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Clinical Investigations: Miscellaneous |

Osteoporosis in Pulmonary Clinic Patients*: Does Point-of-Care Screening Predict Central Dual-Energy X-ray Absorptiometry? FREE TO VIEW

Robert A. Adler; Holly L. Funkhouser; Valentina I. Petkov; Belinda L. Elmore; Patricia S. Via; Cynthia T. McMurtry; Tilahun Adera
Author and Funding Information

*From the Sections of Endocrinology (Drs. Adler, Petkov, and Elmore, Ms. Funkhouser and Ms. Via) and Geriatrics (Dr. McMurtry), Medical Service, McGuire Veterans Affairs Medical Center, Richmond, VA; and the Departments of Internal Medicine (Drs. Adler and McMurtry) and Preventive and Community Medicine (Dr. Adera), Medical College of Virginia/Virginia Commonwealth University, Richmond, VA.

Correspondence to: Robert A. Adler, MD, McGuire VAMC, Endocrinology (111P), 1201 Broad Rock Blvd, Richmond, VA 23249; e-mail: robert.adler@med.va.gov



Chest. 2003;123(6):2012-2018. doi:10.1378/chest.123.6.2012
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Published online

Study objectives: Patients in a pulmonary clinic have disorders that predispose them to osteoporosis and may use glucocorticoid therapy, which has been associated with low bone mineral density (BMD) and increased fracture risk. Ideally, all patients at risk for osteoporosis would be screened using the best test available, which is central BMD by dual-energy x-ray absorptiometry (DXA). We proposed to stratify the risk for osteoporosis by the use of a simple questionnaire and point-of-care heel ultrasound BMD measurements.

Design: Cross-sectional screening study.

Setting: Pulmonary clinic in a single Veterans Affairs Medical Center.

Patients: Approximately 200 male and female patients who had not had previous BMD testing were eligible for the study, and 107 gave consent.

Interventions: One hundred seven men (white, 71 men; black, 35 men; and Asian, 1 man) underwent heel BMD testing and filled out a questionnaire. Ninety-eight men underwent a central DXA.

Results: Of 98 subjects, 24.5% had a spine, total hip, or femoral neck (FN) T-score of ≤ −2.5, which is the generally accepted definition of osteoporosis diagnosed using DXA, and 44.9% had a T-score of ≤ −2.0. The best-fit models for predicting FN or total hip BMD included body weight, heel BMD, corticosteroid use for ≥ 7 days, and race, which accounted for 52 to 57% of the variance. When a heel ultrasound T-score of −1.0 was tested to predict a central DXA T-score of −2.0, the sensitivity was 61% and the specificity 64%. Adding the questionnaire score and body mass index (BMI) to the heel T-score improved sensitivity but not specificity. Moreover, BMI and age predicted central BMD with similar sensitivity and specificity. Importantly, of 24 patients with a central DXA T-score of ≤ −2.5, only 14 were identified by a heel T-score of ≤ −1.0.

Conclusions: Although the findings from a heel ultrasound plus the answers to a questionnaire were reasonably good indicators for predicting the presence of low BMD, little predictability was gained over the use of BMI and age. In a group of pulmonary clinic patients, the prevalence of osteoporosis was clinically significant, and central DXA testing was the preferable technique for identifying patients who were at risk for fracture.

Figures in this Article

Patients with pulmonary diseases are commonly treated with oral or inhaled glucocorticoids. Such therapy clearly increases the risk for the development of osteoporosis.14 Moreover, patients with various pulmonary diseases may have bone loss due to decreased physical activity,5 smoking,6 chronic disease,7 and perhaps the muscle wasting of emphysema. In an ideal world, all patients with lung diseases would be screened for osteoporosis8 using central bone mineral density (BMD) measurements made by dual-energy x-ray absorptiometry (DXA). However, because of the expense and unavailability of DXA testing, many patients with osteoporosis are not identified and treated. Various peripheral bone density measurements have been used in several populations912 to try to identify patients who may be at risk for osteoporosis. In addition, risk assessment questionnaires have been used in women13 and men14 to help stratify risk. We devised a questionnaire based on published instruments but that were adapted to the special characteristics of patients with pulmonary diseases. We hypothesized that a peripheral bone density measurement (ie, heel ultrasound bone density) plus a questionnaire could determine which patients in a pulmonary clinic had osteoporosis, as measured by central DXA.

