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Trabecular bone scores in young HIV-infected men: a matched case-control study

BMC Musculoskeletal Disorders volume 21, Article number: 94 (2020) Cite this article

Abstract

Background

Screening for osteoporosis with dual-energy X-ray absorptiometry (DXA) is recommended for male HIV-infected patients only above the age of 50. Recently, trabecular bone score (TBS) has been introduced as a novel tool to assess bone microarchitecture using DXA of the lumbar spine. Few studies have reported TBS values in HIV-infected individuals younger than 50 years of age. This study compared TBS values in young males infected with HIV and matched controls, and investigated the associations between TBS and demographic parameters, clinical parameters, and bone mineral density (BMD) scores.

Methods

A cross-sectional study of BMD and TBS in HIV-infected men (n = 80) aged between 18 and 50 years and age- and sex-matched controls (n = 80) was conducted.

Results

The proportion of patients with low BMD (Z-score ≤ − 2) was significantly greater among HIV-infected patients than among matched controls (21.3% [17/80] vs. 8.8% [7/80], p = 0.027). Mean TBS values were significantly lower in HIV-infected patients than in controls (1.41 ± 0.07 vs. 1.45 ± 0.07, p = 0.008). In both groups, TBS values were positively correlated with BMD at the lumbar spine, femoral neck, and total hip (p < 0.001); however, TBS was not correlated with body mass index. In the HIV group, TBS was negatively correlated with the duration of tenofovir disoproxil fumarate(TDF) exposure (p = 0.04).

Conclusion

Young men infected with HIV had abnormal bone trabecular microarchitecture, as assessed by both TBS and BMD. TBS values were correlated with both BMD and the duration of TDF exposure.

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Background

Advances in antiretroviral therapy (ART) have improved life expectancy dramatically among people living with HIV. However, this improvement gives to rise to concerns about non-AIDS-related comorbidities that may be related to ART and age, such as cardiovascular, renal, metabolic, and bone disease. A meta-analysis showed that the prevalence of osteopenia or osteoporosis is higher in HIV-infected patients than in controls [1]. The pathogenesis of bone loss in HIV-infected individuals is a complex and multifactorial process, with HIV itself, the use of antiretroviral agents, hypogonadism in men, menopause in women, low body mass index (BMI), aging, malnutrition, steroid use, and smoking all associated with bone disease [2]. Hormonal changes in postmenopausal women or in elderly people are associated changes in the bone remodeling cycle, which leads to bone fragility and an increased risk of bone fracture [3, 4].

Bone mineral density (BMD) is determined by the peak bone mass and amount of bone loss and is the standard measure used for the diagnosis of osteoporosis. BMD evaluates bone quantity, rather than bone microarchitecture or composition [5]. Recently, the trabecular bone score (TBS) has been introduced as a novel tool for assessing bone microarchitecture. TBS values are obtained from dual-energy X-ray absorptiometry (DXA) scans of the lumbar spine using a proprietary software program; TBS is a noninvasive, indirect measurement calculated from the projection of the three-dimensional bone structure onto a two-dimensional plane [6]. TBS has been validated as a good prognostic tool for assessing trabecular microstructure independent of BMD and has been reported to increase the accuracy of fracture prediction in patients with BMD above the osteoporotic threshold [7, 8]. However, few studies have evaluated TBS in HIV-infected individuals, especially young male patients. We calculated TBS values from DXA images of the lumbar spine taken from HIV-infected male patients under 50 years of age. The etiology of osteoporosis in HIV-infected patients is multifactorial; therefore this descriptive study included only male HIV infected patients aged less than 50 years to minimize the influence of traditional risk factors associated with low BMD, such as age and postmenopausal status in women. We compared TBS values obtained from HIV-infected young male patients with those from matched healthy controls and investigated the associations between TBS and demographic parameters, clinical parameters, and BMD scores for the lumbar spine and femoral neck.

Methods

Study population

Male HIV-infected patients aged between 18 and 50 years were recruited from tertiary university hospitals in Korea from March 2015 to December 2018 for inclusion in this cross-sectional study. Only men were included to avoid potential confounds related to menopause-induced osteoporosis in women. Eighty HIV-infected patients were enrolled. Among subjects who attended routine health check-up examinations in tertiary university hospitals during the same period, controls matched for age and sex were included after BMD data was blinded. HIV-infected patients and control subjects with thyroid disorders, parathyroid malignancies, chronic liver disease, or rheumatoid arthritis were excluded. None of the HIV patients or control subjects took corticosteroids, calcium, or bisphosphonate agents. BMI was calculated as weight divided by height squared (kg/m2).

Clinical and laboratory evaluation

Baseline study visits involved collection of demographic, socioeconomic, and clinical information, and renal profile, liver function tests, and bone profiles, assessment of parathyroid hormone (PTH) and serum 25-hydroxy vitamin D (25[OH]D) levels, and measurement of the bone turnover markers serum C-terminal cross-linking telopeptide of type I collagen(CTX) and osteocalcin. CD4+ T-cell counts and HIV-1 RNA were obtained for subjects with HIV.

Measurement of BMD and TBS

TBS and BMD were evaluated in all HIV-infected patients and matched control subjects at the time of enrollment. BMD of the lumbar spine (L1–L4) and left hip was measured with the use of DXA scan (Lumbar Prodigy densitometer, Madison, WI, USA). Grams per square centimeter (g/cm2), as well as T score (compared with values of young adults of the same sex) and Z score (compared with values of adults of the same age and same sex) is reported for the AP lumbar spine and left hip. Low BMD for individuals under 50 years of age was defined as a Z-score ≤ − 2.0 according to the guideline [9]. We evaluated TBS at L1-L4, derived from DXA files from the database using TBS iNsight version 2.1 (Med-Imaps, Pessac, France) as our previous published data [10, 11]. TBS was Control subjects and HIV patients were divided into three TBS groups according to risk of fracture, as described in a recently published study [12]. A TBS score above 1.31 is considered normal (low risk fracture); a value between 1.23 and 1.31 denotes partially degraded bone microarchitecture (interemediate risk frcature); and a value below 1.23 denotes strongly degraded bone microarchitecture(high risk fracutre) [13].

Ethics

The study was approved by the ethics committee of Seoul St. Mary’s Hospital (study number: KC14OISI0768). Written informed consent according to the Declaration of Helsinki was obtained from all study subjects.

Statistical analysis

Statistical analyses were performed in SPSS (version 14.0; SPSS Inc., Chicago, IL, USA). Continuous data are expressed as the mean ± SD, and categorical data are expressed as percentages. Clinical variables were compared using an independent t-test, and categorical variables were compared using a Chi-squared test. Spearman’s correlation coefficient was used to analyze the correlations between variables. All tests were two-tailed, and p-values < 0.05 were considered statistically significant.

Results

Demographic characteristics

The demographic and laboratory characteristics of 80 HIV-infected patients and 80 age- and sex-matched controls are shown in Table 1. In both groups, the mean age of the patients was 39 ± 8 years, and all were male. The two groups did not differ in terms of smoking (p = 0.08), alcohol consumption (p = 1.0), or presence of diabetes mellitus (p = 0.24) or hypertension (p = 0.12). BMI was significantly lower in HIV-infected patients than in the control group (22.9 ± 3.0 vs. 24.9 ± 3.3, p < 0.001). HIV-infected patients had a greater history of previous fractures (12.5% [n = 10] vs. 1% [n = 1], p = 0.009) and presence of dyslipidemia (10.0% [n = 10] vs. 0%, p = 0.028).

Table 1 The comparison of control subjects and patients with HIV
Full size table

Among HIV-infected patients, the current mean CD4 T-cell count was 669 ± 271 cells/μl and the nadir CD4 T-cell count was 349 ± 183 cells/μl. Seventy-eight patients (97.5%) were receiving ART, and 93.7% had plasma HIV-1 RNA < 40 copies/ml. The mean duration of ART was 677.9 ± 411.2 days. The ART regimens used were non-nucleoside reverse transcriptase inhibitor (NNRTI)-based (n = 28, 35.8%), protease inhibitor (PI)-based (n = 29, 37.1%), or integrase inhibitor-based (n = 21, 26.9%). Forty-one (51.3%) patients had had exposure to tenofovir disoproxil fumarate (TDF).

TBS and BMD results

In the HIV group, four (5.0%) patients had an intermediate TBS fracture risk and two (2.5%) patients had a high TBS fracture risk; in the matched control group, seven (8.8%) subjects had an intermediate TBS fracture risk. The fracture risk assessed via TBS was not different between the HIV and control groups (p = 0.244). However, the mean TBS value in HIV-infected patients was 1.41 ± 0.07, which was significantly lower than the mean value for the matched control group (1.45 ± 0.07, p = 0.008) (Fig. 1a).

Fig. 1
figure 1

Trabecular bone score (TBS) and bone mineral density (BMD) in HIV-infected male patients and matched controls. a Comparison of TBS between male HIV patients and controls. b Comparison of BMD at the lumbar spine, femoral neck, and total hip between male HIV patients and controls

Full size image

The proportion of subjects with low BMD was significantly higher in the HIV group than in the control group (21.3% [17/80] vs. 8.8% [7/80], p = 0.027). The proportion of subjects with low BMD at the lumbar spine was significantly different between the two groups (21.3% [17/80] vs. 6.3% [5/80], p = 0.006), but the proportion with low BMD at either the femoral neck or total hip did not differ between the groups (0% [0/80] vs. 2.5% [2/80], p = 0.155). Figure 1b shows the BMD values for the lumbar spine, femoral neck, and total hip for the HIV group and the matched control group. The mean femoral neck BMD values (0.95 ± 0.14 vs. 1.02 ± 0.14, p = 0.009) and total hip BMD values (0.98 ± 0.13 vs. 1.06 ± 0.14, p < 0.001) were significantly lower in the HIV group than in the matched control group; however, BMD values for the lumbar spine did not differ between the two groups (1.16 ± 0.16 vs. 1.19 ± 0.18, p = 0.214).

There was discordance between the BMD and TBS results in 11 patients in the HIV group and 13 subjects in the control group; these proportions were not significantly different (p = 0.66).

In both groups, TBS values were positively correlated with BMD at the lumbar spine, femoral neck, and total hip. However, TBS values were not correlated with BMI in either group (Table 2). In the HIV group, TBS values were negatively correlated with the duration of tenofovir exposure (p = 0.04) and trended toward a negative correlation with the duration of HIV diagnosis (p = 0.07) (Table 2, Additional file 1: Figure S1).

Table 2 Correlations between clinical data, BMD and TBS in patients with HIV and matched controls
Full size table

Laboratory tests of bone metabolism in HIV-infected patients

In the group of 80 HIV-infected male patients, the mean 25[OH]D level was 21.2 ± 8.08 ng/ml, with 45% of patients (n = 36) measuring below 20 ng/ml. The quartile distribution of 25[OH]D values in patients was as follows: < 10 ng/ml (2.6%), 10–19.99 (43.6%), 20–29.99 (44.8%), 30–39.99 (3.8%), ≥40 (5.1%). Mean calcium, phosphorus, and alkaline phosphatase levels were 9.14 ± 0.32 mg/dl, 3.33 ± 0.51 mg/dl, and 64.7 ± 17.95 U/l, respectively. Mean osteocalcin and CTX levels were 18.91 ± 8.4 μg/ml and 0.39 ± 0.22 μg/ml, respectively.

Relationship between clinical characteristics and TBS in HIV-infected patients

Table 3 shows the demographic, laboratory, and disease-related parameters in HIV-infected patients with normal TBS values and HIV-infected patients with low TBS values. BMI, current smoking status, and presence of diabetes mellitus did not differ between the normal-TBS and low-TBS groups. Serum creatinine levels were significantly lower in HIV-infected patients with low TBS (p = 0.003); however, calcium (p = 0.21), phosphorus (p = 0.19), alkaline phosphatase (p = 0.38), 25[OH]D (p = 0.80), osteocalcin (p = 0.41), and CTX (p = 0.08) levels did not differ between the groups. Duration since HIV diagnosis, nadir CD4 T-cell count, TDF exposure, duration of TDF treatment, duration of ART, and ART regimen type did not differ between the normal-TBS and low-TBS groups.

Table 3 Demographic, laboratory, and disease-related variables in HIV-infected patients with normal TBS and low TBS
Full size table

Discussion

In this cross-sectional study, TBS values were significantly lower in HIV-infected young male patients than in age- and sex-matched controls. Furthermore, TBS values were positively correlated with BMD at the lumbar spine, femoral neck, and total hip and negatively correlated with the duration of TDF exposure.

The difference in TBS values between individuals with and without HIV is consistent with prior results from the Women’s Interagency HIV Study [14]. It is well known that age, postmenopausal status, smoking, and low BMI are risk factors for osteoporosis in the general population, and that HIV-related factors such as the direct action of the virus, chronic immune activation, and antiviral toxicity can also affect bone structure [2, 12, 15, 16]. A strength of the present study is that we included only HIV-infected male patients aged between 18 and 50 years to minimize the effects of the general risk factors.

TDF, an acyclic nucleotide analog of adenosine monophosphate, is widely used as a core component of many ART regimens, and several longitudinal studies have reported an association between TDF treatment and significantly reduced BMD [17, 18]. Thus, long-term use of TDF may lead to clinically relevant changes in BMD. One study reported a significant decrease in BMD and TBS after 1 year of TDF therapy [19]. We found that TBS, a measure of bone microarchitecture, was negatively correlated with TDF exposure, suggesting that TDF can affect not only the quantity of bone, but also its microarchitecture. We did not analyze the factors associated with low TBS because of the small number of patients with low TBS values; however, creatinine levels differed between the low-TBS and normal-TBS patient groups. Although the mechanism by which TDF causes bone toxicity is still unclear, TDF has both direct and indirect effects on bone via renal and endocrine systems [18, 20]. Subclinical tubulopathy may be a key factor in TDF-driven reductions in BMD, and our results support the hypothesis that renal function may affect bone microarchitecture in HIV-infected patients. This study also shows that TBS was marginally negatively correlated with the duration of HIV diagnosis, and uncorrelated with serum markers of bone turnover. CTX levels were slightly lower in the low-TBS patient group. HIV infection decreases bone formation and increases bone loss through direct effects related to the virus as well as through indirect effects related to pro-inflammatory cytokines, resulting in an increase in bone resorption and loss. However, the pathophysiology of bone fragility with HIV infection remains incompletely understood [2, 21]. Our results support the hypothesis that virus-associated factors, in addition to a patient’s clinical risk factors, contribute to bone turnover in young HIV-infected male patients despite suppression of the virus by ART. Animal experiments have shown that low BMI leads to osteoclast activation through enhanced production of the receptor activator of nuclear factor kappa-B (RANK) ligand by B-cells, accompanied by downregulation of the antagonist osteoprotegerin [22]. In the present study, the HIV-infected patients had lower BMI scores than the control subjects, which may have affected the bone. Further studies with larger patient groups are warranted to assess the risk factors and bone turnover markers associated with low TBS.

This study found that 21.3% of young male HIV-infected patients had a low BMD for their age (Z-score ≤ − 2.0). Currently, screening for osteoporosis with DXA is recommended in male HIV patients aged ≥50 years [12, 23]. A previous meta-analysis found that 67% of 884 HIV-infected patients had reduced BMD, of whom 15% had osteoporosis, yielding pooled odds ratios of 6.4 and 3.7, respectively, compared with non-HIV-infected controls [24], similar to our results for HIV-infected men aged 50 years and younger. Therefore, our results question the current guidelines for DXA screening in young HIV-infected men, although further studies will be needed to confirm our results. In this study, 7.5% of young HIV-infected men were deemed at high risk of fracture according to the TBS value, although a similar percentage was found for the control group. TBS, a texture index derived from DXA of the lumbar spine, is a widely available and endorsed technique and is included in the World Health Organization (WHO) Fracture Risk Assessment Tool [25, 26]. The correlation coefficient between TBS and BMD varies depending on the study. Some studies have shown that TBS correlates with lumbar BMD; however other studies reported that TBS correlates poorly with BMD [8, 27, 28]. This may be due to the diversity in the underlying diseases and differences in the demographic characteristics of the participants. Studies on the role of TBS as a complement to BMD and as a means of identifying cut-off values to predict fracture risk in HIV-infected populations are limited. Thus, additional studies are warranted to clarify the role that TBS may play in this patient population.

In this study, BMD values of the lumbar spine were not statistically significant between the two groups, although BMD results in HIV-infected patients were lower than in controls. A meta-analysis showed that the prevalence of osteopenia/osteoporosis of the lumbar spine [OR = 2.4 (95% Cl: 2.0–2.8)] and hip [OR = 2.6 (95%Cl: 2.2–3.0)] was significantly higher in HIV-infected groups than in controls [1]. This is probably due to sampling bias or the small number of patients. The pathogenesis of bone loss in HIV-infected patients is a complex and has not been established. Therefore, there exists a possibility that unknown processes are involved in bone turnover in HIV-infected patients.

This study has several limitations. First, laboratory markers related to bone metabolism, such as vitamin D and osteocalcin, were not examined in the control group so we could not compare these parameters between the two groups. Second, we did not obtain long-term follow-up TBS data, and were therefore unable to assess the extent to which TBS predicts fractures. Third, sampling bias could have occurred in the HIV-infected patients group and the control group.

Conclusion

We have presented a cross-sectional study of HIV-infected men aged 50 years and younger, and assessed bone microarchitecture via TBS in this patient population. We observed lower TBS and BMD values in HIV-infected young men than in the control group and found that TBS values were positively correlated with BMD at the lumbar spine, femoral neck, and total hip, and negatively correlated with the duration of TDF exposure.

Availability of data and materials

Not applicable.

Abbreviations

25[OH]D:

25-hydroxy vitamin D

ART:

Antiretroviral therapy

BMD:

Bone mineral density

BMI:

Low body mass index

CTX:

C-terminal cross-linking telopeptide of type I collagen

DXA:

Dual-energy X-ray absorptiometry

PTH:

Parathyroid hormone

SDs:

Standard deviations

TBS:

Trabecular bone score

TDF:

Tenofovir disoproxil fumarate

References

  1. Goh SSL, Lai PSM, Tan ATB, Ponnampalavanar S. Reduced bone mineral density in human immunodeficiency virus-infected individuals: a meta-analysis of its prevalence and risk factors: supplementary presentation. Osteoporos Int. 2018;29(7):1683.

    Article  CAS  Google Scholar 

  2. Compston J. HIV infection and bone disease. J Intern Med. 2016;280(4):350–8.

    Article  CAS  Google Scholar 

  3. Bijelic R, Milicevic S, Balaban J. Risk factors for osteoporosis in postmenopausal women. Mediev Archaeol. 2017;71(1):25–8.

    Google Scholar 

  4. Cannarella R, Barbagallo F, Condorelli RA, Aversa A, La Vignera S, Calogero AE. Osteoporosis from an Endocrine Perspective: The Role of Hormonal Changes in the Elderly. J Clin Med. 2019;8(10):1564–77.

    Article  Google Scholar 

  5. Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R, National OF. Clinician's guide to prevention and treatment of osteoporosis. Osteoporos Int. 2014;25(10):2359–81.

    Article  CAS  Google Scholar 

  6. Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP. Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res. 2014;29(3):518–30.

    Article  Google Scholar 

  7. Hans D, Goertzen AL, Krieg MA, Leslie WD. Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res. 2011;26(11):2762–9.

    Article  Google Scholar 

  8. Boutroy S, Hans D, Sornay-Rendu E, Vilayphiou N, Winzenrieth R, Chapurlat R. Trabecular bone score improves fracture risk prediction in non-osteoporotic women: the OFELY study. Osteoporos Int. 2013;24(1):77–85.

    Article  CAS  Google Scholar 

  9. Baim S, Leonard MB, Bianchi ML, Hans DB, Kalkwarf HJ, Langman CB, Rauch F. Official positions of the International Society for Clinical Densitometry and executive summary of the 2007 ISCD pediatric position development conference. J Clin Densitom. 2008;11(1):6–21.

    Article  Google Scholar 

  10. Yoon HE, Kim Y, Shin SJ, Hong YS, Kang KY. Factors associated with low trabecular bone scores in patients with end-stage kidney disease. J Bone Miner Metab. 2019;37(3):475–83.

    Article  Google Scholar 

  11. Kim HR, Hong YS, Park SH, Ju JH, Kang KY. Low bone mineral density predicts the formation of new syndesmophytes in patients with axial spondyloarthritis. Arthritis Res Ther. 2018;20(1):231.

    Article  Google Scholar 

  12. McComsey GA, Tebas P, Shane E, Yin MT, Overton ET, Huang JS, Aldrovandi GM, Cardoso SW, Santana JL, Brown TT. Bone disease in HIV infection: a practical review and recommendations for HIV care providers. Clin Infect Dis. 2010;51(8):937–46.

    Article  Google Scholar 

  13. McCloskey EV, Oden A, Harvey NC, Leslie WD, Hans D, Johansson H, Barkmann R, Boutroy S, Brown J, Chapurlat R, et al. A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res. 2016;31(5):940–8.

    Article  Google Scholar 

  14. Sharma A Ma Y, Tien PC, Scherzer R, Anastos K, Cohen MH, Hans D, Yin MT. HIV Infection Is Associated With Abnormal Bone Microarchitecture: Measurement of Trabecular Bone Score in the Women’s Interagency HIV Study. 2018.

  15. Castronuovo D, Cacopardo B, Pinzone MR, Di Rosa M, Martellotta F, Schioppa O, Moreno S, Nunnari G. Bone disease in the setting of HIV infection: update and review of the literature. Eur Rev Med Pharmacol Sci. 2013;17(18):2413–9.

    CAS  PubMed  Google Scholar 

  16. Kooij KW, Wit FW, Bisschop PH, Schouten J, Stolte IG, Prins M, van der Valk M, Prins JM, van Eck-Smit BL, Lips P, et al. Low bone mineral density in patients with well-suppressed HIV infection: association with body weight, smoking, and prior advanced HIV disease. J Infect Dis. 2015;211(4):539–48.

    Article  Google Scholar 

  17. Stellbrink HJ, Orkin C, Arribas JR, Compston J, Gerstoft J, Van Wijngaerden E, Lazzarin A, Rizzardini G, Sprenger HG, Lambert J, et al. Comparison of changes in bone density and turnover with abacavir-lamivudine versus tenofovir-emtricitabine in HIV-infected adults: 48-week results from the ASSERT study. Clin Infect Dis. 2010;51(8):963–72.

    Article  Google Scholar 

  18. Woodward CL, Hall AM, Williams IG, Madge S, Copas A, Nair D, Edwards SG, Johnson MA, Connolly JO. Tenofovir-associated renal and bone toxicity. HIV Med. 2009;10(8):482–7.

    Article  CAS  Google Scholar 

  19. Guerri-Fernandez R, Lerma-Chippirraz E, Fernandez Marron A, Garcia-Giralt N, Villar-Garcia J, Soldado-Folgado J, Gonzalez-Mena A, Trenchs-Rodriguez M, Guelar A, Diez-Perez A, et al. Bone density, microarchitecture, and tissue quality after 1 year of treatment with tenofovir disoproxil fumarate. AIDS. 2018;32(7):913–20.

    Google Scholar 

  20. Grant PM, Cotter AG. Tenofovir and bone health. Curr Opin HIV AIDS. 2016;11(3):326–32.

    Article  CAS  Google Scholar 

  21. Mirza FS, Luthra P, Chirch L. Endocrinological aspects of HIV infection. J Endocrinol Investig. 2018;41(8):881–99.

    Article  CAS  Google Scholar 

  22. Vikulina T, Fan X, Yamaguchi M, Roser-Page S, Zayzafoon M, Guidot DM, Ofotokun I, Weitzmann MN. Alterations in the immuno-skeletal interface drive bone destruction in HIV-1 transgenic rats. Proc Natl Acad Sci U S A. 2010;107(31):13848–53.

    Article  CAS  Google Scholar 

  23. Aberg JA, Gallant JE, Anderson J, Oleske JM, Libman H, Currier JS, Stone VE, Kaplan JE. America HIVMAotIDSo. Primary care guidelines for the management of persons infected with human immunodeficiency virus: recommendations of the HIV medicine Association of the Infectious Diseases Society of America. Clin Infect Dis. 2004;39(5):609–29.

    Article  Google Scholar 

  24. Brown TT, Qaqish RB. Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review. AIDS. 2006;20(17):2165–74.

    Article  Google Scholar 

  25. Silva BC, Broy SB, Boutroy S, Schousboe JT, Shepherd JA, Leslie WD. Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 2: trabecular bone score. J Clin Densitom. 2015;18(3):309–30.

    Article  Google Scholar 

  26. Leslie WD, Johansson H, Kanis JA, Lamy O, Oden A, McCloskey EV, Hans D. Lumbar spine texture enhances 10-year fracture probability assessment. Osteoporos Int. 2014;25(9):2271–7.

    Article  CAS  Google Scholar 

  27. Breban S, Briot K, Kolta S, Paternotte S, Ghazi M, Fechtenbaum J, Roux C. Identification of rheumatoid arthritis patients with vertebral fractures using bone mineral density and trabecular bone score. J Clin Densitom. 2012;15(3):260–6.

    Article  Google Scholar 

  28. Dufour R, Winzenrieth R, Heraud A, Hans D, Mehsen N. Generation and validation of a normative, age-specific reference curve for lumbar spine trabecular bone score (TBS) in French women. Osteoporos Int. 2013;24(11):2837–46.

    Article  CAS  Google Scholar 

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Acknowledgements

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Funding

This work was supported by the National Research Foundation of Korea (NRF-2018R1D1A1A02085712) grant funded by the Korea government.

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Author notes

  1. Youn Jeong Kim and Kwi Young Kang contributed equally to this work.

Authors and Affiliations

  1. Division of Infectious Disease, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul, South Korea

    Youn Jeong Kim, Yoonhee Jun, Sang Il Kim & Yang Ree Kim

  2. Department of Internal Medicine, Incheon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, #56, Donsu-Ro, Bupyung-Gu, Incheon, South Korea

    Youn Jeong Kim & Kwi Young Kang

  3. Division of Rheumatology, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul, South Korea

    Kwi Young Kang

  4. Health Promotion Center, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, South Korea

    Juyoung Shin

  5. Division of Endocrinology and Metabolism, Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul, South Korea

    Juyoung Shin

  6. Department of Internal Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 505 Banpodong, Seochogu, 137-701, Seoul, Republic of Korea

    Yoonhee Jun & Sang Il Kim

  7. Department of Internal Medicine, Uijeongbu St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Chonboro 271, Uijeongbu, South Korea

    Yang Ree Kim

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Contributions

YJK contributed to the conception, design, data collection, interpretation, funding and writing of the paper. KYK contributed to the conception, design, data collection, analysis and interpretation. JYS contributed data collection, interpretation and critical review. YHJ and YRK contributed to critical review. SIK contributed to data collection, interpretation, critical review as well as revision of article. All authors read and approved the final manuscript.

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Correspondence to Sang Il Kim.

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Ethics approval and consent to participate

The study was approved by the ethics committee of Seoul St. Mary’s Hospital (study number: KC14OISI0768). Written informed consent according to the Declaration of Helsinki was obtained from all study subjects.

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Supplementary information

Additional file 1: Figure S1.

Correlation between trabecular bone score (TBS) and TDF exposure time. TDF, Tenofovir disoproxil fumarate.

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Kim, Y.J., Kang, K.Y., Shin, J. et al. Trabecular bone scores in young HIV-infected men: a matched case-control study. BMC Musculoskelet Disord 21, 94 (2020). https://doi.org/10.1186/s12891-020-3092-0

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  • DOI: https://doi.org/10.1186/s12891-020-3092-0

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BMC Musculoskeletal Disorders

ISSN: 1471-2474

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