https://orcid.org/0009-0000-0679-2473
Figures
Abstract
Introduction
In spine surgery, poor bone condition is associated with several complications like adjacent segment fractures, proximal junctional kyphosis, and screw loosening. Our study explored the prevalence of osteoporosis in spinal surgery patients older than 50 years through a systematic review and meta-analysis.
Methods
This systematic review and meta-analysis were conducted according to the PRISMA criteria. Three electronic databases, including PubMed, EMBASE, and Web of Science, were searched from inception to August 2022. We used the random-effects model to calculate the overall estimates, and the heterogeneity was measured using Cochran’s Q and I2 tests. Meta-regression and subgroup analyses were used to determine the source of the heterogeneity.
Results
Based on the inclusion and criteria, we chose ten studies with 2958 individuals for our analysis. The prevalence of osteoporosis, osteopenia, and osteoporosis/osteopenia in the spinal surgery patients was 34.2% (95%CI: 24.5%–44.6%), 43.5% (95%CI: 39.8%–47.2%), and 78.7% (95%CI: 69.0%–87.0%), respectively. Regarding different diagnoses, the prevalence was highest in patients with lumbar scoliosis (55.8%; 95%CI: 46.8%-64.7%) and the lowest in patients with cervical disc herniation (12.9%; 95%CI: 8.1%-18.7%). In age groups 50–59, 50–69,70–79, the prevalence was 27.8%, 60.4%, 75.4% in females, and 18.9%, 17.4%, 26.1% in males.
Conclusions
This study showed a high prevalence of osteoporosis in patients undergoing spine surgery, especially in females, people of older age, and patients who received degenerative scoliosis and compression fractures. Current osteoporosis screening standards for patients undergoing spine surgery may not be adequate. Orthopedic specialists should make more efforts regarding preoperative osteoporosis screening and treatment.
Citation: Fan Z-q, Yan X-a, Li B-f, Shen E, Xu X, Wang H, et al. (2023) Prevalence of osteoporosis in spinal surgery patients older than 50 years: A systematic review and meta-analysis. PLoS ONE 18(5): e0286110. https://doi.org/10.1371/journal.pone.0286110
Editor: Koji Akeda, Mie University Graduate School of Medicine, JAPAN
Received: January 25, 2023; Accepted: May 9, 2023; Published: May 25, 2023
Copyright: © 2023 Fan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper and its Supporting Information files.
Funding: Shaanxi Provincial Department of Science and Technology, Innovative Talents Promotion Plan - Youth Science and Technology Star Project (2021KJXX-57), Dr Zhi-qiang Fan. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: No applicable
List of abbreviations: BMD, Bone mineral density; DXA, Dual-energy Xray absorptiometry; ISCD, International Society for Clinical Densitometry; PRISMA, Preferred Reporting Items for Systematic and Meta-analyses guidelines
Introduction
Osteoporosis is a common disease in the elderly, characterized by a decrease in bone mass and an increased risk of fragility fractures [1]. In adults aged> 50 years, the global prevalence of osteoporosis was reported as 20.5% [2]. Twenty-two million women and 5.5 million men were estimated to experience osteoporosis in Europe in 2010, causing 3.5 million fragility fractures and a €37 billion economic burden annually [3].
As the global population ages, more people are required to receive spine surgery, which burdens society heavily [4]. In spine surgery, osteoporosis has been considered to be linked with several complications, including adjacent segment fractures, screw loosening, and proximal junctional kyphosis [5, 6]. For instance, Bone mineral density (BMD) is a key determinant of screw fusion rates in spine surgery. A lower spine BMD could result in a long recovery time for patients who experienced fusion procedures with instrumentation [7]. Previous studies showed that osteoporosis was highly prevalent in spinal surgery patients [8, 9]. In a cohort of 104 spine surgery candidates, Anderson PA et al. [8] reported 48 patients (46%) with osteoporosis and 50 patients (48%) with osteopenia when using WHO (World health organization) diagnosis criteria (osteopenia as -2.5 < T-score < -1.0, osteoporosis as T-scores< -2.5). In a retrospective study conducted by Chin DK et al. [9], osteoporosis was found in 51.4% of females and 14.5% of males undergoing spine surgery. Strategies like drug treatment, the use of cement augmentation of pedicle screws, multiple points fixations, and the newly designed pedicle screw have been carried out by surgeons to address the issues [10, 11]. In a prospective study in Japan, S. Ohtori et al. [12] found that teriparatide could improve the quality of the pedicle cortex and bone marrow. Nevertheless, surgeons did not pay enough attention to the bone quality of spinal surgery patients [13, 14]. A survey of surgeons showed that only 44% of instrumented fusion patients received preoperative Dual-energy Xray absorptiometry (DXA). A recommendation by the International Society for Clinical Densitometry (ISCD) suggested that surgeons should evaluate bone health in males aged ≥70 years and females aged ≥65 years who undergo spine surgery [15]. In a study of preoperative BMD assessment for spinal deformity surgery, T. K. Kuprys et al. [16] reported that the rate of DXA screening was less than the recommended guidelines. In addition, the high prevalence of osteoporosis in female patients older than 50 indicated that the ISCD recommendation might not be adequate [17, 18]. Although some studies have investigated the prevalence of osteoporosis in spinal surgery patients, there has not been a study analyzing these data. Therefore, this study aims to estimate the osteoporosis prevalence in patients undergoing spine surgery through a systematic review and meta-analysis.