Subjects

Over a 4-month period, we visited a weekly general pulmonary clinic in a single Veterans Affairs medical center. Only patients who had not had a previous measurement of BMD (by any technique) were eligible for the study. Patients were asked whether they would participate, and all signed a consent form approved by the Veterans Affairs medical center institutional review board. After signing the consent form, each patient filled out the questionnaire and underwent heel ultrasound BMD testing (Sahara densitometer; Hologic, Inc; Bedford, MA). Standard heel measurements include broadband ultrasound attenuation (BUA) and speed of sound (SOS) through the calcaneus. From BUA and SOS, a quantitative ultrasound index (QUI), sometimes called the stiffness QUI, is calculated, as is an apparent BMD and a T-score (ie, the number of SDs from the mean of healthy, white, young women), as provided by the manufacturer. The QUI, BMD, and T-score are calculated automatically by the instrument. We also calculated a heel T-score based on data from healthy young men obtained by Nattrass et al.15 Within 1 month, 98 patients underwent testing of central bone density (QDR 4500 densitometer; Hologic, Inc). We measured the BMD and T-score of the spine (L1 to L4), the total hip, and the femoral neck (FN). The DXA T-scores were also calculated by the instrument using the manufacturer’s normal data for spine BMD, which were obtained from young subjects who had been matched for gender and ethnic group, and using National Health, Education, and Nutrition Survey data for hip measurements.

Derivation and Calculation of Questionnaire Score

We modified questionnaires that had been devised for other populations1314 to derive a questionnaire that would be particularly applicable to a predominantly male population of patients who had pulmonary diseases. Twenty-four questions could each be answered “yes” or “no.” The questionnaire (Table 1 ) was scored by the individual question, and a total score was devised by giving 1 point for each answer that reflected a potential risk factor. We determined which questions represented independent variables (identified in Table 1 ), so that the final number of independent questions used to calculate the score was 14.

Data Management and Analysis

All the data were entered into a database for later analysis (SPSS, version 10.0 for Windows; SPSS Inc; Chicago, IL). Analyses included multiple regression and calculation of relative risk (RR). Characteristics of the screening tests were determined, and receiver operating characteristic (ROC) curves were constructed for individual tests as well as for combinations of tests. The BMD in the spine, total hip, and FN were used as dependent variables in the multiple regression models. Osteoporosis and severe osteopenia were defined as a T-score obtained by central DXA of ≤ −2.5 and ≤ −2.0, respectively. Significance was determined using a two-sided α level of 0.05.

Over a 4-month period, 107 subjects from the pulmonary clinic agreed to participate, of approximately 200 patients who attended the clinic and were eligible for the study. About 100 additional clinic patients had already undergone BMD testing for osteoporosis. It was not possible to determine whether there were any differences between those who participated and those who did not. Demographic data are shown in Table 2 . No female pulmonary clinic patients met the inclusion criteria and were willing to participate. Most of the subjects were white men > 60 years of age. The averages of the heel ultrasound bone density measurements and the central DXA measurements are listed in Table 2 . Of 98 subjects, 24.5% had a T-score of the spine, total hip, or FN of ≤ −2.5, which is generally accepted as a diagnostic criterion for osteoporosis in postmenopausal white women.16 Using a central BMD T-score cutoff of ≤ −2.0, 44.9% of subjects had low bone mass that may require intervention. Osteopenia has been defined as low bone mass as measured by a central DXA T-score between −1 and −2.5. Using this criterion, 76.5% of the subjects had osteopenia. In contrast, fewer subjects had osteoporosis or osteopenia, as defined by heel ultrasound T-score using either a white female database or a white male database (Table 3 ).

