Skip to main content
Top
Published in: BMC Endocrine Disorders 1/2023

Open Access 01-12-2023 | Osteoporosis | Research

Prevalence of osteoporosis in patients with diabetes mellitus: a systematic review and meta-analysis of observational studies

Authors: Xueying Liu, Fuhua Chen, Lei Liu, Qiu Zhang

Published in: BMC Endocrine Disorders | Issue 1/2023

Login to get access

Abstract

Background

Osteoporosis (OP) and diabetes mellitus (DM) are two major healthcare issues in the world. Numerous population based-studies have reported an increased prevalence of OP among individuals with DM, though, estimates vary significantly.

Purpose

The objective of this study is to estimate the prevalence of OP in patients with DM.

Methods

To identify relevant literature, PubMed, Embase, Medline, CBM and Cochrane Library were searched for studies published from inception till July 2022, The search was conducted, and studies were included without countries and language restrictions. For full-text articles included in the study, the references were also independently searched. Random inverse variance-weighted models were used by Stata version 17.0 to estimate the prevalence of OP in patients with diabetes across studies. The heterogeneity was examined with I2 via the χ2 test on Cochrane’s Q statistic. Subgroup analysis and meta-regression were used to explore potential sources of heterogeneity. Egger’s test was used to assess publication bias.

Results

A high OP prevalence of 27.67% (95% confidence interval (CI) 21.37-33.98%) was found in a pooled analysis of 21 studies involving 11,603 T2DM patients. Methodological value of the included articles was high, with only three medium-quality studies and no low-quality studies. A significantly high heterogeneity (I2 = 98.5%) was observed.

Conclusions

Worldwide, a high prevalence of OP was found in patients with T2DM. Therefore, strong measures to prevent and treat osteoporosis in diabetic patients are required.

