The prevalence of osteoporosis in Korean ... - Wiley Online Library

JBMR

ORIGINAL ARTICLE

The Prevalence of Osteoporosis in Korean Adults Aged 50 Years or Older and the Higher Diagnosis Rates in Women Who Were Beneficiaries of a National Screening Program: The Korea National Health and Nutrition Examination Survey 2008–2009 Yong Jun Choi , 1 Han Jin Oh , 2 Dae Jung Kim , 1 Yunhwan Lee , 3,4 and Yoon-Sok Chung1,4 1

Department of Endocrinology and Metabolism, Ajou University School of Medicine, Suwon, South Korea Department of Family Medicine, College of Medicine, Kwandong University, Gangneung, South Korea 3 Department of Preventive Medicine & Public Health, Ajou University School of Medicine, Suwon, South Korea 4 Institute on Aging, Ajou University Medical Center, Suwon, South Korea 2

ABSTRACT For the prevention of osteoporotic fracture, adequate screening and treatment are important. However, there are few published data on diagnosis and treatment rates of osteoporosis in Asia. We used data from the fourth Korea National Health and Nutrition Examination Survey 2008–2009 to estimate the nationwide prevalence, physician diagnosis rate, and treatment rate of osteoporosis in adults aged 50 years and older. The bone mineral density (BMD) measurements of central skeletal sites (lumbar spine, femoral neck, and total hip) were obtained using dual-energy X-ray absorptiometry (DXA) (Discovery-W; Hologic Inc., Waltham, MA, USA). Diagnosis of osteopenia or osteoporosis was defined by the World Health Organization (WHO) T-score criteria. The prevalence of osteoporosis in adults aged 50 years or older was 35.5% in women and 7.5% in men. The prevalence of osteoporosis in Korea was similar to other East Asian countries but higher than that in Caucasians. Lumbar spine bone density T-scores tended to be lower than those of the femoral neck or hip. The estimated diagnosis rate was 26.2% (women 29.9%, men 5.8%) and the treatment rate was 12.8% (women 14.4%, men 4.0%). The physician diagnosis rate was significantly higher in females aged 66 to 68 years who were the beneficiaries of the national screening program than that in females of other ages (43.6% versus 28.1%, p < 0.05). The national screening program for osteoporosis may have contributed to an increased diagnosis rate in older Korean women. However, it was evident that treatment following a diagnosis of osteoporosis was still inadequate. ß 2012 American Society for Bone and Mineral Research. KEY WORDS: OSTEOPOROSIS; PREVALENCE; DIAGNOSIS; TREATMENT; KOREA

Introduction

G

iven a progressive increase in the size of the world’s elderly population, osteoporosis has become an important global health problem.(1) Moreover, the Asian region is considered to be on the verge of an emerging osteoporosis epidemic. It is estimated that 50% of the world’s osteoporotic hip fractures will occur in Asian women by 2050.(2) Patients with osteoporosis have a higher risk of hip fracture, which is a major cause of morbidity and mortality.(3) The 1-year mortality for hip fracture among the elderly population in Korea was 16.6%, which is 2.85 times higher than the mortality rate for the general population (5.8%), based on Korean National Health Insurance claims data.(4) For the prevention of osteoporotic fracture, adequate screening

and treatment are important. However, despite the recommendation of the U.S. Preventive Services Task Force, the National Osteoporosis Foundation, and the American College of Physicians,(5–7) most individuals with osteoporosis remain undiagnosed and untreated in the United States.(8–10) Moreover, there have been few published data on diagnosis and treatment rate of osteoporosis in Asia. The prevalence of osteoporosis varies according to sex, race, design, and region. In the United States and Canada, about 10% of all postmenopausal women have osteoporosis.(11,12) In Korea, a paucity of studies have been conducted on osteoporosis prevalence.(13,14) Previous studies have been regionally based; thus, reliable nationwide data on the prevalence of osteoporosis and osteopenia are not available. In this study, we investigated

Received in original form September 3, 2011; revised form March 16, 2012; accepted April 2, 2012. Published online April 24, 2012. Address correspondence to: Yoon-Sok Chung, MD, PhD, Department of Endocrinology and Metabolism, Ajou University School of Medicine, San 5 Wonchon-dong, Yeongtong-gu, Suwon, 443-721, South Korea. E-mail: [email protected] Journal of Bone and Mineral Research, Vol. 27, No. 9, September 2012, pp 1879–1886 DOI: 10.1002/jbmr.1635 ß 2012 American Society for Bone and Mineral Research

1879

the prevalence of osteoporosis as well as its management status, based on an analysis of the diagnosis and treatment rates of osteoporosis among Korean adults aged 50 years or older using data from the Korea National Health and Nutrition Examination Survey (KNHANES), a nationwide survey of residents in Korea. In 1988, Korea launched the National Screening Program, which targeted chronic disorders such as hypertension and diabetes mellitus. To advance the program, the Ministry of Health and Welfare of Korea introduced a new national screening program entitled, the ‘‘Screening Program for Transitional Ages,’’ which has targeted those aged 40 and 66 years. As part of the program since 2007, bone mineral density (BMD) measurements for women have been performed for the 66-year-old age group only.(15) We also compared the physician diagnosis and treatment rate between beneficiaries and nonbeneficiaries of the screening program to evaluate the effects of the screening program on the diagnosis and treatment rate in Korean women.