The maximum possible questionnaire score was 14, with most subjects having a score that was less than half of that. Individual responses are shown in Table 1 . Significant correlations were found among hip BMDs (ie, FN and total hip) and heel ultrasound measurements (ie, T-score, BMD, BUA, and QUI), age, body weight, body mass index (BMI) [r = 0.38 to 0.66; all p < 0.0001], and total questionnaire score (r= −0.30 to −0.32; p < 0.012). Subjects who reported prednisone use for > 7 days (p < 0.006) or a decrease in height (p < 0.021) had lower hip BMD measurements. Lower BMD in the hip was observed in whites (p < 0.011). Then, we used these factors to build prediction models of hip BMD. The best-fit model of total hip BMD included body weight, heel BMD, prednisone use for > 7 days, and race (Table 4 ). The model accounted for 57% of the variance (p < 0.0001). Using the total questionnaire score instead of individual risk factors yielded a model of total hip BMD (ie, 0.508 + 0.004 × body weight + 0.284 × BMD in the heel − 0.02 × questionnaire score), as is listed in Table 4 . Separately, body weight, heel BMD, and questionnaire score explained 44%, 20%, and 10% of the variability of total hip BMD, respectively. A model including body weight and heel BMD accounted for 50% of the variance. Adding the total questionnaire score increased the adjusted R2 to only 54%.

The FN BMD showed significant relationships with the same factors as for the total hip. Multiple regression models for predicting FN BMD were very similar to those for the total hip (data not shown). Replacing the heel BMD with other heel ultrasound measurements (ie, heel T-score, BUA, and QUI, but not SOS) gave similar results. Using BMI instead of body weight decreased the adjusted R2 slightly.

In bivariate analysis, body weight, BMI (p < 0.0001), BUA (p = 0.041), and prednisone use (p = 0.037) were significant predictors for spine BMD. We used factors identified as significant predictors of hip BMD to build a model of spine BMD. Although stepwise multiple regression analysis identified body weight (p < 0.0001), height loss of > 1 inch (p = 0.001), prednisone use for > 7 days (p = 0.017), and race (p = 0.043) as significant predictors, the model accounted for only 27% of the variance.

In another analysis, we categorized study subjects according to their T-scores in the heel (≤ −1.5), BMI (≤ 25), corticosteroid use, and age (≥ 65 years). Using severe osteopenia (T-score, ≤ −2.0, as examined by central DXA at any of the following sites: spine, total hip, or FN) as an outcome variable, we calculated absolute risk and RR associated with a single factor as well as combinations of risk factors. Statistically significant associations are reported in Table 5 . BMI < 25, age > 65 years, current use of steroids, prednisone use for > 7 days, and heel T-score < −1.5 were associated with significantly increased RR for having severe osteopenia. Adding a second or third risk factor increased the absolute risk and, in most of the cases, the RR. We performed the same analysis using a cutoff point of T-score, obtained by central DXA, of −2.5 (data not shown). Although similar, the results were less robust.

We chose the following two cutoffs of heel T-score: ≤ −1.0 and ≤ −1.5 to determine the sensitivity and specificity of heel ultrasound to predict a T-score by central DXA of ≤ −2.0 (sensitivity, 61% and 41%, respectively; specificity, 64% and 77%, respectively). The lack of heel ultrasound sensitivity and specificity is reflected by the ROC curve area of 0.688 (95% confidence interval [CI], 0.583 to 0.794). We used an additive scoring system based on BMI, heel T-score, and questionnaire score to determine whether the tests together had a higher predictive value for osteopenia (T-score, ≤ −2.0). ROC analysis (Table 6 and Fig 1 ) indicated that combining the heel T-score with BMI, age, or questionnaire score produced larger areas under the curve than individual tests, reflecting improved sensitivity. The same analyses were performed using T-score obtained by central DXA of ≤ −2.5. The results (data not shown) were similar.

The very large National Osteoporosis Risk Assessment study in women has established that heel ultrasound BMD is a good predictor of future fracture.17 No similar studies exist for men. In addition, we have reported9 that the concordance in men between heel ultrasound BMD and central DXA is inadequate. Others14 have suggested that a simple questionnaire can predict central BMD in men. Thus, we chose to use both heel ultrasound and a questionnaire to find patients who were at risk for osteoporosis in a population with many risk factors for low bone mass. Indeed, we found that, using the best available test (ie, central DXA), 24.5% of the subjects had a T-score that would be defined as osteoporosis (ie, ≤ −2.5). Using a BMD cutoff of −2.0, 44.9% of the subjects would be considered for osteoporosis treatment, although it is not known whether this cutoff should be applied to men as well as to postmenopausal women. It should be noted here that we studied only those patients who had not had a previous measurement of bone density. Therefore, many patients who are at clear risk for osteoporosis, such as lung transplant candidates (who receive BMD testing as part of their routine evaluation) were excluded from the study. Nonetheless, low bone mass was common among the patients studied. Of the 24 subjects with a spine, total hip, or FN T-score of ≤ −2.5, only 14 were identified by a heel ultrasound T-score of ≤ −1.0. Using the central DXA to diagnose severe osteopenia (T-score, ≤ −2.0) in this population, the positive predictive value of the heel ultrasound (T-score, ≤ −1.0) was only 59%, and the negative predictive value was 67%. Thus, if only the heel ultrasound were used, many pulmonary patients who are at risk for osteoporosis would not be identified and treated appropriately.

