–39 years) with longitudinal household income data using the Korean National Health Information Database (NHID). To overcome the limitations in previous studies, we included approximately six million individuals, analysed temporal household income changes over 4 years and designed multivariate models with covariates, including anthropometric data, lifestyle habits, comorbidities and history of respiratory illness.

Methods

Data source

The Korean National Health Insurance Service (NHIS) provides a public database, the NHID, which includes data on national health examination, medical treatment and claims information, healthcare use, sociodemographic characteristics and mortality in the entire South Korean population since 2001.24 25 The Korean government runs a mandatory universal public health insurance system that covers approximately 97% of the population, and the NHIS is a single insurer. ‘Medical aid’ is a public assistance that uses government subsidies to provide low-income populations with healthcare services. Medical aid covers the 3% of the population in the lowest income bracket who cannot pay any insurance premium; however, the NHIS also takes care of all the administrative processes for the Medical aid recipients.

The NHIS has provided a national health examination for early detection and prevention of diseases since 1995.26 Until 2018, all adult employees or adults aged ≥40 years with national health insurance underwent a national health examination biannually (annually for manual workers), including simple chest radiographs, laboratory tests and questionnaires about lifestyle habits and medical history.25 27

Study population

Individuals aged 20–39 years who underwent a national health examination between 2009 and 2012 were eligible for inclusion. Our search of the NHID revealed 6 891 400 eligible individuals. We excluded 658 316 individuals with insufficient household income data, 4929 individuals with any insurance claim with International Classification of Diseases 10th Revision (ICD-10) codes for COPD before their health screening, 259 323 individuals with insufficient medical records and 3466 individuals with any insurance claim with ICD-10 codes for COPD within 1 year after the index date (1 year lag period). To exclude the possibility of over-detection of COPD after the health examination, we applied a 1 year lag period and started follow-up 1 year after the index date. The remaining 5 965 366 eligible individuals were included and followed up until December 2019, and 13 296 individuals were identified with newly developed COPD (online supplemental figure 1). Regarding the time frame, time zero started 1 year after the index date (lag period). The follow-up stopped at death, censor (eg, immigration) or COPD development (outcome).28 The mean follow-up duration was 8.35±1.15 years.

Outcome and household income ascertainment

The outcome of this study was new COPD development. We defined COPD as medical insurance claims of ICD-10 codes for COPD (J44.x) or emphysema (J43.x), except for J43.0 (unilateral pulmonary emphysema, Macleod’s syndrome), more than three times per year for at least 2 years (three times each year).28 29

The NHIS consists of a mandatory universal public health insurance system covering 97% of the Korean population and Medical aid covering 3% of the population in the lowest income bracket. The household income level was categorised into quartiles (Q1=the lowest and Q4=the highest) based on subscribers’ annual national health insurance premium, which is a proxy for household income.30–33 Individuals receiving Medical aid benefits were assessed as a separate income category (Medical aid, corresponding to the lowest income category). To evaluate the temporal change of household income status, we annually collected and categorised individuals’ household income status during the past 4 years before the baseline.

Covariates

Information on anthropometric measurements (body weight, height and blood pressure) and lifestyle habits (cigarette smoking, alcohol consumption and regular exercise) was collected from self-reported questionnaires on the national health examination within 2 years before the index date. Body mass index (BMI) was calculated by dividing the body weight by the height squared (kg/m2) and classified into five groups (<18.5, 18.5–22.9, 23–24.9, 25–29.9 and ≥30 kg/m2) according to the Asian BMI criteria.34 Cigarette smoking was classified into never-smoker, former smoker and current smoker groups. Alcohol consumption was classified as none, mild (<30 g/day) or heavy (≥30 g/day). Regular exercise was defined as >30 min of moderate physical activity at least five times per week or >20 min of strenuous physical activity at least three times per week.35 Residential regions were categorised into metropolitan (Seoul, Busan, Daegu, Incheon, Gwangju, Daejeon, Ulsan and Sejong) and other regions (Gyeonggi, Gangwon, Chungcheongbuk, Chungcheongnam, Jeollabuk, Jeollanam, Gyeongsangbuk, Gyeongsangnam and Jeju).