Materials and Methods The Ministry of Health and Welfare of Korea has conducted KNHANES every 3 to 4 years since 1998 to examine the general health and nutrition status of Koreans.(16,17) KNHANES is a crosssectional, nationally representative survey, using a stratified multistage sampling design. The fourth KNHANES was conducted during the period from July 2007 to December 2009. KNHANES consisted of four different measures: a health interview, a health behavior survey, a health examination, and a nutrition survey. In the fourth KNHANES, 31,705 individuals aged >1 year were sampled by the health interview and examination (6455 in 2007; 12,528 in 2008; and 12,722 in 2009); these individuals represented 9421 households (1739 in 2007; 3707 in 2008; and 3975 in 2009). From the 31,705 initial sample, 24,871 individuals participated in the survey (4594 in 2007; 9744 in 2008; and 10,533 in 2009), with a response rate of 78.4% (71.2% in 2007; 77.8% in 2008; and 82.8% in 2009). The osteoporosis examination began during the second year of the

fourth KNHANES (2008); therefore, BMD measurements were not obtained from those participants evaluated in 2007; therefore, those participants were excluded from the present study (n ¼ 4594). From the 20,277 participants during 2008–2009, a total of 10,649 individuals underwent femur and lumbar spine BMD measurements. In the present study, we analyzed the data from 4946 subjects (2851 women and 2095 men) aged 50 years (Fig. 1).

Measurements of anthropometric parameters and BMD Height and body weight were measured by standard method in light clothes. Body mass index (BMI) was calculated as weight divided by height squared (kg/m2). The BMD (g/cm2) measurements of central skeletal sites (lumbar spine, femoral neck, and total hip) were obtained using dual-energy X-ray absorptiometry (DXA) (Discovery-W; Hologic Inc., Waltham, MA, USA) in the vehicle carrying the machine. BMD measurements were performed according to the recommendation of the International Society for Clinical Densitometry (ISCD) in 2007.(18) For lumbar spine BMD, the L1 to L4 value was chosen for analyses, and when the specific vertebrae were not suitable for analysis due to compression fracture, degenerative changes, or any other reason, BMD was calculated excluding the affected vertebrae. Diagnosis of osteopenia or osteoporosis were made using the World Health Organization (WHO) T-score criteria (2.5 < T-score < 1 or T-score 2.5, respectively) calculated from the Asian reference data.

Measurement of serum 25 hydroxyvitamin D For measurements of serum 25 hydroxyvitamin D [25(OH)D] levels, blood samples of individual subjects were collected. Of the original 2851 subjects, 2701 (94.7%) had 25(OH)D levels taken. On the same day, the samples were properly processed, refrigerated, and transported in cold storage to the Central Laboratory in Seoul, Korea. Serum 25(OH)D levels were measured using a g-counter (1470 Wizard; Perkin-Elmer, Turku, Finland) with radioimmunoassay method (DiaSorin, Stillwater, MN, USA).

Fig. 1. Subject selection process in this study.

1880

CHOI ET AL.

Journal of Bone and Mineral Research

The interassay coefficients of variation were 11.7%, 10.5%, 8.6%, and 12.5%, at 8.6, 22.7, 33.0, and 49.0 ng/mL, respectively.

Physician diagnosis rate and treatment rate Those who answered ‘‘yes’’ to the question; ‘‘Have you ever been diagnosed with osteoporosis by a physician?’’ were classified as known cases of osteoporosis. Those who were first diagnosed with osteoporosis in this study were classified as newly diagnosed cases of osteoporosis. The number of people with osteoporosis was the sum of the known cases of osteoporosis and the newly diagnosed cases of osteoporosis. The physician diagnosis rate was determined as the number of known cases of osteoporosis divided by the total number of people with osteoporosis. The treatment rate was determined as the number of patients who answered ‘‘yes’’ to the question; ‘‘Are you currently taking osteoporosis medication?’’ divided by the total number of osteoporosis patients, including those with known and newly diagnosed osteoporosis. The treatment rate for known osteoporosis was also obtained.