We attempted to improve the predictive ability of heel ultrasound by adding information obtained from a simple questionnaire. The models that we constructed were robust, but in practice the lack of adequate positive and negative predictive values using various heel ultrasound value cutoffs decreases their usefulness. The BMI appears to be a good predictor of central BMD, as others18 have reported. The addition of heel ultrasound and the questionnaire (either specific questions or a total score) did not augment the predictive value of BMI plus age, nor did it provide enough information to avoid needing a central DXA measurement. In practice, where DXA is available the predictive value of the heel measurements would not be adequate to prevent unnecessary DXA testing or to ensure that those patients who are at risk for osteoporosis would be identified. Thus, we conclude that heel ultrasound BMD, even augmented with a questionnaire, did not adequately predict central DXA for the diagnosis of osteoporosis. Our study population included only patients who had not had previous BMD testing. In this group, the prevalence of low bone mass was clinically significant, and central DXA was the method preferred for identifying patients who were at risk for fracture.

Abbreviations: BMD = bone mineral density; BMI = body mass index; BUA = broadband ultrasound attenuation; CI = confidence interval; DXA = dual-energy x-ray absorptiometry; FN = femoral neck; QUI = quantitative ultrasound index; ROC = receiver operating characteristics; RR = relative risk; SOS = speed of sound

Dr. Adler receives research support from Merck, Eli Lilly, and Novartis. He has been a speaker at sessions sponsored by Merck, Lilly, Novartis, and Procter & Gamble. Dr. McMurtry receives research support from Novartis. The current research was supported in part by a grant from Merck & Co, Inc.

Table Graphic Jump Location
Table 1. Proportional Distribution of Risk Factors Answered in the Affirmative
* 

Variables considered to be independent and thus used for determining the questionnaire score. Race was the 14th variable used in calculating the final questionnaire score (1 point if white; 0 points if black or other).

Table Graphic Jump Location
Table 2. Characteristics of the Study Subjects
* 

The T-scores were calculated automatically by Sahara densitometer, using a white female normative database.

 

T-scores were calculated using a white male normative database provided by Nattrass et al.15

Table Graphic Jump Location
Table 3. T-scores by Central DXA and Heel QUS*
* 

QUS = quantitative ultrasound.

 

Central DXA uses a male database adjusted for ethnic background.

 

The female heel QUS database is derived from studies of white women.

§ 

The male heel QUS database is based on 250 white men studied by Nattrass et al.15

Table Graphic Jump Location
Table 4. Parameter Estimates from Multiple Regression Models of BMD in the Total Hip
Table Graphic Jump Location
Table 5. Risk Factors for Severe Osteopenia*
* 

CS = corticosteroid; severe osteopenia = T-score of ≤ − 2.0 in the spine, total hip, or femoral neck.

Table Graphic Jump Location
Table 6. ROC Curves of Heel T-score, BMI, Age, Questionnaire Score, and Combinations Using Cutoff of T-score by Central DXA of −2.0
Figure Jump LinkFigure 1. ROC curves for heel T-score plus questionnaire score, heel T-score plus BMI, and BMI plus age, using a T-score of −2.0 obtained by central DXA.Grahic Jump Location
Adler, RA, Rosen, CJ (1994) Glucocorticoids and osteoporosis.Endocrinol Metab Clin North Am23,641-654. [PubMed]
 
McEvoy, CE, Ensrud, KE, Bender, E, et al Association between corticosteroid use and vertebral fractures in older men with chronic obstructive pulmonary disease.Am J Respir Crit Care Med1998;157,704-709. [PubMed]
 