Comorbidities were identified using the NHIS and national health examination data within 1 year before the index date. Definitions were as follows: (1) diabetes, either an insurance claim for ICD-10 codes E11–14 with prescription of hypoglycaemic medications or a fasting serum glucose of ≥126 mg/dL in a health examination; (2) hypertension, either an insurance claim for ICD-10 codes I10–13 and I15 with a prescription of antihypertensive medications or high blood pressure (systolic blood pressure ≥140 mmHg or diastolic blood pressure ≥90 mmHg) measured during a health examination; (3) dyslipidaemia, either an insurance claim for ICD-10 code E78 with a prescription of lipid-lowering medications or serum total cholesterol of ≥240 mg/dL during a health examination; (4) chronic kidney disease, either an insurance claim for ICD-10 codes N18–19 or an estimated glomerular filtration rate of <60 mL/min/1.73 m2 by the Modification of Diet in Renal Disease equation during a health examination; (5) asthma, insurance claims of ICD-10 code for asthma (J45) more than three times per year and within 5 years before the COPD diagnosis; and (6) pneumonia, an insurance claim of hospitalisation for ICD-10 codes for pneumonia (J10.0, J11.0, J12–J18, or A481) within 5 years before the COPD diagnosis.

Statistical analysis

Continuous variables are presented as mean±SD, and categorical variables are expressed as numbers (percentage). Student’s t-test and χ2 test were used to compare continuous and categorical variables, respectively. The incidence rate of COPD was calculated as the ratio between the number of patients with newly developed COPD and the number of person-years at risk of COPD (per 1000). The Kaplan–Meier analysis was used to illustrate the cumulative incidence of COPD according to household income categories. A multivariate Cox proportional hazards model was used to assess the impact of risk factors on the time-to-event of COPD development. The proportional hazards assumption was checked using Schoenfeld residuals. Multicollinearity between covariates was measured using Variance Inflation Factor (online supplemental tables 1–3). Model 1 was non-adjusted. In Model 2, the covariates included age, sex and residential region. Model 3 included the covariates in Model 2 and BMI, cigarette smoking, alcohol consumption, regular exercise, diabetes, hypertension and dyslipidaemia. Model 4 (the main analysis model) contained covariates in Model 3 and asthma and pneumonia. In the multivariate analyses, age and BMI were included as continuous variables. All P values were two-tailed, with statistical significance set at p<0.05. All statistical analyses were performed using SAS version 9.4 (SAS institute, Cary, NC, United States), and the PHREG procedure was used for the Cox proportional hazards model.

Ethical statement

This study protocol was approved by the Institutional Review Board of Asan Medical Center, Seoul, Republic of Korea (approval no. 2022–1593). The requirement for informed consent was waived, as this was a retrospective study, and the data used were anonymised. This study complied with the guidelines stipulated in the Declaration of Helsinki, and all methods were performed in accordance with the relevant guidelines.

Patient and public involvement

Patients or the public were not involved in the design, conduct, reporting or dissemination plans of our research.

Results

Baseline characteristics

Table 1 shows the baseline characteristics of the study population according to the household income categories. The mean age of all participants was 30.91±4.99 years (men: 58.8%). The participants in the Medical aid group were predominantly young (62.4%, age <30 years) and underweight (12.5%, BMI <18.5 kg/m2). Regarding lifestyle habits, participants were predominantly never-smokers (68.1%) and non-alcohol drinkers (54.7%). Furthermore, a small proportion of the participants had a more frequent history of asthma (5.6%) and pneumonia (2.1%). Additionally, some difference in sexual proportion was observed between excluded and included populations (online supplemental table 4).

Table 1
|
Baseline characteristics of study population

Risk of COPD development according to household income status

Table 2 shows the associations between household income status and COPD development. According to the baseline household income status, the Medical aid group had an incidence rate of 0.56/1000 person-years for developing COPD. They had an increased risk of developing COPD (adjusted HR (aHR) 2.45, 95% CI 1.91 to 3.13) compared with the highest income group (Q4, figure 1). According to the household income status 4 years before baseline, individuals with Medical aid benefits had an incidence rate of 0.31/1000 person-years for developing COPD. They had an increased risk of developing COPD (aHR 1.77, 95% CI 1.51 to 2.07) compared with the highest income group (online supplemental table 5).

Figure 1
Figure 1

Cumulative incidence of chronic obstructive pulmonary disease (COPD) plotted using a Kaplan–Meier curve. (A) The development of COPD by baseline household income status. (B) The development of COPD by cumulative number of years of receiving Medical aid. COPD, chronic obstructive pulmonary disease; MA, Medical aid.