Trial registration

This study has been registered on PROSPERO, number CRD42021286580.
Appendix
Available only for authorised users
Literature
1.
go back to reference Consensus development conference. Diagnosis, prophylaxis, and treatment of osteoporosis. Am J Med. 1993;94(6):646–50.CrossRef Consensus development conference. Diagnosis, prophylaxis, and treatment of osteoporosis. Am J Med. 1993;94(6):646–50.CrossRef
2.
go back to reference Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet. 2019;393(10169):364–76.CrossRef Compston JE, McClung MR, Leslie WD. Osteoporosis. Lancet. 2019;393(10169):364–76.CrossRef
3.
go back to reference Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 9(th) edition. Diabetes Res Clin Pract. 2019;157:107843.CrossRef Saeedi P, Petersohn I, Salpea P, Malanda B, Karuranga S, Unwin N, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 9(th) edition. Diabetes Res Clin Pract. 2019;157:107843.CrossRef
4.
go back to reference Pan Y, Xu J. Association between muscle mass, bone mineral density and osteoporosis in type 2 diabetes. J Diabetes Investig. 2022;13(2):351–8.CrossRef Pan Y, Xu J. Association between muscle mass, bone mineral density and osteoporosis in type 2 diabetes. J Diabetes Investig. 2022;13(2):351–8.CrossRef
5.
go back to reference Xiu S, Chhetri JK, Sun L, Mu Z, Wang L. Association of serum prealbumin with risk of osteoporosis in older adults with type 2 diabetes mellitus: a cross-sectional study. Ther Adv Chronic Dis. 2019;10:2040622319857361.CrossRef Xiu S, Chhetri JK, Sun L, Mu Z, Wang L. Association of serum prealbumin with risk of osteoporosis in older adults with type 2 diabetes mellitus: a cross-sectional study. Ther Adv Chronic Dis. 2019;10:2040622319857361.CrossRef
6.
go back to reference Si Y, Wang C, Guo Y, Xu G, Ma Y. Prevalence of osteoporosis in patients with type 2 diabetes mellitus in the Chinese mainland: a systematic review and Meta-analysis. Iran J Public Health. 2019;48(7):1203–14. Si Y, Wang C, Guo Y, Xu G, Ma Y. Prevalence of osteoporosis in patients with type 2 diabetes mellitus in the Chinese mainland: a systematic review and Meta-analysis. Iran J Public Health. 2019;48(7):1203–14.
7.
go back to reference Wang L, Yu W, Yin X, Cui L, Tang S, Jiang N, et al. Prevalence of osteoporosis and fracture in China: the China osteoporosis prevalence study. JAMA Netw Open. 2021;4(8):e2121106.CrossRef Wang L, Yu W, Yin X, Cui L, Tang S, Jiang N, et al. Prevalence of osteoporosis and fracture in China: the China osteoporosis prevalence study. JAMA Netw Open. 2021;4(8):e2121106.CrossRef
8.
go back to reference Hoy D, Brooks P, Woolf A, Blyth F, March L, Bain C, et al. Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol. 2012;65(9):934–9.CrossRef Hoy D, Brooks P, Woolf A, Blyth F, March L, Bain C, et al. Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol. 2012;65(9):934–9.CrossRef
9.
go back to reference Noubiap JJ, Bigna JJ, Nansseu JR, Nyaga UF, Balti EV, Echouffo-Tcheugui JB, et al. Prevalence of dyslipidaemia among adults in Africa: a systematic review and meta-analysis. Lancet Glob Health. 2018;6(9):e998–e1007.CrossRef Noubiap JJ, Bigna JJ, Nansseu JR, Nyaga UF, Balti EV, Echouffo-Tcheugui JB, et al. Prevalence of dyslipidaemia among adults in Africa: a systematic review and meta-analysis. Lancet Glob Health. 2018;6(9):e998–e1007.CrossRef
10.
go back to reference Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013;67(11):974–8.CrossRef Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013;67(11):974–8.CrossRef
11.
go back to reference DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.CrossRef DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.CrossRef
12.
go back to reference World Health Organization. WHO: recommended definitions, terminology and format for statistical tables related to the perinatal period and use of a new certificate for cause of perinatal deaths. Modifications recommended by FIGO as amended October 14, 1976. Acta Obstet Gynecol Scand. 1977;56(3):247–53. World Health Organization. WHO: recommended definitions, terminology and format for statistical tables related to the perinatal period and use of a new certificate for cause of perinatal deaths. Modifications recommended by FIGO as amended October 14, 1976. Acta Obstet Gynecol Scand. 1977;56(3):247–53.
13.