Iqbal, F, Michaelson, J, Thaler, L, et al Declining bone mass in men with chronic pulmonary disease.Chest1999;116,1616-1624. [PubMed] [CrossRef]
 
Israel, E, Banerjee, TR, Fitzmaurice, GM, et al Effects of inhaled glucocorticoids on bone density in premenopausal women.N Engl J Med2001;345,941-947. [PubMed]
 
Teegarden, D, Proulx, WR, Kern, W, et al Previous physical activity relates to bone mineral measures in young women.Med Sci Sports Exerc1996;28,105-113. [PubMed]
 
Daniell, HW Osteoporosis and the slender smoker: marked vertebral compression fractures and loss of metacarpal cortex in relation to postmenopausal smoking and lack of obesity.Arch Intern Med1976;136,298-304. [PubMed]
 
Seeman, E, Melton, LJ, III, O’Fallon, WM, et al Risk factors for spinal osteoporosis in men.Am J Med1983;75,977-983. [PubMed]
 
Cummings, SR, Black, DM, Nevitt, MC, et al Bone density at various sites for prediction of hip fractures.Lancet1993;341,72-75. [PubMed]
 
Adler, RA, Funkhouser, HL, Holt, CM Utility of heel ultrasound bone density in men.J Clin Densitom2001;3,225-230
 
Frost, ML, Blake, GM, Fogelman, I Contact quantitative ultrasound: an evaluation of precision, fracture discrimination, age-related bone loss and applicability of the WHO criteria.Osteoporos Int1999;10,441-449. [PubMed]
 
Miller, PD, Bonnick, SL, Johnston, CC, et al The challenges of peripheral bone density testing: which patients need additional central density skeletal measurements?J Clin Densitom1998;1,211-217. [PubMed]
 
Ayers, M, Prince, M, Ahmadi, S, et al Reconciling quantitative ultrasound of the calcaneus with x-ray-based measurements of the central skeleton.J Bone Miner Res2000;15,1850-1855. [PubMed]
 
Cadarette, SM, Jaglal, SB, Murray, TM Validation of the simple calculated osteoporosis risk estimation (SCORE) for patient selection for bone densitometry.Osteoporos Int1999;10,85-90. [PubMed]
 
Zimering, MB, Krishnamesetty, N, Shah, J, et al Development of a simple self-administered questionnaire useful for predicting low bone mass in men [abstract]. J Bone Miner Res. 2000;;15(suppl) ,.:S416
 
Nattrass, S, Orwoll, E, Tylaksky, F, et al Male and ethnic reference ranges for the Sahara clinic bone sonometer [abstract]. J Bone Miner Res. 1999;;14(suppl) ,.:S501
 
Kanis, JA, Johnell, O, Oden, A, et al Risk of hip fracture according to the World Health Organization criteria for osteopenia and osteoporosis.Bone2000;27,585-590. [PubMed]
 
Siris, ES, Miller, PD, Barrett-Connor, E, et al Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women.JAMA2001;286,2815-2822. [PubMed]
 
Edelstein, SL, Barrett-Connor, E Relation between body size and bone mineral density in elderly men and women.Am J Epidemiol1993;138,160-169. [PubMed]
 

Figures

Figure Jump LinkFigure 1. ROC curves for heel T-score plus questionnaire score, heel T-score plus BMI, and BMI plus age, using a T-score of −2.0 obtained by central DXA.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Proportional Distribution of Risk Factors Answered in the Affirmative
* 

Variables considered to be independent and thus used for determining the questionnaire score. Race was the 14th variable used in calculating the final questionnaire score (1 point if white; 0 points if black or other).

Table Graphic Jump Location
Table 2. Characteristics of the Study Subjects
* 

The T-scores were calculated automatically by Sahara densitometer, using a white female normative database.

 

T-scores were calculated using a white male normative database provided by Nattrass et al.15

Table Graphic Jump Location
Table 3. T-scores by Central DXA and Heel QUS*
* 

QUS = quantitative ultrasound.

 

Central DXA uses a male database adjusted for ethnic background.

 

The female heel QUS database is derived from studies of white women.

§ 

The male heel QUS database is based on 250 white men studied by Nattrass et al.15

Table Graphic Jump Location
Table 4. Parameter Estimates from Multiple Regression Models of BMD in the Total Hip
Table Graphic Jump Location
Table 5. Risk Factors for Severe Osteopenia*
* 

CS = corticosteroid; severe osteopenia = T-score of ≤ − 2.0 in the spine, total hip, or femoral neck.

Table Graphic Jump Location
Table 6. ROC Curves of Heel T-score, BMI, Age, Questionnaire Score, and Combinations Using Cutoff of T-score by Central DXA of −2.0

References

Adler, RA, Rosen, CJ (1994) Glucocorticoids and osteoporosis.Endocrinol Metab Clin North Am23,641-654. [PubMed]
 
McEvoy, CE, Ensrud, KE, Bender, E, et al Association between corticosteroid use and vertebral fractures in older men with chronic obstructive pulmonary disease.Am J Respir Crit Care Med1998;157,704-709. [PubMed]
 
Iqbal, F, Michaelson, J, Thaler, L, et al Declining bone mass in men with chronic pulmonary disease.Chest1999;116,1616-1624. [PubMed] [CrossRef]
 
Israel, E, Banerjee, TR, Fitzmaurice, GM, et al Effects of inhaled glucocorticoids on bone density in premenopausal women.N Engl J Med2001;345,941-947. [PubMed]
 
Teegarden, D, Proulx, WR, Kern, W, et al Previous physical activity relates to bone mineral measures in young women.Med Sci Sports Exerc1996;28,105-113. [PubMed]
 
Daniell, HW Osteoporosis and the slender smoker: marked vertebral compression fractures and loss of metacarpal cortex in relation to postmenopausal smoking and lack of obesity.Arch Intern Med1976;136,298-304. [PubMed]
 
Seeman, E, Melton, LJ, III, O’Fallon, WM, et al Risk factors for spinal osteoporosis in men.Am J Med1983;75,977-983. [PubMed]
 
Cummings, SR, Black, DM, Nevitt, MC, et al Bone density at various sites for prediction of hip fractures.Lancet1993;341,72-75. [PubMed]
 
Adler, RA, Funkhouser, HL, Holt, CM Utility of heel ultrasound bone density in men.J Clin Densitom2001;3,225-230
 
Frost, ML, Blake, GM, Fogelman, I Contact quantitative ultrasound: an evaluation of precision, fracture discrimination, age-related bone loss and applicability of the WHO criteria.Osteoporos Int1999;10,441-449. [PubMed]
 
Miller, PD, Bonnick, SL, Johnston, CC, et al The challenges of peripheral bone density testing: which patients need additional central density skeletal measurements?J Clin Densitom1998;1,211-217. [PubMed]
 
Ayers, M, Prince, M, Ahmadi, S, et al Reconciling quantitative ultrasound of the calcaneus with x-ray-based measurements of the central skeleton.J Bone Miner Res2000;15,1850-1855. [PubMed]
 
Cadarette, SM, Jaglal, SB, Murray, TM Validation of the simple calculated osteoporosis risk estimation (SCORE) for patient selection for bone densitometry.Osteoporos Int1999;10,85-90. [PubMed]
 
Zimering, MB, Krishnamesetty, N, Shah, J, et al Development of a simple self-administered questionnaire useful for predicting low bone mass in men [abstract]. J Bone Miner Res. 2000;;15(suppl) ,.:S416
 
Nattrass, S, Orwoll, E, Tylaksky, F, et al Male and ethnic reference ranges for the Sahara clinic bone sonometer [abstract]. J Bone Miner Res. 1999;;14(suppl) ,.:S501
 
Kanis, JA, Johnell, O, Oden, A, et al Risk of hip fracture according to the World Health Organization criteria for osteopenia and osteoporosis.Bone2000;27,585-590. [PubMed]
 
Siris, ES, Miller, PD, Barrett-Connor, E, et al Identification and fracture outcomes of undiagnosed low bone mineral density in postmenopausal women.JAMA2001;286,2815-2822. [PubMed]
 
Edelstein, SL, Barrett-Connor, E Relation between body size and bone mineral density in elderly men and women.Am J Epidemiol1993;138,160-169. [PubMed]
 
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