BMD measurements. For continuous variables, the PASW complex-samples general linear models were used, and for categorical or ordinal variables, the PASW complex-samples crosstabs procedure was used. Additionally, an age-stratified analysis was performed to compare the diagnosis and treatment rate between those who would have been in the age range to benefit from the screening program (females aged 66–68 years) and those who would have not received any special screening recommendation. The PASW complex-samples crosstabs procedure was used to compare physician diagnosis rate and treatment rate between females aged 66 to 68 years and the remaining females of other ages (ie, females aged 50 [except for 66–68] years) and the medical screening rate of known cases of osteoporosis between females aged 66 to 68 years and the adjacent age groups (ie, females aged 63–65 and 69–71 years). All statistical analyses were conducted using PASW 18.0 (SPSS Inc., Chicago, IL, USA). Values of p < 0.05 were considered statistically significant.

Covariates

Results

The participants also received standardized questionnaires on lifestyle, medical and family history, socioeconomic status, household income, and education. Household income was divided into quartiles. Educational background status was divided into elementary school graduate, middle school graduate, high school graduate, and college graduate or above. Residential area was divided into urban and rural categories. A positive history of fracture was defined as self-reported fracture of physician-diagnosed fracture at hip, wrist, or spine. A positive family history of osteoporosis was defined as a self-reported history of physician-diagnosed osteoporosis or kyphosis or fracture with minor trauma in the participant’s first-degree relatives. The information on current smoking, alcohol drinking (5 units a day), menopausal status, having general medical examination, taking regular exercise (walking for over 30 minutes or taking a moderate degree of physical activity, five times a week) was also obtained from the participant’s questionnaire.

Figure 2 presents the prevalence of osteoporosis and osteopenia in KNHANES (2008–2009). The prevalence of osteoporosis in adults aged 50 years was 35.5% in women and 7.5% in men. The prevalence of known cases of osteoporosis was 10.6% in women and 0.4% in men, and the prevalence of subjects with newly diagnosed osteoporosis was 24.9% in women and 7.1% in men. In addition, the prevalence of osteopenia was 46.7% in women and 47.2% in men aged 50 years according to the WHO criteria. Based on prevalence estimates and National Census Data in 2005 from the Korea National Statistical Office, the number of Korean adults with osteoporosis or osteopenia was estimated to be about 2.8 million (2.4 in women, 0.4 in men) and 5.9 million (3.1 in women, 2.8 in men), respectively. The prevalence of osteoporosis increased with age and reached its peak in the aged 70 years group. In Table 1, the demographic and biological characteristics of normal, osteopenic, and osteoporotic study subjects are presented. Compared with normal subjects, men and women with osteopenia or osteoporosis were older, and had lower height, weight, BMI, lumbar spine BMD, total hip BMD, femoral neck BMD, household income, education level, and likelihood of having general medical examination. Among women, there were significant differences between normal subjects and those with osteopenia or osteoporosis regarding residential area, history of fracture, smoking habits, menopausal status, and exercise frequency. There were no differences in vitamin D levels among normal, osteopenic, or osteoporotic subjects. We could not also find any definite differences among groups in other variables. Figure 3 shows the distribution of estimated population levels by T-score in Korean men and women aged 50 years. Lumbar bone density T-scores tended to be lower than those of the femoral neck or hip. We also determined the prevalence of osteoporosis according to the skeletal sites (lumbar spine, femoral neck, and total hip). The prevalence of osteoporosis at the femoral neck was 22.4% in women and 3.3% in men. The prevalence of osteoporosis was lowest at the total hip because

Statistical analysis All sample and weight variables were stratified, and the Predictive Analytics Software (PASW) complex-samples procedure was used for the statistical analysis. PASW complex-samples includes complex sample designs such as stratified, clustered, or multistage sampling. We used the stratification variables and sampling weights designated by the Korean Centers for Disease Control and Prevention for prevalence calculations, which were based on the sample design for each survey year. Sampling weights were adjusted for nonresponse according to demographic factors after the surveys were completed. The PASW complex-samples frequencies procedure was used as follows: (1) to evaluate the prevalence of osteoporosis and osteopenia, clustered on the sampling-district variable; and (2) to obtain the distribution of estimated population levels of T-score by age in Korean men and women aged 50 years. The PASW complexsample descriptive procedure was used to evaluate the distribution of sociodemographic and clinical variables and Journal of Bone and Mineral Research

PREVALENCE, DIAGNOSIS, AND TREATMENT OF OSTEOPOROSIS IN KOREANS

1881

Fig. 2. Prevalence of known and newly-diagnosed osteoporosis and osteopenia cases in Korean adults aged 50 years. (A) male and (B) female. The number of cases is the actual number of study subjects. yThe percentages were calculated from the PASW complex-samples procedure using the stratification variables and sampling weights.

only 4% of women and 0.5% of men had osteoporosis at that site. On the other hand, 27% of women and 6.0% of men had osteoporosis at the lumbar spine. Figure 4 shows physician diagnosis rate and treatment rate in women with osteoporosis according to age. It was estimated that osteoporosis was diagnosed in 29.9% of women aged 50 years in Korea. The treatment rate including known and newly diagnosed osteoporosis patients was estimated to be 14.4%. The treatment rate for the subjects who were already diagnosed with osteoporosis by a physician was much higher (48.3%). The physician diagnosis rate was highest for subjects in their 60s (ie, ages 60–69 years). The treatment rate showed a similar pattern to the diagnosis rate. However, the treatment rate for known osteoporosis patients increased with age. We compared physician diagnosis rate and treatment rate between females aged 66 to 68 years and the remaining females of other ages (ie, females aged 50 [except for 66–68] years). The physician diagnosis rate was significantly higher in the females aged 66 to 68 years (43.6% versus 28.1%, p < 0.05) (Fig. 5A). We also obtained the treatment rate between females aged 66 to 68 years and aged 50 (except for 66–68) years; however, we did not find significant differences (16.9% versus 14.1%, p > 0.05) (Fig. 5A).

Discussion There is a paucity of epidemiological studies investigating the epidemiology of osteoporosis in Korea(13,14); however, as far as we are aware, this is the first study to examine the prevalence and management status of osteoporosis at the national level. In our study, the prevalence of osteoporosis in adults aged 50 years was 35.5% in women and 7.5% in men. Although the prevalence of osteoporosis in Asian countries is not clear, because there are only a few studies in these populations, the osteoporosis prevalence in women aged from 50 to 79 years was reported as about 38% in China(19) and 31.0% in Japan.(20)

1882

CHOI ET AL.

The prevalence in East Asian countries was quite similar to our data. The prevalence of osteoporosis among these older than 50 years of age in the United States was reported as 10% in women and 2% in men from the National Health and Nutrition Examination Survey (NHANES) 2005–2006,(11) which was a lower prevalence compared to our study. Several factors might contribute to the differences in osteoporosis prevalence. First, the spine BMD was not measured in the NHANES. However, in the present study, the prevalence was 13.6% (female 22.4%, male 3.3%) at the femoral neck and still higher than the prevalence in the United States. Second, the NHANES, non-Hispanic white, non-Hispanic black, and Mexican Americans were included in the survey, but no Asians.(11) In a Canadian multicenter study, the prevalence of osteoporosis was reported as 15.8% for female and 6.6% for males, which was also a lower prevalence compared to our study. In this study, all non-Caucasian participants were also eliminated.(12) It has been reported that Asians have the lowest BMD compared to Blacks, Hispanics, and Caucasians.(21,22) Therefore, ethnic differences might contribute to this discrepancy between these North American studies and our study. In addition, it has been reported that Asian populations have a less dramatic increase in hip fracture rates associated with age than Caucasians, but the vertebral fracture rates were higher.(23,24) We found that lumbar bone density T-scores tended to be lower than those of the femoral neck or hip, and the prevalence of osteoporosis was higher at the lumbar spine than the femoral neck or total hip. This may explain the ethnic differences between Asians and Caucasians in vertebral and hip fracture incidence. Twenty-six percent of the Korean osteoporosis patients (female 29.9%, male 5.8%) had previously been diagnosed by a physician. Interestingly, in this study, the diagnosis rate was highest among women in their 60s. The highest rate of previous osteoporosis diagnosis in the 60s age group may be due to the ‘‘National Screening Program for the Transitional Ages’’ in Korea. Since 2007, BMD measurements have been performed for Journal of Bone and Mineral Research



1883

37.4 12.0 – 61.8 62.4

35.0 11.6 – 65.8 63.7 (62.1, 69.4) (59.8, 67.5)

(31.3, 38.8) (9.4, 14.2)

74.2 25.8 0.1 12.8

73.1 (66.2, 79.0) 26.9 (21.0, 33.8) 0 13.1 (10.5, 16.1)

29.3 24.9 22.7 23.1 39.1 20.3 24.9 15.6

(22.3, (18.9, (23.7, (20.8,

25.7 22.2 27.3 24.8

19.5) 29.8) 26.7) 37.5) 43.3) 23.6) 28.2) 18.8)

33.0) 28.4) 26.3) 27.0)

(58.0, 65.5) (58.5, 66.1)

(34.0, 41.0) (9.8, 14.7)

(68.3, 79.3) (20.7, 31.7) (0.0, 0.4) (10.3, 15.7)

(35.1, (17.4, (21.9, (12.9,

(25.9, (21.7, (19.5, (19.6,

62.3 (61.7, 63.0) 166.2 (165.8, 166.7) 64.0 (63.4, 64.7) 23.2 (22.9, 23.4) 0.87 (0.87, 0.88) 0.88 (0.87, 0.88) 0.69 (0.69, 0.70) 22.0 (21.3, 22.8)

Osteopenia (n ¼ 1014)

29.3) 26.0) 31.2) 29.2)

(13.9, (23.0, (21.0, (29.6,

16.5 26.3 23.8 33.5

59.2 (58.7, 59.7) 168.0 (167.6, 168.4) 70.4 (69.7, 71.1) 24.9 (24.7, 25.1) 1.05 (1.04, 1.06) 1.03 (1.02, 1.04) 0.85 (0.84, 0.85) 22.5 (21.8, 23.2)

Normal (n ¼ 900)

38.5 10.1 – 52.7 54.0

72.1 27.9 1.7 14.9

53.9 16.3 21.1 8.8

51.6 21.9 12.9 13.6

(43.8, 61.4) (45.3, 62.4)

(30.3, 47.5) (5.8, 17.1)

(62.7, 79.9) (20.1, 37.3) (0.4, 7.8) (9.0, 23.7)

(44.9, 62.6) (10.6, 24.1) (14.8, 19.2) (4.6, 16.0)

(42.7, 60.4) (15.8, 29.5) (8.2, 19.7) (8.2, 21.7)

68.0 (66.2, 69.8) 163.7 (162.5, 165.0) 56.6 (54.3, 58.8) 21.0 (20.3, 21.7) 0.70 (0.68, 0.71) 0.75 (0.73, 0.77) 0.58 (0.56, 0.60) 22.0 (20.2, 23.8)

Osteoporosis (n ¼ 181)

2.0 2.0 69.9 64.6 61.0

79.2 20.8 0.3 14.9

39.1 21.3 31.0 8.6

17.9 23.8 25.2 33.1

22.5) 29.1) 29.8) 39.3)

(1.0, 3.8) (1.0, 3.9) (64.5, 74.8) (59.3, 69.6) (55.3, 66.4)

(72.4, 84.7) (15.3, 27.6) (0.0, 2.3) (11.6, 18.9)

(33.4, 45.1) (17.3, 25.9) (26.1, 36.4) (5.7, 12.8)

(14.0, (19.2, (21.1, (27.5,

54.9 (54.4, 55.4) 156.7 (156.1, 157.3) 61.8 (60.9, 62.7) 25.2 (24.8, 25.5) 1.01 (1.00, 1.02) 0.95 (0.94, 0.96) 0.79 (0.78, 0.79) 18.9 (18.1, 19.8)

Normal (n ¼ 450)

4.9 1.3 92.9 61.4 57.2

74.4 25.6 0.9 18.0

58.1 17.5 19.2 5.2

28.9 26.7 22.3 22.1

31.9) 29.8) 25.8) 25.3)

(3.6, 6.6) (0.7, 2.1) (90.8, 94.6) (58.1, 64.7) (53.8, 60.6)

(68.9, 79.2) (20.8, 31.1) (0.5, 1.6) (15.8, 20.4)

(54.6, 61.4) (15.4, 19.9) (16.6, 22.1) (3.7, 7.2)

(26.1, (23.8, (19.2, (19.2,

60.9 (60.4, 61.4) 154.1 (153.8, 154.4) 58.1 (57.6, 58.6) 24.5 (24.3, 24.7) 0.84 (0.83, 0.84) 0.81 (0.80, 0.81) 0.65 (0.64, 0.65) 19.3 (18.7, 19.9)

Osteopenia (n ¼ 1319)

Women

5.9 0.5 99.6 50.9 47.9

69.2 30.8 4.3 16.4

81.3 8.0 8.1 2.6

47.4 23.8 16.8 12.0

(4.4, 8.0) (0.2, 1.2) (98.5, 99.9) (47.1, 54.8) (44.3, 51.6)

(63.4, 74.4) (25.6, 36.6) (3.1, 5.8) (13.7, 19.5)

(77.9, 84.3) (6.2, 10.4) (6.0, 10.7) (1.6, 4.2)

(43.4, 51.5) (20.9, 27.0) (13.9, 20.3) (9.2, 15.5)

69.7 (69.0, 70.5) 150.6 (150.2, 151.1) 52.8 (52.2, 53.3) 23.3 (23.0, 23.5) 0.68 (0.67, 0.69) 0.67 (0.66, 0.68) 0.52 (0.52, 0.53) 18.8 (18.1, 19.5)

Osteoporosis (n ¼ 1082)

The number of cases is the actual number of study subjects. The percentage (range) and mean (range) values in the table were calculated from the PASW complex-samples procedure using the stratification variables and sampling weights. L-spine ¼ lumbar spine; BMD ¼ bone mineral density; PASW ¼ Predictive Analytics Software. p < 0.05 comparing normal subjects with those with osteopenia or osteoporosis in both men and women. p < 0.05 comparing normal subjects with those with osteopenia or osteoporosis only in women.

Age (years) Height (cm) Weight (kg) Body mass index (kg/m2) L-spine BMD (g/cm2) Total femur BMD (g/cm2) Femur neck BMD (g/cm2) Serum 25(OH)D (ng/mL) Household income (%) Lowest Lower intermediate Upper intermediate Highest Education level (%) Primary Middle High College or more Residential area (%) City Rural area History of fragility fracture (%) Family history of osteoporotic fracture (%) Current smoking (%) Alcohol (6 units a day) (%) Menopause (%) Taking medical screening (%) Regular exercise (%)

Characteristics

Men

Table 1. Basal Characteristics of Normal, Osteopenic, and Osteoporotic Subjects in the Survey

Fig. 3. Distribution of estimated population levels of T-score in Korean adults aged 50 years. (A) male and (B) female.

females aged 66 years in a new national screening program called the Screening Program for Transitional Ages.(15) The physician diagnosis rate was significantly higher in women aged 66 to 68 years who were beneficiaries of the screening program than other-aged women (females aged 50 [except for 66– 68] years). Moreover, the medical screening rate of women aged 66 to 68 years was higher than the adjacent aged groups (females aged 63–65 and 69–71 years; 76.1% versus 60.5% and 58.0%, respectively) (Fig. 5B). Although we could not confirm whether females aged 66 to 68 years took part in general medical examinations in the national screening program, it appears that the new national screening program may have led to an increase in the diagnosis of osteoporosis in older Korean women. Few reliable published reports exist on the diagnosis rate for osteoporosis in Asia; therefore, there are few comparable data. In the United States, among Medicare beneficiaries 65 years of age in 1999–2005, the total proportion of women and men who received BMD measurement was 30.0% and 4.4%, respectively.(25) Although we could not confirm whether the known osteoporosis patients in this study were diagnosed by BMD measurement, BMD was measured in more than one-half of the patients who were diagnosed with osteoporosis by a physician according to the data from the Health Insurance Review and Assessment Service in Korea (47%–76% in patients 50 years).(26) We could assume that most diagnoses by physicians were made by BMD measurements in this study. Thus, the diagnosis rate in Korea could be similar to the previous study.(25) The treatment rate for osteoporosis patients in Korea was 12.8% (female 14.4%, male 4.0%). There were few reliable published reports on the treatment rate for osteoporosis in the general population. A systematic review of 37 studies of patients with fragility fracture completed between 1994 and 2002 identified a treatment rate of >25% in only 3 of 11 studies focusing on osteoporosis treatment with a combination of

Fig. 4. Physician diagnosis rate and treatment rate of osteoporosis according to the specified age groups in Korean women aged 50 years. (A) Physician diagnosis rate of total osteoporosis patients. (B) Treatment rate of total osteoporosis patients. (C) Treatment rate of known osteoporosis patients. The number of cases is the actual number of study subjects. yThe percentages were calculated from the PASW complex-samples procedure using the stratification variables and sampling weights.

1884

CHOI ET AL.


Fig. 5. Comparison between the females aged 66 to 68 years who were the beneficiaries of the screening program and the other aged females. (A) Physician diagnosis rate and treatment rate between females aged 66 to 68 years and 50 (except for ages 66–68) years. (B) Medical screening rate of known cases of osteoporosis between females aged 66 to 68 years and the adjacent age groups (females aged 63–65 and 69–71 years). The number of cases is the actual number of study subjects. yThe percentages were calculated from the PASW complex-samples procedure using the stratification variables and sampling weights.

vitamin D and calcium, and a treatment rate of >10% in only 6 of 20 reports that listed the use of bisphosphonates.(27) Recently, a Canadian study of patients with fragility fracture reported that 36.2% of patients had been previously diagnosed and treated for osteoporosis.(28) In this study, the treatment rate was 44.4% for known osteoporosis patients. Therefore, the treatment rate is not low compared to other countries. However, the treatment rate for hypertension(29) and diabetes mellitus(16) in Korea was reported as about 66% and 48.8%, respectively. Therefore, the treatment rate for osteoporosis in Korea was much lower (12.8%) than other chronic diseases. Moreover, the treatment rate for known female osteoporosis patients was not highest in the 60s age group in which the diagnosis rate was highest. The treatment rate for females aged 66 to 68 years was also not significantly higher than the females of other ages (ie, females 50 [except 66–68] years). That means that diagnosis for osteoporosis resulting from the screening program was not followed by treatment for osteoporosis in Korea. More efforts are required to improve the treatment rate for osteoporosis in Korea. There are some limitations to our study. First is the questionnaire’s reliance on patient self-reporting. KNHANES was a nationwide survey of Koreans’ general health. Therefore, we could not validate the accuracy from medical records of individual answers for the history of fracture, diagnosis by a physician, and treatment for osteoporosis. For example, we could not evaluate which drugs were prescribed for known osteoporosis patients, nor verify whether the diagnosis was actually made by BMD measurements using central DXA. Second, we could not assess institutionalized people, an important at-risk group for osteoporosis. That could underestimate the prevalence and affect the diagnosis rate and the treatment rate in this study. Third, there is no BMD T-score reference for Koreans with Hologic DXA. Thus, diagnosis of osteopenia or osteoporosis was made using T-score calculated from the Asian reference data. Fourth, selective nonresponse might have effects on prevalence Journal of Bone and Mineral Research

estimates. However, the response rate of BMD examinations in the KNHANES 2008–2009 (71.1% for age 50 years) was higher than those of the U.S. NHANES 2005–2006 (58% for age 50 years).(11) Moreover, the KNHANES sampling procedure was designed to produce a national representative sample, and the sampling weights were further adjusted for nonresponse according to demographic factors. However, these data were obtained from a nationwide population with a high response rate and therefore provided representative information on the Korean osteoporosis status. Furthermore, there were few studies on the management status of osteoporosis in Asia. In this regard, this study has several strengths. In conclusion, the prevalence of osteoporosis in Korean adults was quite similar to the prevalence in other East Asian countries and higher than in Caucasians. We also found that lumbar bone density T-scores tended to be lower than those of the femoral neck or hip, and the prevalence of osteoporosis was higher at the lumbar spine than the femoral neck or total hip. That might explain the ethnic difference between Asians and Caucasians in vertebral and hip fracture incidence. The physician diagnosis rate and treatment rate for osteoporosis was not low compared to other studies. However, the rate was lower than other chronic diseases in Korea. A national screening program for osteoporosis in Korea may have contributed to an increased diagnosis rate in the 60s age group. Therefore, a large-scale screening program for osteoporosis could help increase the diagnosis rate for osteoporosis. However, there appeared to be inadequate treatment following a diagnosis of osteoporosis. More efforts are needed to improve the diagnosis and treatment rate for osteoporosis.

Disclosures All authors state that they have no conflicts of interest.


1885

Acknowledgments The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Korean Centers for Disease Control and Prevention, Department of Health and Welfare of Korea. Authors’ roles: Study design: YJC and YSC. Data analysis: YJC, DJK, and YL. Data interpretation: YJC, HJO, YL, and YSC. Drafting manuscript: YJC. Revising manuscript content: YL and YSC. Approving final version of manuscript: YJC, HJO, DJK, YL, and YSC. YSC takes responsibility for the integrity of the data analysis.

References 1. Cooper C, Compion G, Melton LJ 3rd. Hip fractures in the elderly: a worldwide projection. Osteoporos Int. 1992;2:285–9. 2. Mithal A, Dhingra V, Lau E. The Asian audit: epidemiology, costs and burden of osteoporosis in Asia 2009 [Internet]. Nyon, Switzerland: International Osteoporosis Foundation; 2009 [cited 2012 April 15]. Available from http://www.iofbonehealth.org/sites/default/files/ PDFs/Audit%20Asia/Asian_regional_audit_2009.pdf. 3. Johnell O, Kanis JA. An estimate of the worldwide prevalence, mortality and disability associated with hip fracture. Osteoporos Int. 2004;15:897–02. 4. Kang HY, Yang KH, Kim YN, Moon SH, Choi WJ, Kang DR, Park SE. Incidence and mortality of hip fracture among the elderly population in South Korea: a population-based study using the National Health Insurance claims data. BMC Public Health. 2010;10:230. 5. U.S. Preventive Services Task Force. Screening for osteoporosis in postmenopausal women: recommendations and rationale. Ann Intern Med. 2002;137:526–528. 6. The National Osteoporosis Foundation (NOF). Clinician’s guide to prevention and treatment of osteoporosis. Washington, DC: National Osteoporosis Foundation; 2008. 7. Qaseem A, Snow V, Shekelle P, Hopkins R Jr, Forciea MA. Owens DK; Clinical Efficacy Assessment Subcommittee of the American College of Physicians. Screening for osteoporosis in men: a clinical practice guideline from the American College of Physicians. Ann Intern Med. 2008;148:680–4. 8. Kiebzak GM, Beinart GA, Perser K, Ambrose CG, Siff SJ, Heggeness MH. Undertreatment of osteoporosis in men with hip fracture. Arch Intern Med. 2002;162:2217–22. 9. Morris CA, Cabral D, Cheng H, Katz JN, Finkelstein JS, Avorn J, Solomon DH. Patterns of bone mineral density testing: current guidelines, testing rates, and interventions. J Gen Intern Med. 2004;19:783–90. 10. Gehlbach SH, Fournier M, Bigelow C. Recognition of osteoporosis by primary care physicians. Am J Public Health. 2002;92:271–3. 11. Looker AC, Melton LJ 3rd, Harris TB, Borrud LG, Shepherd JA. Prevalence and trends in low femur bone density among older US adults: NHANES 2005–2006 compared with NHANES III. J Bone Miner Res. 2010;25:64–71. 12. Tenenhouse A, Joseph L, Kreiger N, Poliquin S, Murray TM, Blondeau L, Berger C, Hanley DA, Prior JC. Estimation of the prevalence of low bone density in Canadian women and men using a populationspecific DXA reference standard: the Canadian Multicentre Osteoporosis Study (CaMos). Osteoporos Int. 2000;11:897–04. 13. Cui LH, Choi JS, Shin MH, Kweon SS, Park KS, Lee YH, Nam HS, Jeong SK, Im JS. Prevalence of osteoporosis and reference data for lumbar

1886

CHOI ET AL.

spine and hip bone mineral density in a Korean population. J Bone Miner Metab. 2008;26:609–17. 14. Shin CS, Choi HJ, Kim MJ, Kim JT, Yu SH, Koo BK, Cho HY, Cho SW, Kim SW, Park YJ, Jang HC, Kim SY, Cho NH. Prevalence and risk factors of osteoporosis in Korea: a community-based cohort study with lumbar spine and hip bone mineral density. Bone. 2010;47:378–87. 15. Kim YT, Lee WC, Cho B. National Screening Program for the Transitional Ages in Korea. J Korean Med Assoc. 2010;53:371–6. 16. Choi YJ, Kim HC, Kim HM, Park SW, Kim JO, Kim DJ. Prevalence and management of diabetes in Korean adults: Korea National Health and Nutritional Surveys 1998-2005. Diabetes Care. 2009;32:2016–20. 17. Kim SM, Lee JS, Lee J, Na JK, Han JH, Yoon DK, Baik SH, Choi DS, Choi KM. Prevalence of diabetes and impaired fasting glucose in Korea: Korean National Health and Nutrition Survey 2001. Diabetes Care. 2006;29:226–31. 18. Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, Kalkwarf HJ, Langman CB, Plotkin H, Rauch F, Zemel BS, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Silverman S. International Society for Clinical Densitometry 2007 Adult and Pediatric Official Positions. Bone. 2008;43:1115–21. 19. Wu XP, Liao EY, Zhang H, Dai RC, Shan PF, Cao XZ, Liu SP, Jiang Y. Determination of age-specific bone mineral density and comparison of diagnosis and prevalence of primary osteoporosis in Chinese women based on both Chinese and World Health Organization criteria. J Bone Miner Metab. 2004;22:382–91. 20. Iki M, Kagamimori S, Kagawa Y, Matsuzaki T, Yoneshima H, Marumo F. Bone mineral density of the spine, hip and distal forearm in representative samples of the Japanese female population: Japanese Population-Based Osteoporosis (JPOS) Study. Osteoporos Int. 2001; 12:529–37. 21. Handa R, Ali Kalla A, Maalouf G. Osteoporosis in developing countries. Best Pract Res Clin Rheumatol. 2008;22:693–708. 22. Barrett-Connor E, Siris ES, Wehren LE, Miller PD, Abbott TA, Berger ML, Santora AC, Sherwood LM. Osteoporosis and fracture risk in women of different ethnic groups. J Bone Miner Res. 2005;20:185–94. 23. Bow CH, Cheung E, Cheung CL, Xiao SM, Loong C, Soong C, Tan KC, Luckey MM, Cauley JA, Fujiwara S, Kung AW. Ethnic difference of clinical vertebral fracture risk. Osteoporos Int. 2012 Mar; 23(3):879–85. 24. Ross PD, Fujiwara S, Huang C, Davis JW, Epstein RS, Wasnich RD, Kodama K, Melton LJ 3rd. Vertebral fracture prevalence in women in Hiroshima compared to Caucasians or Japanese in the US. Int J Epidemiol. 1995;24:1171–7. 25. Curtis JR, Carbone L, Cheng H, Hayes B, Laster A, Matthews R, Saag KG, Sepanski R, Tanner SB, Delzell E. Longitudinal trends in use of bone mass measurement among older Americans, 1999-2005. J Bone Miner Res. 2008;23:1061–7. 26. Jang S, Park C, Jang S, Yoon H-K, Shin CS, Kim D-Y, Ha Y-C, Lee S-S, Choi HJ, Lee Y-K, Kim B-T, Choi J-Y. Medical service utilization with osteoporosis. Endocrinol Metab. 2010;25:326–39. 27. Elliot-Gibson V, Bogoch ER, Jamal SA, Beaton DE. Practice patterns in the diagnosis and treatment of osteoporosis after a fragility fracture: a systematic review. Osteoporos Int. 2004;15:767–78. 28. Bogoch ER, Elliot-Gibson V, Beaton DE, Jamal SA, Josse RG, Murray TM. Effective initiation of osteoporosis diagnosis and treatment for patients with a fragility fracture in an orthopaedic environment. J Bone Joint Surg Am. 2006;88:25–34. 29. Kim KI, Chang HJ, Cho YS, Youn TJ, Chung WY, Chae IH, Choi DJ, Kim CH. Current status and characteristics of hypertension control in community resident elderly Korean people: data from a Korean longitudinal study on health and aging (KLoSHa study). Hypertens Res. 2008;31:97–105.