go back to reference He W, Li Q, Yang M, Jiao J, Ma X, Zhou Y, et al. Lower BMI cutoffs to define overweight and obesity in China. Obesity (Silver Spring). 2015;23(3):684–91.CrossRef He W, Li Q, Yang M, Jiao J, Ma X, Zhou Y, et al. Lower BMI cutoffs to define overweight and obesity in China. Obesity (Silver Spring). 2015;23(3):684–91.CrossRef
14.
go back to reference Schwartz AV, Sellmeyer DE, Strotmeyer ES, Tylavsky FA, Feingold KR, Resnick HE, et al. Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res. 2005;20(4):596–603.CrossRef Schwartz AV, Sellmeyer DE, Strotmeyer ES, Tylavsky FA, Feingold KR, Resnick HE, et al. Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res. 2005;20(4):596–603.CrossRef
15.
go back to reference Li X, Chattopadhyay K, Xu S, Chen Y, Xu M, Li L, et al. Prevalence of comorbidities and their associated factors in patients with type 2 diabetes at a tertiary care department in Ningbo, China: a cross-sectional study. BMJ Open. 2021;11(1):e040532. Li X, Chattopadhyay K, Xu S, Chen Y, Xu M, Li L, et al. Prevalence of comorbidities and their associated factors in patients with type 2 diabetes at a tertiary care department in Ningbo, China: a cross-sectional study. BMJ Open. 2021;11(1):e040532.
16.
go back to reference Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629–34.CrossRef Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997;315(7109):629–34.CrossRef
17.
go back to reference De Luis Román DA, Aller R, Perez Castrillon JL, De Luis J, Gonzalez Sagrado M, Izaola O, et al. Effects of dietary intake and life style on bone density in patients with diabetes mellitus type 2. Ann Nutr Metab. 2004;48(3):141–5.CrossRef De Luis Román DA, Aller R, Perez Castrillon JL, De Luis J, Gonzalez Sagrado M, Izaola O, et al. Effects of dietary intake and life style on bone density in patients with diabetes mellitus type 2. Ann Nutr Metab. 2004;48(3):141–5.CrossRef
18.
go back to reference Afshinnia F, Chacko S, Zahedi T. Association of lower serum cholesterol levels with higher risk of osteoporosis in type 2 diabetes. Endocr Pract. 2007;13(6):620–8.CrossRef Afshinnia F, Chacko S, Zahedi T. Association of lower serum cholesterol levels with higher risk of osteoporosis in type 2 diabetes. Endocr Pract. 2007;13(6):620–8.CrossRef
19.
go back to reference Yaturu S, Humphrey S, Landry C, Jain SK. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit. 2009;15(1):CR5–9. Yaturu S, Humphrey S, Landry C, Jain SK. Decreased bone mineral density in men with metabolic syndrome alone and with type 2 diabetes. Med Sci Monit. 2009;15(1):CR5–9.
20.
go back to reference Viegas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F. Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. J Diabetes Complicat. 2011;25(4):216–21.CrossRef Viegas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F. Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. J Diabetes Complicat. 2011;25(4):216–21.CrossRef
21.
go back to reference Karimifar M, Pasha MAP, Salari A, Zamani A, Salesi M, Motaghi P. Evaluation of bone loss in diabetic postmenopausal women. J Res Med Sci. 2012;17(11):1033–8. Karimifar M, Pasha MAP, Salari A, Zamani A, Salesi M, Motaghi P. Evaluation of bone loss in diabetic postmenopausal women. J Res Med Sci. 2012;17(11):1033–8.
22.
go back to reference Jianbo L, Zhang H, Yan L, Xie M, Mei Y, Jiawei C. Homocysteine, an additional factor, is linked to osteoporosis in postmenopausal women with type 2 diabetes. J Bone Miner Metab. 2014;32(6):718–24.CrossRef Jianbo L, Zhang H, Yan L, Xie M, Mei Y, Jiawei C. Homocysteine, an additional factor, is linked to osteoporosis in postmenopausal women with type 2 diabetes. J Bone Miner Metab. 2014;32(6):718–24.CrossRef
23.
go back to reference Al-Homood IA, Sheshah I, Mohammed AGA, Gasim GI. The prevalence and risk factors of osteoporosis among a Saudi female diabetic population. Open Access Maced J Med Sci. 2017;5(2):177–81.CrossRef Al-Homood IA, Sheshah I, Mohammed AGA, Gasim GI. The prevalence and risk factors of osteoporosis among a Saudi female diabetic population. Open Access Maced J Med Sci. 2017;5(2):177–81.CrossRef
24.