Table 2
|
Impact of low household income status on chronic obstructive pulmonary disease development

Risk of COPD development according to consecutive low household income

Table 3 shows the associations between the consecutive low household income status and COPD development. The risk for developing COPD increased with the cumulative number of Medical aid and was highest in individuals under the Medical aid benefit for 4 consecutive years compared with individuals without a history of Medical aid benefits (aHR 2.37, 85% CI 1.80 to 3.11, online supplemental table 6, figure 1).

Table 3
|
Impact of cumulative household income status on COPD development

Risk of COPD development according to the longitudinal household income changes

Table 4 shows the associations between the longitudinal household income change and COPD development. The household income status was compared between the baseline and 4 years before the baseline. A household income decline to the Medical aid group significantly increased the risk of developing COPD (Q3 to Medical aid, aHR 3.86, 95% CI 1.45 to 10.29; Q2 to Medical aid, aHR 2.50, 95% CI 1.12 to 5.56) compared with the risk in individuals who remained in their household income categories.

Table 4
|
Change of household income status between the two time points (4 years before the baseline vs baseline) and the corresponding risk of chronic obstructive pulmonary disease development

Discussion

In this nationwide population-based cohort study, which included approximately six million participants aged 20–39, we investigated the relationship between low household income and the new development of COPD. The baseline household income status of Medical aid beneficiaries was significantly associated with an increased risk of developing COPD. Individuals who consecutively received Medical aid benefits for the previous 4 years showed an increased risk of developing COPD compared with those who had never been Medical aid beneficiaries. In addition, a longitudinal household income decline to the Medical aid group was also significantly associated with an increased risk of developing COPD compared with those who maintained their household income status. Therefore, we suggest that low household income is an important risk factor for developing COPD in young individuals.

Previous studies have linked low household income status to increased COPD risk. One possible explanation is the association between financial vulnerability and other socioeconomic risk factors for COPD development, including cigarette smoking, alcohol consumption, malnutrition and limited access to healthcare facilities.36–39 In this study, individuals in the Medical aid group were prominently underweight (BMI <18.5 kg/m2), reflecting their poor nutritional status. However, they had a reduced history of cigarette smoking and alcohol consumption, suggesting that other factors may be associated with the risk of COPD.

Another possible explanation is the association between low household income and ambient air pollution, such as occupational exposure, biomass fuel and particulate matter.40 41 Low household income and financial instability can cause mental illness, such as depression and anxiety, which affects employment and household income, augmenting the risk for COPD.42 43 Low household income may be associated with impaired immune function and could be a precursor to chronic inflammatory disease.44 45 For example, a previous study reported the association between low socioeconomic status and DNA methylation, resulting in chronic inflammatory disease.46 Therefore, the effect of income status on COPD development in young individuals requires further investigation.

This study had some strengths. First, the large sample size of the nationwide population-based cohort enhanced the statistical power to determine the relationships between low household income and COPD development in young individuals. Second, using the NHID database, we analysed other medical comorbidities as covariates and tracked temporal household income changes 4 years before the initial diagnosis of COPD.

However, this study also had some limitations. First, owing to the limitations of national health examination data, the development of COPD was defined using the health insurance claims of relevant diagnostic codes, and lung function could not be evaluated. To overcome this, we defined COPD as insurance claims of COPD at least three times per year for at least 2 years to select patients with regular hospital visits for COPD. Second, regarding potential risk factors for COPD, other socioeconomic conditions, including low educational level, poor living conditions, malnutrition, poor access to healthcare and air pollution, could not be evaluated as covariates owing to the limitation of source data.4–9 Furthermore, some potential risk factors affecting lung function trajectories, such as low birth weight and childhood respiratory illness, could not be evaluated.1–3 47 Finally, this study was conducted among the Korean population; thus, generalising the results to other ethnicities requires caution. Nevertheless, our findings indicate that economically vulnerable young individuals are more susceptible to COPD. Further prospective large-scale cohort studies are required to ascertain our findings.

In conclusion, low household income at the time of the initial diagnosis was an important risk factor for developing COPD in young individuals. Furthermore, sustained low household income and longitudinal household income decline before the initial diagnosis were also significantly associated with COPD development. These findings suggest that attending physicians and the national health examination programme should focus on respiratory symptoms and impairments among individuals with low household income, even in young individuals.