Methods
This study was conducted based on the Preferred Reporting Items for Systematic and Meta-analyses guidelines (PRISMA) [19] (PRISMA checklist; S1 Appendix).
Search strategy
Three electronic databases (PubMed, EMBASE, and Web of Science) were chosen for searching the article that reported the osteoporosis prevalence in patients undergoing spine surgery from inception to August 2022. The search language was limited to only English. The following terms and keywords were combined for searching: “spine surgery”, “lumbar surgery”, “osteoporosis”, “osteopenia”, “bone mineral density”, “prevalence”, “incidence”, and “epidemiology.” We also conducted a hand search of references in relevant articles. The detailed search strategy is listed in S2 Appendix.
Study eligibility
Two reviewers (FZQ, YXA) independently reviewed titles and abstracts on eligibility criteria for inclusion and then read the full article. Any discrepancies will be resolved by the discussion between two authors (FZQ, YXA) and a third reviewer (ZY). Inclusion criteria are as following: (1) Longitudinal observational studies; Cross-sectional studies (2) Studies reporting the osteoporosis prevalence in patients undergoing spine surgery (3) BMD was measured by DXA examination at femur or lumbar spine. (4) Osteoporosis and osteopenia were defined by WHO diagnosis criteria (osteopenia as -2.5 < T-score < -1.0, osteoporosis as T-scores< -2.5).
The exclusion criteria are as following: (1) Conference abstracts, reviews, letters, or comments. (2) BMD is not measured by DXA; (3) Studies with no full text or sufficient data.
Data extraction
Two reviewers independently collected the following data: Publication year, author’s name, study period, number of females, sample size, study design, number of patients with osteoporosis and osteopenia, diagnosis method, body mass index (BMI), mean age, DXA examination sites, procedure indications, and study quality. Any disagreements between two reviewers are resolved by discussing with a third reviewer.
Quality assessment
Each study was assessed using a quality assessment checklist developed from the ‘Risk of bias tool’ from Hoy et al. [20], which contains 10 criteria (S3 Appendix). Each criterion provides a "yes," "no," or "don’t know" response option. If the answer to a criterion is "yes," the score is "1." A "No" or "Don’t know" answer is scored as "0." Accordingly, the aggregate scores for the chart span from 0 to 10. Studies with scores between 8 to 10 are considered "low-risk," 5 to 7 are considered "moderate risk," and 0 and 4 are considered "high-risk." High-risk studies will be excluded after quality assessment.
Statistical analysis
All analyses were performed using R software (version 4.1). A random effects model was used to calculate the integrated estimates. To stabilize the variance, we transformed the data using the Freeman-Tukey double arcsine transform. The primary outcome was the pooled prevalence of osteoporosis and osteopenia in spinal surgery patients. We used Cochran’s Q test and the I2 statistic to analyze heterogeneity, and I2≥50% was considered high heterogeneity. Subgroup analysis was also conducted as follows: Sex (female, male); Procedure indications; Age (>50, 50–59, 60–69, 70–79); Continent (Europe, Asia, and North America). Funnel plot and Egger’s test were used to measure publication bias.
Results
Literature search and characteristic
Fig 1 provides the flow chart of study selection. We initially searched 2,936 citations from three databases (PubMed: 625, Embase: 1,133, Web of Science: 1,178). Then, 555 citations were excluded since duplication, 2,381 citations were excluded after the title and abstract screening, and 23 were excluded after full-text reading. Finally, 10 studies met the inclusion criteria for analysis. A total of 2,958 individuals (1,764 females and 1,194 males) undergoing spine surgery were included in our study. The osteoporosis prevalence varied from 9.6% to 50.8% in included studies. Studies were carried out in eight countries including Spin [21], Germany [22], Sweden [17], France [23], China [18, 24], Korea [9], India [25], America [8, 26]. The mean age of participants in individual studies varied from 60.9 to 71.2. The detailed characteristics of included studies were shown in Table 1. After quality assessment, there were 8 low-risk studies, 2 moderate-risk studies, and no high-risk studies. The quality assessment form was presented in S4 Appendix.
Overall
The overall osteoporosis prevalence in patients > 50 years undergoing spine surgery was 34.2% (95%CI: 24.5%–44.6%; I2 = 90.3%; P<0.01) (Fig 2A). The osteopenia prevalence was 43.5% (95%CI: 39.8%–47.2%; I2 = 56.3%; P = 0.01) (Fig 2B). The osteoporosis/osteopenia prevalence was 78.7% (95%CI: 69.0%–87.0%; I2 = 91.5%; P<0.01) (Fig 2C).
(a) prevalence of osteoporosis. (b) osteopenia. (c) osteoporosis /osteopenia.
Sex- and age-specific groups
The osteoporosis prevalence in male and female were 19.9% (95%CI: 9.1%–33.6%; I2 = 86.6%; P<0.01) and 43.0% (95%CI: 28.6%–58.1%; I2 = 89.5%; P<0.01) (S5 Appendix), respectively. In females, the osteoporosis prevalence in 50–59, 50–69, and 70–79 was 27.8%, 60.4%, 75.4% (Fig 3). In males, the prevalence of osteoporosis in 50–59, 50–69, and 70–79 was 18.9%, 17.4%, 26.1% (Fig 3).
Continent
Ten studies from three continents were included in our study. The prevalence of osteoporosis in Europe, Asia, and North America was 24.2% (95%CI: 8.9%–43.6%; I2 = 92.0%; P<0.01), 38.1% (95%CI: 36.1%–40.1%; I2 = 69.1%; P<0.01), 35.1% (95%CI: 16.5%–56.3%; I2 = 92.8%; P<0.01), respectively (Fig 4).
Diagnoses classification
The osteoporosis prevalence is different based on different diagnosis classifications (Fig 5). The highest prevalence occurred in patients with lumbar scoliosis (55.8%; 95%CI: 46.8%-64.7%; I2 = 0%; P = 0.86) (Fig 5A), and the lowest occurred in patients with cervical disc herniation (12.9%; 95%CI: 8.1%-18.7%; I2 = 0%; P = 0.48) (Fig 5F). In patients with a compression fracture, lumbar spinal stenosis, lumbar spondylolisthesis, and lumbar disc herniation were 53.0%, 34.9%, 30.8%, and 27.4%, respectively (Fig 5B–5E).
(a) Degenerative scoliosis. (b) Compression fracture. (c) Lumbar spinal stenosis. (d) Lumbar spondylolisthesis. (e) Lumbar disc herniation. (f) Cervical disc herniation.
Meta-regression analyses.
The results of meta-regression analysis indicated that sample size (P = 0.81), quality score (P = 0.99), number of female participants (P = 0.82), publication year (P = 0.92), mean age of participants (P = 0.93), and study design (P = 0.77) were not contributed to the overall heterogeneity (S6 Appendix).
Sensitivity analysis and publication bias.
After sensitivity analysis by eliminating individual studies, the overall osteoporosis prevalence varied from 31.6% (95%CI: 22.9–41.0%) to 37.4% (95%CI: 29.2–45.8%), and the I2 statistic values varied from 83.5% to 91.2%. The result of the funnel plot indicated the asymmetry between studies (S7 Appendix). However, Egger’s test (P = 0.61) indicated no publication bias.
Discussion
Our systematic review and meta-analysis showed a high prevalence of osteoporosis in spinal surgery patients. In total, the prevalence of osteoporosis, osteopenia, and osteoporosis/osteopenia in patients undergoing spine surgery is 34.2%, 43.5%, and 78.7%, respectively. The prevalence of osteoporosis is significantly higher in females (43.0%) than in males (19.9%). A recommendation by the International Society for Clinical Densitometry (ISCD) suggested that surgeons should evaluate bone health in males aged ≥70 years and females aged ≥65 years who undergo spine surgery [15]. However, our study showed an unexpectedly high osteoporosis prevalence in patients aged under these cut-offs. In age groups 50–59, 60–69, and 70–79, the prevalence of osteoporosis is 27.8%, 60.4%, and 75.4% in females and 18.9%, 17.4%, and 26.1% in males. Considering the high osteoporosis rate and its associated surgery complication, the current osteoporosis screening and treatment before spine surgery may not be inadequate and need to raise awareness among orthopedic specialists in the future.
In our study, the prevalence of osteoporosis was higher than in some previous studies that investigated ordinary people [2, 27]. A large population-based meta-analysis showed that the global prevalence of osteoporosis was 14.1%, 31.8%, 50.9% for females, and 10.3%, 12.9%, 22.6% for males in 50–59, 60–69, and 70–79 years [2]. The prevalence of osteoporosis in our study varied by different procedures. The prevalence is highest in patients with degenerative scoliosis (55.8%). The lowest prevalence of osteoporosis occurs in patients with cervical disc herniation (12.9%). This finding is consistent with the previous research by Pappou et al. [28], which indicated that degenerative scoliosis is an important predictor of osteoporosis. One explanation may be that patients with osteoporosis are more prone to deformation of the weaker vertebrae in case of asymmetric loading caused by degenerative facet joints and the lumbar disc [29]. Another possible reason is that lumbar degenerative diseases such as scoliosis can cause considerable restriction of activities, which is associated with bone loss and osteoporosis [30]. In contrast, most types of cervical disc herniation usually do not experience the activity restriction. Another non-negligible reason for a higher osteoporosis rate in degenerative scoliosis patients is that they are usually older than other patients, such as those with cervical disc herniation. Previous studies have shown that degenerative scoliosis usually starts around the age of 50, and the average age of these patients is 70.5 years [31]. Other spinal disorders have also been reported to be associated with a risk of osteoporosis. A study by Kim et al. [32] showed a higher bone turnover rate in patients with spinal stenosis. In a case-control study, Park et al. [33] suggested that patients with spinal stenosis are less likely to benefit from ibandronate treatment compared with the control group. The neurological claudication caused by spinal stenosis could lead to reduced strength in the lower extremities and a higher bone loss rate [34]. In addition, a large retrospective study showed that patients with untreated spinal cord cervical spondylosis had 1.59 times the risk of fracture compared to general population controls [35]. Lumbar spondylolisthesis may be associated with spinal curvatures, such as thoracic kyphosis, which is an important alternative osteoporosis marker [36, 37]. These direct or indirect factors may lead to a high osteoporosis rate in patients with spinal disorders. However, the pathological mechanisms contributing to the tendency of osteoporosis, such as its biomechanical alterations [38], need to be further investigated.
Our results showed the prevalence of osteoporosis in females (43.0%) is significantly higher than in males (19.9%), in line with the previous findings [39]. We found that female patients are more likely to be affected by age. In the 50–59 age group, the osteoporosis prevalence was slightly higher in women than in men (27.8% vs. 18.9%). However, In the 70–79 age group, the prevalence was much higher in women than in men (75.4% vs. 26.1%), and more than three-quarters of female patients had osteoporosis. Postmenopausal estrogen deficiency and differences in the distribution of factors like diabetes, obesity, and metabolic syndrome between the gender may account for this difference [40–42]. The subgroup analysis in the study showed that the previous was highest in Asia (38.1%) and lowest in Europe (24.2%). Some previous studies observed that Asians have lower BMD than Europeans, which could be explained by the smaller body and bone size of Asians [43, 44]. Nevertheless, more studies are needed to validate our results due to the potential heterogeneity led by the small number of enrolled studies.
Bone health in orthopedic surgery has attracted wide attention since it may influence the outcome of the surgery [45–47]. In joint arthroplasty [45], osteoporosis will impair osseointegration and lead to failed surgery. Similarly, osteoporosis in spine surgery has raised concerns recently, as successful spine surgery requires adequate BMD for proper fixation strength, long-term stability, and lower instrumentation failure risk [48]. In a retrospective study in America, DeWald et al. [49] investigated the early and late complications in osteoporosis patients who received lumbar fusions. They found that 13% of participants experienced early complications (under 3 months), including epidural hemaoma and adjacent compression fractures. Furthermore, late postoperative complications including pseudoarthroses with rod breakage (11%), disc herniation (4%), instrumentation loosening (7%), instrumentation (11%), and proximal junctional kyphosis (26%) [49]. In cervical spine surgery, Guzman et al. revealed that patients with osteoporosis experienced a higher risk of postoperative hemorrhage (OR: 1.70), a higher risk of revision (OR: 1.54) and a longer hospitalization time and costs [50]. Therefore, perioperative management has been widely used in osteoporotic patients, including pharmacological therapy, cement augmentation of pedicle screws, multiple points fixations, and the newly designed pedicle screw [10, 51]. In a prospective randomized trial, Nagahama et al. [52] found that patients who received an alendronate treatment had higher fusion rates and lowered cage subsidence rates compared with control group after posterior lumbar interbody fusion. Surgeons have widely discussed surgical techniques in the osteoporosis spine. Guo et al. [10] reported that selective cement augmentation of cranial and caudal pedicle screws could provide comparable stability for osteoporosis patients. Cement screws have been considered appropriate for osteoporotic spine [53]. The management of osteoporosis for patients undergoing elective spine surgeries should be a concern for orthopedic surgeons. Experts recommend that all patients undergoing elective spine surgery have adequate preoperative vitamin D and calcium status [54]. In addition, bone anabolic pharmaceuticals like abaloparatide or teriparatide are recommended as the first-line treatment for osteoporosis patients undergoing spine surgery if there are no contraindications [54]. However, several previous studies have reported insufficient preoperative bone health screening for spinal surgery [13, 55]. Díaz-Romero et al. showed that 32.5% of surgeons would not consider a bone health assessment before the spinal arthrodesis, and 37.7% of surgeons would not consider an osteoporosis treatment before and after treatment [55]. A survey of 114 surgeons revealed that only 60% of surgeons would consider a preoperative bone health assessment for patients who experienced a low-energy spine fracture. The proportion dropped to 44% for patients with instrumented fusion [13]. Thus, the high osteoporosis rate in spine surgery should be a major concern for spine surgeons, and bone health in patients undergoing spinal surgery should be appropriately screened and optimized.
Our study has some limitations. First, we included only DXA as a criterion for the osteoporosis diagnosis due to the original study data limitations. In recent years, the vertebral body HU values estimated from CT scans have been extensively studied for the assessment of osteoporosis [13, 56, 57]. Zou et al. reported a 74.1% diagnosis specificity of DXA compared with CT scans in patients with degenerative diseases. They explain that the CT HU is less affected by lumbar degeneration by avoiding the degenerative regions [18]. However, there has been no consensus on the specific HU values for diagnosing osteoporosis [56, 58]. More serious radiation damage from CT compared to DXA is also an essential factor in physician decision-making. Whether the CT scan for osteoporosis is better than DXA has also not been proven and needs further investigation [59, 60]. Second, osteoporosis was defined differently based on the femur or lumbar spine in the original studies. Previous studies have proven that the osteoporosis rate was different based on these sites in the same cohort [61]. Third, only ten studies and 2,958 participants were included in our analysis, which could increase the heterogeneity. Fourth, we included studies from different countries, which may increase heterogeneity because of the different backgrounds of the populations. Fifth, the overall heterogeneity across the studies was high. More studies with a larger sample and stronger evidence should be conducted to explore the association between osteoporosis and lumbar surgery.
Conclusion
Our results showed a high prevalence of osteoporosis in patients undergoing spine surgery, especially in females, people of older age, and patients who received degenerative scoliosis and compression fractures. Current osteoporosis screening standards for patients undergoing spine surgery may not be adequate. Orthopedic specialists should make more efforts regarding preoperative osteoporosis screening and treatment.
Supporting information
S2 Appendix. Detailed search strategy in three databases.
https://doi.org/10.1371/journal.pone.0286110.s002
(DOCX)
S3 Appendix. Risk of bias tool for prevalence studies.
https://doi.org/10.1371/journal.pone.0286110.s003
(DOCX)
S4 Appendix. The checklist of prevalence study quality.
https://doi.org/10.1371/journal.pone.0286110.s004
(DOCX)
S5 Appendix.
Forest plot of prevalence of female (a) and male (b) in patients undergoing spine surgery.
https://doi.org/10.1371/journal.pone.0286110.s005
(TIF)
S6 Appendix. Meta-regression analyses of the effects of potential moderators on overall heterogeneity.
https://doi.org/10.1371/journal.pone.0286110.s006
(DOCX)
S7 Appendix. The funnel plots for included studies of prevalence of osteoporosis in patients undergoing spine surgery.