go back to reference Zhou L, Song J, Yang S, Meng S, Lv X, Yue J, et al. Bone mass loss is associated with systolic blood pressure in postmenopausal women with type 2 diabetes in Tibet: a retrospective cross-sectional study. Osteoporos Int. 2017;28(5):1693–8.CrossRef Zhou L, Song J, Yang S, Meng S, Lv X, Yue J, et al. Bone mass loss is associated with systolic blood pressure in postmenopausal women with type 2 diabetes in Tibet: a retrospective cross-sectional study. Osteoporos Int. 2017;28(5):1693–8.CrossRef
25.
go back to reference Abdulameer SA, Sahib MN, Sulaiman SAS. The prevalence of osteopenia and osteoporosis among Malaysian type 2 diabetic patients using quantitative ultrasound densitometer. Open Rheumatol J. 2018;12:50–64.CrossRef Abdulameer SA, Sahib MN, Sulaiman SAS. The prevalence of osteopenia and osteoporosis among Malaysian type 2 diabetic patients using quantitative ultrasound densitometer. Open Rheumatol J. 2018;12:50–64.CrossRef
26.
go back to reference Kanazawa I, Takeno A, Tanaka KI, Yamane Y, Sugimoto T. Osteoporosis and vertebral fracture are associated with deterioration of activities of daily living and quality of life in patients with type 2 diabetes mellitus. J Bone Miner Metab. 2019;37(3):503–11.CrossRef Kanazawa I, Takeno A, Tanaka KI, Yamane Y, Sugimoto T. Osteoporosis and vertebral fracture are associated with deterioration of activities of daily living and quality of life in patients with type 2 diabetes mellitus. J Bone Miner Metab. 2019;37(3):503–11.CrossRef
27.
go back to reference Guo Y, Wang Y, Chen F, Wang J, Wang D. Assessment of risk factors for fractures in patients with type 2 diabetes over 60 years old: a cross-sectional study from Northeast China. J Diabetes Res. 2020;2020:1508258.CrossRef Guo Y, Wang Y, Chen F, Wang J, Wang D. Assessment of risk factors for fractures in patients with type 2 diabetes over 60 years old: a cross-sectional study from Northeast China. J Diabetes Res. 2020;2020:1508258.CrossRef
28.
go back to reference Li Y, Zhao Z, Wang L, Fu Z, Ji L, Wu X. The prevalence of osteoporosis tested by quantitative computed tomography in patients with different glucose tolerances. J Clin Endocrinol Metab. 2020;105(1):dgz036. Li Y, Zhao Z, Wang L, Fu Z, Ji L, Wu X. The prevalence of osteoporosis tested by quantitative computed tomography in patients with different glucose tolerances. J Clin Endocrinol Metab. 2020;105(1):dgz036.
29.
go back to reference Qiu M, Zhai S, Liu D. DPP4 activities are associated with osteopenia/osteoporosis and fracture risk in newly diagnosed type 2 diabetes. Int J Endocrinol. 2020;2020:8874272. Qiu M, Zhai S, Liu D. DPP4 activities are associated with osteopenia/osteoporosis and fracture risk in newly diagnosed type 2 diabetes. Int J Endocrinol. 2020;2020:8874272.
30.
go back to reference Fang L, Zhong S, Ma D, Li C, Hao Y, Gao Y, et al. A cross-sectional study: an assessment of low muscle mass and osteoporosis in type 2 diabetes mellitus patients with a high glycated hemoglobin level. Ther Adv Chronic Dis. 2021;12:20406223211026762. Fang L, Zhong S, Ma D, Li C, Hao Y, Gao Y, et al. A cross-sectional study: an assessment of low muscle mass and osteoporosis in type 2 diabetes mellitus patients with a high glycated hemoglobin level. Ther Adv Chronic Dis. 2021;12:20406223211026762.
31.
go back to reference Ghodsi M, Keshtkar AA, Razi F, Mohammad Amoli M, Nasli-Esfahani E, Zarrabi F, et al. Association of vitamin D receptor gene polymorphism with the occurrence of low bone density, osteopenia, and osteoporosis in patients with type 2 diabetes. J Diabetes Metab Disord. 2021;20(2):1375–83.CrossRef Ghodsi M, Keshtkar AA, Razi F, Mohammad Amoli M, Nasli-Esfahani E, Zarrabi F, et al. Association of vitamin D receptor gene polymorphism with the occurrence of low bone density, osteopenia, and osteoporosis in patients with type 2 diabetes. J Diabetes Metab Disord. 2021;20(2):1375–83.CrossRef
32.
go back to reference Li J, Niu X, Si Q, Song Q, Jin M, Zhou R, et al. Plasma periostin as a biomarker of osteoporosis in postmenopausal women with type 2 diabetes. J Bone Miner Metab. 2021;39(4):631–8.CrossRef Li J, Niu X, Si Q, Song Q, Jin M, Zhou R, et al. Plasma periostin as a biomarker of osteoporosis in postmenopausal women with type 2 diabetes. J Bone Miner Metab. 2021;39(4):631–8.CrossRef
33.
go back to reference Wu Y, Xiang S, Jiang X, Wang L, Wang K, Hua F. Relationship of bone status with serum uric acid and bilirubin in men with type 2 diabetes: a cross-sectional study. Med Sci Monit. 2021;27:e930410. Wu Y, Xiang S, Jiang X, Wang L, Wang K, Hua F. Relationship of bone status with serum uric acid and bilirubin in men with type 2 diabetes: a cross-sectional study. Med Sci Monit. 2021;27:e930410.
