Nationwide Trends in Osteoporosis in Koreans With Disabilities From 2008 to 2017

ABSTRACT This study examined the 10‐year trends in the prevalence of osteoporosis according to disability grade and type compared with those without disabilities in South Korea. We linked national disability registration data with the National Health Insurance claims data. Age‐ and sex‐standardized prevalence of osteoporosis were analyzed from 2008 to 2017 according to sex, disability type, and disability grade. Adjusted odds ratios for osteoporosis according to disability characteristics in the most recent years' data were also confirmed by multivariate analysis. Over the past decade, the prevalence of osteoporosis has increased in people with disabilities compared with people without disabilities, and the gap has gradually widened from 7% to 15%. By analysis of the most recent year data, both male and female individuals with disabilities had a higher risk of osteoporosis than those without disability (odds ratios [OR] 1.72, 95% confidence interval [CI] 1.70–1.73 in males; OR 1.28, 95% CI 1.27–1.28 in females); the multivariate‐adjusted OR was especially prominent in disability related to respiratory disease (OR 2.07, 95% CI 1.93–2.21 in males; OR 1.74; 95% CI 1.60–1.90 in females), epilepsy (OR 2.16, 95% CI 1.78–2.61 in males; OR 1.71; 95% CI 1.53–1.91 in females), and physical disability types (OR 2.09, 95% CI 2.06–2.21 in males; OR 1.70; 95% CI 1.69–1.71 in females). In conclusion, the prevalence and risk of osteoporosis have increased in people with disabilities in Korea. In particular, the risk of osteoporosis increases significantly in people with respiratory diseases, epilepsy, and physical disability types. © 2023 The Authors. JBMR Plus published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research.

osteoporosis in all individuals (40-79 years old) was 13.1% for men and 24.3% for women, satisfying the WHO criteria (15) in 2010. Another study reported that the prevalence of osteoporosis in Korea was 7.3% in men and 38.0% in women aged ≥50 years, and the prevalence of osteopenia in Korea was 46.5% in men and 48.7% in women aged ≥50 years in 2014. (16) Osteoporosis commonly occurs at the onset of disability, regardless of etiology. (17)(18)(19) However, osteoporosis in people with disabilities has not been well studied. In a previous review of intellectual disabilities, including learning disabilities and intellectual and developmental disability, the association between disability and osteoporosis was surveyed. (20) However, no studies could be included in the review; the authors failed to explain this association. (20) In particular, it is difficult to prevent and treat osteoporosis and osteoporotic fractures in patients with disabilities because they have low accessibility to medical services owing to environmental and economic reasons. In addition, only few studies have evaluated the association between osteoporosis and disability in the entire population. population of South Korea, maintained by the NHIS. (21) From this dataset, we extracted information on the history of inpatient and ambulatory care, drug prescriptions, comorbidities, and sociodemographic variables including age, sex, insurance premium, income level, and residential area.
Using the national disability registration data (NDRD), we collected information disability types and severity levels. The NDRD comprises data from the national registration system for people with disabilities primarily for the provision of welfare benefit. (22) Its registration requires submission of appropriate and validated documentation to a local National Pension Service office. The paperwork includes appraised results of disability diagnosis by a specialist physician in the corresponding field according to detailed criteria for the specific disability, as defined by the national disability registration system. (23) The database covers 93.8% of the total population with disabilities in 2011. (24) Using the Korean personal identification number, disability types and severity levels were linked with the variables selected from the NHID, as mentioned in the previous paragraph. After excluding individuals with a history of Paget's disease and cancer for each year, we analyzed data from more than 50 million individuals throughout the 10-year period (Fig. 1).  Note: Value of p indicates a significant difference between people with and without disabilities. Abbreviation: SD = standard deviation. Other variables collected from the NHIS database included age, sex, insurance premium, residential area, and comorbidities. As a proxy measure for actual household income, we used the insurance premium categories of medical aid in quintiles: I (lowest), II, III, and IV (highest), as provided by the NHIS. Insurance premiums were calculated based on income, property, and automobile taxes for each household. Residential areas were grouped into three categories: metropolitan, urban, and rural, based on the Korean ZIP code. Comorbidities were considered potential confounding factors. Comorbidities including diabetes (E10-E14), chronic kidney disease (N18, Z49), and chronic obstructive pulmonary disease (J41-J43), were defined by ICD-10. The Charlson comorbidity index was used to group study participants into four categories based on the index score: 0, 1-2, 3-4, and ≥5 (the most severe). (25) The national disability registration data defines 15 categories of disability. Disability severity is officially graded from 1 (very severe) to 6 (very mild) based on functional losses and clinical impairment as determined by a medical specialist. In this study, disability severity was classified as severe (grades 1-3) or mild (grades 4-6).

Ethics approval statement
The study protocol was approved by the Institutional Review Board of Chungbuk National University (CBNU-202010-HRHR-0171).

Statistical analyses
In this serial cross-sectional study, we calculated the age-and sex-standardized osteoporosis prevalence for each calendar year from 2008 to 2017 according to disability presence and severity by sex and age group. We developed a multivariate logistic regression adjusting for age, income level, residence, comorbidities (diabetes, chronic kidney disease, chronic obstructive pulmonary disease), and Charlson comorbidity index to examine the association between disability and osteoporosis. All analyses were performed using the SAS software version 9Á4 (SAS Institute Inc., Cary, NC, USA). Two-sided p values of 0.05 were considered significant.

Study participants
The number and baseline characteristics of participants by age group, sex, disability, severity, and type of disability (Table S1) Table 3.  during the period (2008-2017) are summarized in Table 1. In the 2017 analysis, there was no difference in sex distribution compared with 2008, but the proportion of participants aged 50 years or older increased. The proportion of people with severe disabilities decreased from 42.8% to 39.7%, although there was no significant difference in the proportion of people with disabilities in the entire population (Table 1).
In the most recent year (2017), the number of individuals with and without disabilities was 2,365,082 (4.7%) and 48,053,570 (95.3%), respectively. The results of the comparison of the two groups are presented in Table 2. People with disability were older (59.7 AE 18.3 years in the with-disability group and 39.2 AE 20.8 years in the without disability group, p < 0.001), and the proportion of men with disabilities was higher (58.1% versus 50.1%, p < 0.001). Among the disabled, metropolitan residents (54.7% versus 62.8%, p < 0.001) were lower, and the percentage of those using medical aids according to income level was significantly higher (17.0% versus 2.0%, p < 0.001). In people with disability, the number of individuals with comorbidities such as diabetes, chronic kidney disease, and chronic obstructive pulmonary disease (COPD) and the comorbidity scores measured by Charlson comorbidity index were also significantly higher compared with those without disability (all p < 0.001). People with severe disability accounted for 39.3% of the disabled, with physical disability representing the highest percentage (50.6%) ( Table 2).    Prevalence of osteoporosis from 2008 to 2017 Table 3 shows the crude prevalence of osteoporosis according to the disability status from 2008 to 2017. Overall, people with disabilities, including males and females, had a higher rate of osteoporosis than those without disabilities throughout the 10-year period ( Table 3, Table S2). In addition, there were significant differences in the prevalence of osteoporosis in the people with disabilities compared with those without disabilities during the same period (from 2.1% to 5.6% in people without disabilities versus from 9.4% to 21% in people with disabilities, p < 0.001). These differences were more pronounced in patients with mild disabilities than in those with severe disabilities (from 11.4% to 25.2% in mild disabilities versus from 6.7% to 14.6% in severe disabilities, p < 0.001).
When assessing the prevalence of osteoporosis by year according to the type of disability, ostomy showed a steep rise, followed by hearing and physical disabilities (24%, 18%, and 13% differences, respectively). The differences of the type of disability between men and women are described in Table S2. The age-standardized prevalence of osteoporosis was also higher in both male and female individuals with disabilities than in those without disabilities in the most recent year analysis according to age group, sex, and disability status. The overall prevalence of osteoporosis was higher with age ( Fig. 2A-D). The gap in the prevalence of osteoporosis according to disability status showed the greatest difference in men in their 70s and women in their 60s (Fig. 3A,B). In the age-standardized analysis by severity and type of disability, osteoporosis in mild disability was more prevalent in women older than 50 years of age than in those with severe disability, and the most prevalent type of disability was respiratory disease in both the female and male groups (Table S3).

Risk factors for osteoporosis
The results of the multivariate analysis by sex, disability grade, and type are presented in Table 4. People with disability had a higher risk for osteoporosis (in both sexes) than those without disability (adjusted odds ratio [aOR] 1.72; 95% confidence interval [CI] 1.70-1.73 in males; aOR 1.28, 95% CI 1.27-1.28 in women). Similar results were observed in the 50 years and older groups (aOR 1.63, 95% CI 1.62-1.65 in men; aOR 1.28; 95% CI 1. 28-1.29 in women).
The risk factors, according to the severity and type of disability, showed different results in men and women. The risk of osteoporosis was high in all subtypes of disability in the male group with disability compared with the male group without disability. The OR for osteoporosis was high in both mild and severe disability groups without a difference according to the severity of the disorder. In particular, the risk of osteoporosis was highest in people with disabilities associated with liver disease (aOR 2.38, 95% CI 2.03-2.80), epilepsy (aOR 2.16, 95% CI 1.78-2.61), respiratory disease (aOR 2.07, 95% CI 1.93-2.21), and physical disability (aOR 2.09, 95% CI 2.04-2.11). In contrast, in the female group, the risk of osteoporosis was significantly high in the mild disability group (aOR 1.49, 95% CI 1.48-1.50) according to severity, respiratory disease-related disability (aOR 1.74, 95% CI 1.60-1.90), epilepsy (aOR 1.71, 95% CI 1.53-1.91), and physical disability (aOR 1.70, 95% CI 1.69-1.71, Table 4) related with disability type.

Discussion
In this study, the prevalence and risk of osteoporosis were higher in people with disabilities than in those without disabilities. The prevalence of osteoporosis between the groups with and without disability showed a significant difference over time. This  increase showed a marked trend in types such as ostomy, hearing, and physical disabilities. It is known that the most dominant risk factor for osteoporosis is age. (5) When the age-standardized prevalence of osteoporosis was analyzed with the most recent data from 2017, a high percentage of disability subtypes were respiratory disease and epilepsy in both the male and female groups in our study. Previous studies have reported that the risk of osteoporosis increases in patients with respiratory diseases including chronic obstructive lung disease, (26,27) asthma, (28) and interstitial lung disease. (29) There are various causes for this; in particular, inhaled corticosteroids or systemic corticosteroids seem to act as important factors. (28) The association between epilepsy, use of antiepileptic drugs, and risk of osteoporotic fractures is well recognized. Several studies have reported that patients with epilepsy have an increased risk of skeletal fractures compared with the general population. (30)(31)(32) In the most recent data analysis, the top three types of disability with high multivariate-OR for osteoporosis in both sexes were respiratory disease ( . A similar trend was observed in the 50 years and older group. According to the severity of disability, the mild disability group showed a tendency to have a high OR of osteoporosis compared with the severe disability group, which was prominent in women. Several studies have examined the incidence of low BMD in both women and men with disabilities (33)(34)(35) but these studies were usually physical disability-specific, including spinal cord injury and neurologic deficits. Moreover, people who do not attain optimal bone mass during childhood and adolescence because of the early onset of disability may develop osteoporosis with accelerated bone loss. (36) In addition, previous studies have reported that people with physical disabilities, such as spinal cord injuries, also had various complications of fragility fractures, delayed diagnosis due to sensory loss, pressure sores, delayed union or nonunion, hip and knee joint loss of range of motion, increased muscle spasms, and autonomic dysreflexia. (36)(37)(38)(39)(40) People with disabilities have limitations of mobility, and they also have financial problems due to decreased economic activity; our research supports this. Table 2 shows that the ratio of those in the first quartile with low income and medical aid is significantly higher in people with disabilities than in those without. As access to medical facilities decreases, there are restrictions on the prevention and treatment of osteoporosis.
Our study had several limitations. We used the ICD code to define osteoporosis and could not present BMD measurements because of the limitations of medical insurance data. However, to be covered by health insurance for osteoporosis treatment, BMD tests and application of osteoporosis ICD-codes are required. Therefore, the application of ICD codes for osteoporosis is highly reliable in Korea, although there may be some underestimation. Second, our study did not fully evaluate factors that drugs, dietary habits, smoking, and alcohol consumption can affect osteoporosis. However, this study is significant as it is the first large-scale population-based study to show the prevalence of osteoporosis in people with disabilities compared to people without disabilities through a long-term follow-up of 10 years from 2008 to 2017. In addition, various subanalyses, including age, sex, comorbidities, severity, and type, were conducted to clarify the risk factors affecting osteoporosis in disabled people. This is also a strength of the present study.
In conclusion, people with disabilities had a high prevalence and increased risk of osteoporosis compared with people without disabilities in this study. The risk of osteoporosis was significantly high in people with respiratory diseases, epilepsy, and physical disabilities. Therefore, it is important to recognize the risk of osteoporosis in people with disabilities and actively prevent and treat it.