https://doi.org/10.1371/journal.pone.0286110.s007
(TIF)
References
- 1. Sambrook PN. Osteoporosis. Med J Aust 1996;165:332–6 pmid:8862335
- 2. Xiao PL, Cui AY, Hsu CJ et al. Global, regional prevalence, and risk factors of osteoporosis according to the World Health Organization diagnostic criteria: a systematic review and meta-analysis. Osteoporos Int 2022. pmid:35687123
- 3. Hernlund E, Svedbom A, Ivergård M et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. A report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos 2013;8:136. pmid:24113837
- 4. Sivasubramaniam V, Patel HC, Ozdemir BA, Papadopoulos MC. Trends in hospital admissions and surgical procedures for degenerative lumbar spine disease in England: a 15-year time-series study. BMJ Open 2015;5:e009011. pmid:26671956
- 5. Lubelski D, Choma TJ, Steinmetz MP, Harrop JS, Mroz TE. Perioperative Medical Management of Spine Surgery Patients With Osteoporosis. Neurosurgery 2015;77 Suppl 4:S92–7. pmid:26378362
- 6. Uei H, Tokuhashi Y, Maseda M et al. Exploratory analysis of predictors of revision surgery for proximal junctional kyphosis or additional postoperative vertebral fracture following adult spinal deformity surgery in elderly patients: a retrospective cohort study. J Orthop Surg Res 2018;13:252. pmid:30314520
- 7. Galbusera F, Volkheimer D, Reitmaier S, Berger-Roscher N, Kienle A, Wilke HJ. Pedicle screw loosening: a clinically relevant complication? Eur Spine J 2015;24:1005–16. pmid:25616349
- 8. Anderson PA, Kadri A, Hare KJ, Binkley N. Preoperative bone health assessment and optimization in spine surgery. Neurosurg Focus 2020;49:E2. pmid:32738805
- 9. Chin DK, Park JY, Yoon YS et al. Prevalence of osteoporosis in patients requiring spine surgery: incidence and significance of osteoporosis in spine disease. Osteoporos Int 2007;18:1219–24. pmid:17387420
- 10. Guo HZ, Guo DQ, Tang YC, Liang D, Zhang SC. Selective cement augmentation of cranial and caudal pedicle screws provides comparable stability to augmentation on all segments in the osteoporotic spine: a finite element analysis. Ann Transl Med 2020;8:1384. pmid:33313129
- 11. Tang YC, Guo HZ, Guo DQ et al. Effect and potential risks of using multilevel cement-augmented pedicle screw fixation in osteoporotic spine with lumbar degenerative disease. BMC Musculoskelet Disord 2020;21:274. pmid:32345282
- 12. Ohtori S, Inoue G, Orita S et al. Comparison of teriparatide and bisphosphonate treatment to reduce pedicle screw loosening after lumbar spinal fusion surgery in postmenopausal women with osteoporosis from a bone quality perspective. Spine (Phila Pa 1976) 2013;38:E487–92. pmid:23354115
- 13. Dipaola CP, Bible JE, Biswas D, Dipaola M, Grauer JN, Rechtine GR. Survey of spine surgeons on attitudes regarding osteoporosis and osteomalacia screening and treatment for fractures, fusion surgery, and pseudoarthrosis. Spine J 2009;9:537–44. pmid:19328744
- 14. Allen RT, Lee YP, Garfin SR. Spine surgeons survey on attitudes regarding osteoporosis and osteomalacia screening and treatment for fractures, fusion surgery, and pseudoarthrosis. Spine J 2009;9:602–4. pmid:19560054
- 15. Anderson PA, Morgan SL, Krueger D et al. Use of Bone Health Evaluation in Orthopedic Surgery: 2019 ISCD Official Position. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 2019;22:517–543. pmid:31519473
- 16. Kuprys TK, Steinmetz LM, Fischer CR et al. Preoperative Assessment of Bone Quality in Spine Deformity Surgery: Correlation With Clinical Practice and Published Recommendations. Spine (Phila Pa 1976) 2019;44:E735–e741. pmid:30540720
- 17. Bergh C, Söderpalm AC, Brisby H. Preoperative dual-energy X-ray absorptiometry and FRAX in patients with lumbar spinal stenosis. J Orthop Surg Res 2018;13:253. pmid:30326950
- 18. Zou D, Jiang S, Zhou S et al. Prevalence of Osteoporosis in Patients Undergoing Lumbar Fusion for Lumbar Degenerative Diseases: A Combination of DXA and Hounsfield Units. Spine (Phila Pa 1976) 2020;45:E406–e410. pmid:31725127
- 19. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ (Clinical research ed) 2009;339:b2535. pmid:19622551
- 20. Hoy D, Brooks P, Woolf A et al. Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol 2012;65:934–9. pmid:22742910
- 21. Paz RD, Henríquez MS, Melián KA, Martin CB. Prevalence of Poor Bone Quality in Patients Undergoing Spine Surgery: A Comprehensive Approach. Global Spine J 2022;12:1412–1419. pmid:33487013
- 22. Schmidt T, Ebert K, Rolvien T et al. A retrospective analysis of bone mineral status in patients requiring spinal surgery. BMC Musculoskelet Disord 2018;19:53. pmid:29439698
- 23. Banse C, Ould-Slimane M, Foulongne E et al. Impact of assessment of bone status before corrective surgery of lumbar spine in patients over 50 years old. Open Access Rheumatol 2019;11:111–115. pmid:31123425
- 24. Mo X, Zhao S, Wen Z et al. High prevalence of osteoporosis in patients undergoing spine surgery in China. BMC Geriatr 2021;21:361. pmid:34120598
- 25. Dave D, Bhattacharjee SK, Shah DD et al. Osteoporosis in Indian Patients Undergoing Elective Arthroplasty and Spinal Procedures: An Observational Study. Cureus 2022;14:e27275. pmid:35910701
- 26. St Jeor JD, Jackson TJ, Xiong AE et al. Osteoporosis in spine surgery patients: what is the best way to diagnose osteoporosis in this population? Neurosurg Focus 2020;49:E4. pmid:32738802
- 27. Wang L, Yu W, Yin X et al. Prevalence of Osteoporosis and Fracture in China: The China Osteoporosis Prevalence Study. JAMA Netw Open 2021;4:e2121106. pmid:34398202
- 28. Pappou IP, Girardi FP, Sandhu HS et al. Discordantly high spinal bone mineral density values in patients with adult lumbar scoliosis. Spine (Phila Pa 1976) 2006;31:1614–20. pmid:16778698
- 29. Aebi M. The adult scoliosis. Eur Spine J 2005;14:925–48. pmid:16328223
- 30. Tang YJ, Sheu WH, Liu PH, Lee WJ, Chen YT. Positive associations of bone mineral density with body mass index, physical activity, and blood triglyceride level in men over 70 years old: a TCVGHAGE study. J Bone Miner Metab 2007;25:54–9. pmid:17187194
- 31. Silva FE, Lenke LG. Adult degenerative scoliosis: evaluation and management. Neurosurg Focus 2010;28:E1. pmid:20192655
- 32. Kim HJ, Lee HM, Kim HS et al. Bone metabolism in postmenopausal women with lumbar spinal stenosis: analysis of bone mineral density and bone turnover markers. Spine (Phila Pa 1976) 2008;33:2435–9. pmid:18923320
- 33. Park HY, Ha JY, Kim KW, Baek IH, Park SB, Lee JS. Effect of lumbar spinal stenosis on bone mineral density in osteoporosis patients treated with ibandronate. BMC Musculoskelet Disord 2021;22:412. pmid:33947363
- 34. Anand A, Shetty AP, Renjith KR, K SS, Kanna RM, Rajasekaran S. Does Sarcopenia Increase the Risk for Fresh Vertebral Fragility Fractures?: A Case-Control Study. Asian Spine J 2020;14:17–24. pmid:31575110
- 35. Horowitz JA, Puvanesarajah V, Jain A et al. Fragility Fracture Risk in Elderly Patients With Cervical Myelopathy. Spine (Phila Pa 1976) 2019;44:96–102. pmid:29939973
- 36. Schneider DL, von Mühlen D, Barrett-Connor E, Sartoris DJ. Kyphosis does not equal vertebral fractures: the Rancho Bernardo study. J Rheumatol 2004;31:747–52 pmid:15088302
- 37. Ettinger B, Black DM, Palermo L, Nevitt MC, Melnikoff S, Cummings SR. Kyphosis in older women and its relation to back pain, disability and osteopenia: the study of osteoporotic fractures. Osteoporos Int 1994;4:55–60. pmid:8148573
- 38. Routh RH, Rumancik S, Pathak RD, Burshell AL, Nauman EA. The relationship between bone mineral density and biomechanics in patients with osteoporosis and scoliosis. Osteoporos Int 2005;16:1857–63. pmid:15999291
- 39. Chen P, Li Z, Hu Y. Prevalence of osteoporosis in China: a meta-analysis and systematic review. BMC Public Health 2016;16:1039. pmid:27716144
- 40. Gur A, Nas K, Cevik R, Sarac AJ, Ataoglu S, Karakoc M. Influence of number of pregnancies on bone mineral density in postmenopausal women of different age groups. J Bone Miner Metab 2003;21:234–41. pmid:12811629
- 41. Hajian-Tilaki KO, Heidari B. Prevalence of obesity, central obesity and the associated factors in urban population aged 20–70 years, in the north of Iran: a population-based study and regression approach. Obesity reviews: an official journal of the International Association for the Study of Obesity 2007;8:3–10. pmid:17212790
- 42. Hajian-Tilaki K, Heidari B, Firouzjahi A, Bagherzadeh M, Hajian-Tilaki A, Halalkhor S. Prevalence of metabolic syndrome and the association with socio-demographic characteristics and physical activity in urban population of Iranian adults: a population-based study. Diabetes & metabolic syndrome 2014;8:170–6. pmid:25220921
- 43. Roy D, Swarbrick C, King Y et al. Differences in peak bone mass in women of European and South Asian origin can be explained by differences in body size. Osteoporos Int 2005;16:1254–62. pmid:15702264
- 44. Bhudhikanok GS, Wang MC, Eckert K, Matkin C, Marcus R, Bachrach LK. Differences in bone mineral in young Asian and Caucasian Americans may reflect differences in bone size. J Bone Miner Res 1996;11:1545–56. pmid:8889856
- 45. Russell LA. Osteoporosis and orthopedic surgery: effect of bone health on total joint arthroplasty outcome. Curr Rheumatol Rep 2013;15:371. pmid:24085661
- 46. Xiao PL, Hsu CJ, Ma YG et al. Prevalence and treatment rate of osteoporosis in patients undergoing total knee and hip arthroplasty: a systematic review and meta-analysis. Arch Osteoporos 2022;17:16. pmid:35029750
- 47. Bernatz JT, Brooks AE, Squire MW, Illgen RI, 2nd, Binkley NC, Anderson PA. Osteoporosis Is Common and Undertreated Prior to Total Joint Arthroplasty. J Arthroplasty 2019;34:1347–1353. pmid:30992237
- 48. Ponnusamy KE, Iyer S, Gupta G, Khanna AJ. Instrumentation of the osteoporotic spine: biomechanical and clinical considerations. Spine J 2011;11:54–63. pmid:21168099
- 49. DeWald CJ, Stanley T. Instrumentation-related complications of multilevel fusions for adult spinal deformity patients over age 65: surgical considerations and treatment options in patients with poor bone quality. Spine (Phila Pa 1976) 2006;31:S144–51. pmid:16946632
- 50. Guzman JZ, Feldman ZM, McAnany S, Hecht AC, Qureshi SA, Cho SK. Osteoporosis in Cervical Spine Surgery. Spine (Phila Pa 1976) 2016;41:662–8. pmid:26656054
- 51. Hirsch BP, Unnanuntana A, Cunningham ME, Lane JM. The effect of therapies for osteoporosis on spine fusion: a systematic review. Spine J 2013;13:190–9. pmid:22658879
- 52. Nagahama K, Kanayama M, Togawa D, Hashimoto T, Minami A. Does alendronate disturb the healing process of posterior lumbar interbody fusion? A prospective randomized trial. J Neurosurg Spine 2011;14:500–7. pmid:21275549
- 53. Mu S, Wang J, Gong S. Application of Medical Imaging Based on Deep Learning in the Treatment of Lumbar Degenerative Diseases and Osteoporosis with Bone Cement Screws. Comput Math Methods Med 2021;2021:2638495. pmid:34671416
- 54. Sardar ZM, Coury JR, Cerpa M et al. Best Practice Guidelines for Assessment and Management of Osteoporosis in Adult Patients Undergoing Elective Spinal Reconstruction. Spine (Phila Pa 1976) 2022;47:128–135. pmid:34690329
- 55. Díaz-Romero Paz R, Sosa Henríquez M, Armas Melián K, Coloma Valverde G. Trends and attitudes of spine surgeons regarding osteoporosis. Neurocirugia (Astur: Engl Ed) 2019;30:268–277. pmid:31175021
- 56. Zou D, Li W, Deng C, Du G, Xu N. The use of CT Hounsfield unit values to identify the undiagnosed spinal osteoporosis in patients with lumbar degenerative diseases. Eur Spine J 2019;28:1758–1766. pmid:30306332
- 57. Lee SJ, Binkley N, Lubner MG, Bruce RJ, Ziemlewicz TJ, Pickhardt PJ. Opportunistic screening for osteoporosis using the sagittal reconstruction from routine abdominal CT for combined assessment of vertebral fractures and density. Osteoporos Int 2016;27:1131–1136. pmid:26419470
- 58. McNabb-Baltar J, Manickavasagan HR, Conwell DL et al. A Pilot Study to Assess Opportunistic Use of CT-Scan for Osteoporosis Screening in Chronic Pancreatitis. Front Physiol 2022;13:866945. pmid:35721529
- 59. Löffler MT, Jacob A, Scharr A et al. Automatic opportunistic osteoporosis screening in routine CT: improved prediction of patients with prevalent vertebral fractures compared to DXA. Eur Radiol 2021;31:6069–6077. pmid:33507353
- 60. Mikula AL, Lakomkin N, Pennington Z et al. Association between lower Hounsfield units and proximal junctional kyphosis and failure at the upper thoracic spine. J Neurosurg Spine 2022:1–9. pmid:35561697
- 61. Melton LJ 3rd, Looker AC, Shepherd JA et al. Osteoporosis assessment by whole body region vs. site-specific DXA. Osteoporos Int 2005;16:1558–64. pmid:15812599