34.
go back to reference Xu X, Zhang M, Fei Z, Sheng H, Qu S, Cui R. Calcification of lower extremity arteries is related to the presence of osteoporosis in postmenopausal women with type 2 diabetes mellitus: a cross-sectional observational study. Osteoporos Int. 2021;32(6):1185–93.CrossRef Xu X, Zhang M, Fei Z, Sheng H, Qu S, Cui R. Calcification of lower extremity arteries is related to the presence of osteoporosis in postmenopausal women with type 2 diabetes mellitus: a cross-sectional observational study. Osteoporos Int. 2021;32(6):1185–93.CrossRef
35.
go back to reference Leidig-Bruckner G, Grobholz S, Bruckner T, Scheidt-Nave C, Nawroth P, Schneider JG. Prevalence and determinants of osteoporosis in patients with type 1 and type 2 diabetes mellitus. BMC Endocr Disord. 2014;14:33.CrossRef Leidig-Bruckner G, Grobholz S, Bruckner T, Scheidt-Nave C, Nawroth P, Schneider JG. Prevalence and determinants of osteoporosis in patients with type 1 and type 2 diabetes mellitus. BMC Endocr Disord. 2014;14:33.CrossRef
36.
go back to reference Qi W, Jiang Y, Liu W, Chi Y, Jiajue R, Pang Q, et al. Bone microarchitecture in obese postmenopausal Chinese women: the Chinese vertebral osteoporosis study (ChiVOS). Front Endocrinol (Lausanne). 2022;13:891413.CrossRef Qi W, Jiang Y, Liu W, Chi Y, Jiajue R, Pang Q, et al. Bone microarchitecture in obese postmenopausal Chinese women: the Chinese vertebral osteoporosis study (ChiVOS). Front Endocrinol (Lausanne). 2022;13:891413.CrossRef
37.
go back to reference NIH consensus development panel on osteoporosis prevention D, and therapy. Osteoporosis prevention, diagnosis, and therapy. Jama. 2001;285(6):785–95.CrossRef NIH consensus development panel on osteoporosis prevention D, and therapy. Osteoporosis prevention, diagnosis, and therapy. Jama. 2001;285(6):785–95.CrossRef
38.
go back to reference Wright NC, Looker AC, Saag KG, Curtis JR, Delzell ES, Randall S, et al. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res. 2014;29(11):2520–6.CrossRef Wright NC, Looker AC, Saag KG, Curtis JR, Delzell ES, Randall S, et al. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res. 2014;29(11):2520–6.CrossRef
40.
go back to reference Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al. Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med. 2004;164(10):1108–12.CrossRef Siris ES, Chen YT, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, et al. Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med. 2004;164(10):1108–12.CrossRef
41.
go back to reference Xu Y, Wu Q. Decreasing trend of bone mineral density in US multiethnic population: analysis of continuous NHANES 2005-2014. Osteoporos Int. 2018;29(11):2437–46.CrossRef Xu Y, Wu Q. Decreasing trend of bone mineral density in US multiethnic population: analysis of continuous NHANES 2005-2014. Osteoporos Int. 2018;29(11):2437–46.CrossRef
42.
go back to reference Chen HL, Deng LL, Li JF. Prevalence of osteoporosis and its associated factors among older men with type 2 diabetes. Int J Endocrinol. 2013;2013:285729.CrossRef Chen HL, Deng LL, Li JF. Prevalence of osteoporosis and its associated factors among older men with type 2 diabetes. Int J Endocrinol. 2013;2013:285729.CrossRef
43.
go back to reference Doğan A, Nakipoğlu-Yüzer GF, Yıldızgören MT, Ozgirgin N. Is age or the body mass index (BMI) more determinant of the bone mineral density (BMD) in geriatric women and men? Arch Gerontol Geriatr. 2010;51(3):338–41.CrossRef Doğan A, Nakipoğlu-Yüzer GF, Yıldızgören MT, Ozgirgin N. Is age or the body mass index (BMI) more determinant of the bone mineral density (BMD) in geriatric women and men? Arch Gerontol Geriatr. 2010;51(3):338–41.CrossRef
Metadata
Title
Prevalence of osteoporosis in patients with diabetes mellitus: a systematic review and meta-analysis of observational studies
Authors
Xueying Liu
Fuhua Chen
Lei Liu
Qiu Zhang
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Endocrine Disorders / Issue 1/2023
Electronic ISSN: 1472-6823
DOI
https://doi.org/10.1186/s12902-022-01260-8

Other articles of this Issue 1/2023

BMC Endocrine Disorders 1/2023 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine