Exploring the interplay between paraspinal muscular status and bone health in osteoporosis and fracture risk: a comprehensive literature review on computed tomography (CT) and magnetic resonance imaging (MRI) studies

Introduction

Osteoporosis (OP) is a systemic skeletal disease which represents a major public health issue in aging societies. It is characterized by low bone mineral density (BMD) and degradation of bone microstructure, leading to a reduction of bone strength and, consequently, an increased susceptibility to fractures (1-4). BMD is influenced by genetic factors such as endocrine parameters, body fat content, lean body mass and muscle strength (5,6). It is also correlated with correctable factors like body fat content, lean body weight and muscle power (7,8).

Indeed, OP is a multifactorial disorder is driven by an imbalance in bone remodeling due to various factors: hormonal shifts (e.g., estrogen, testosterone), nutritional deficiencies (e.g., calcium, vitamin D), medical conditions (e.g., inflammatory, kidney disease), and lifestyle (e.g., inactivity, smoking, alcohol) (1-8). Understanding this complex pathogenesis is critical for developing therapies and preventative strategies to combat the significant healthcare burden associated with OP (1-8).

Recently, studies have shown that bone and skeletal muscle, considered as common functional units, have a role in the pathological process that leads to OP (9,10). More specifically, sarcopenia, defined by the European Working Group on Sarcopenia in Older People as a reduction of muscle strength accompanied by low muscle mass and quality (11), has been shown to be related with low BMD and OP (12-14). With aging, the musculoskeletal system degenerates leading to a reduction of function and strength (15). The decline of muscle strength is associated with structural changes such as atrophy and fat infiltration, the latter being the main factor involved; these modifications can be observed as a decrease in muscle volume (or cross-sectional area, CSA) and an increase in muscle fat fraction (FF) (16,17). At the same time, muscle weakness increases the risk of falls, playing an important role in the occurrence of fractures, especially in patients affected by OP who have an intrinsic increased risk of developing fractures (18,19). Osteoporotic vertebral fractures (OVF) have a significant impact on the health status of elderly people and can result in a decline in the patients’ quality of life and survival rate (20,21).

Paraspinal muscle, or paravertebral muscles, especially the multifidus, erector spinae, and psoas, are a group of skeletal muscles located in both sides of the spine and have an important role on spinal stability and function (22,23). It has also been demonstrated their relationship with low back pain, sagittal balance, and quality of life (24-26). Density, atrophy, and fatty degeneration of the paraspinal muscles can be evaluated using imaging technics like computed tomography (CT) and magnetic resonance imaging (MRI) (27-29).

In the last two decades, several studies have put a focus on the morphology of paraspinal muscles with different disorders, especially low back pain and spinal disorders. A significant number of studies have also described the relationship between paraspinal muscles and BMD/OP and between paraspinal muscles and OVF. The conclusions of studies regarding these correlations needs to be summarized. Therefore, we have reviewed the scientific literature about the role of morphological characteristics of paraspinal muscles in (I) BMD and OP and (II) OVF. We present this article in accordance with the Narrative Review reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-23-1770/rc).

Methods

The literature research was carried out on September 2023 using PubMed, Scopus, and Cochrane databases. Only articles written in English and published after January 1 of 2000 were included. The keywords used for the articles search were: paraspinal muscle OR psoas OR multifidus AND (osteoporosis OR bone density OR fracture) (Table 1). The titles of all the articles of potential interest to our topic were screened and we identified 31 papers of interest. We proceeded the screening by reading all the articles abstracts. The exclusion criteria were the following: (I) review articles, case reports articles, animal studies; (II) studies comparing paraspinal muscles characteristics in other diseases such as low back pain, lumbar spinal stenosis, lumbar disc herniation or degeneration; (III) studies in which the muscles characteristics were analyzed thanks to other imaging modalities (ultrasound or dual energy X-ray absorptiometry). We included in this manuscript the articles investigating BMD, OP, and fractures together with paraspinal muscles morphology, studied thanks to CT or MRI.

Results

After screening titles and abstracts, 28 articles were selected for this study (Figure 1). The studies included in this review analyzed the paraspinal muscle degeneration in the lumbar spine using CT or MRI as imaging modalities. More specifically, the parameters considered were fatty infiltration, cross sectional area, muscle area, muscle index, percentage of muscle fibre, the two formers being the most commonly observed. The studies investigated the possible correlation between paraspinal muscle degeneration and osteopenia/OP and fractures in patients that underwent or not surgical procedures. We divided the studies into two categories, identifying 13 studies about osteopenia/OP and 15 studies about fractures.

Figure 1 Flowchart diagram showing the articles selection process.

Discussion

The degeneration of the paraspinal musculature has become an important topic of interest in recent years. Many authors have studied the changes regarding these muscles in the general population, trying to find a correlation with clinical data. Some authors found that paraspinal muscles undergo degenerative changes, such as atrophy and fat infiltration, with physiologic ageing (30). Other studies have reported a correlation between paraspinal muscle degeneration and parameters like sex and body mass index (BMI); for example, it has been demonstrated a larger paraspinal muscles FF signal in females compared to males (31), while other authors have found a positive correlation between weight and muscle area (32). A correlation, linking the level of physical activity, fatty infiltration, and asymmetry of the paraspinal musculature was also demonstrated in another study (32). In the last two decades many studies have put a focus on the possible link between the morphology of paraspinal musculature and various conditions. Many authors studied the morphology of these muscle in patients presenting with low back pain and found atrophy and fatty infiltration to be very common, therefore recognizing the role of paraspinal musculature degeneration in low back pain (33,34). Other studies have oriented their research on the correlation between paraspinal muscles degeneration and spinal diseases, such as spinal stenosis and reported similar results (35,36). More recently it has been developed an interest on the possible role of these muscles in the pathology of OP and fractures, being two important and widespread conditions of the ageing society. Interesting results have emerged, and we have summarized them dividing the two topics of interest.

Paraspinal muscles and osteopenia/OP

In recent years, several research studies investigated the correlation between the morphology of paraspinal muscles and BMD or OP (Figure 2). The major characteristics of these studies are summarized in Table 2.

Figure 2 Association between osteoporosis and muscle atrophy. Dual-energy X-ray absorptiometry (A) and sagittal T2-weighed MRI (B) of a 79-year-old woman. The images show the association of osteoporosis (A) with fatty degeneration of paraspinal muscles [arrow in (B)]. BMD, bone mineral density; BMC, bone mineral content; AM, age-related; CV, coefficient of variation; ACF, autocorrelation function; BCF, bias correction factor; TH, total hip; CHI, classification.

One of the first studies that found a correlation between the cited parameters was conducted by Lee et al. (37). They showed a statistically significant correlation between paraspinal muscle area and lumbar BMD, but no significant correlation was found with psoas muscle area.

Ekin et al. (38) demonstrated that psoas and paraspinal muscle atrophy was 5.7 times more frequent in patients that showed a reduction of BMD; these results were significantly observed more frequently in women.

Zhao et al. (39) were the first study group that used the combination of chemical shift encoding-based water-fat MRI to investigate paraspinal muscle fat infiltration and quantitative CT (QCT) to measure lumbar BMD. A moderate inverse correlation between paraspinal muscle proton density fat fraction (PDFF) and lumbar QCT-BMD was found after controlling for age, sex, and BMI. They evaluated the fatty infiltration of erector spinae, multifidus, and psoas independently, and demonstrated that all these paraspinal muscles fatty infiltration had an inverse correlation with lumbar BMD.

Sollman et al. (40) have highlighted differences between males and females, the former showing significantly higher lumbar BMD, psoas and erector spinae muscle CSA and CSA ratio (CSAR) at L2 and L4/L5 levels. After adjusting for age, BMD and CSAR were significantly correlated al level L4/L5 as well as muscle attenuation and CSAR, however, there was no correlation between BMD and muscle attenuation with CSAR at level L2. No correlations with vertebral fractures were found other than with BMD. These results indicates that paraspinal muscle CSA and BMD are correlated at L4/L5 level.

Kajiki et al. (41) demonstrated a significant association between psoas muscle index (MI) and BMD at the lumbar spine and femoral neck level; they also observed that psoas MI was lower in patients suffering from OP and it was also correlated with fracture risk measured by Fracture Risk Assessment Tool (FRAX). According to ROC analysis, psoas MI had moderate accuracy in the diagnosis of OP and FRAX.

Gassert et al. (42) conducted a study with the aim of assessing longitudinal changes in PDFF, T2* and CSA of the paraspinal musculature over 6 months of time in patients with or without osteopenia/OP. They showed that paraspinal muscles CSA decreased more significantly over 6 months in patients with osteopenia/OP compared to those without. Additionally, greater vertebral PDFF and paraspinal muscles PDFF at baseline were associated with greater bone fragility. Because of these results, the study group suggests that longitudinal PDFF and T2* mapping may be useful tools for the assessment and prediction of muscle and bone health, especially in patients suffering from osteopenia/OP.

Gurusamy et al. (43), observed that greater psoas, paraspinal and oblique muscle density was significantly associated with higher lumbar BMD at L3 level in both men and women; at the same time, higher muscle FF was associated with lower L3-BMD.

Han et al. (44) reported that patients with OP showed lower BMI and higher multifidus and erector spinae muscle fatty infiltration at L4/L5 level compared to patients with normal BMD; both multifidus and erector spinae muscle fatty infiltration were significantly correlated with lumbar T-score and minimum T-score.

Huang et al. (45) found a close correlation between psoas muscle index and BMD in the femoral neck and lumbar spine; a strong association was also found with the FRAX. This study group demonstrated that L3-based muscle index could be a useful tool in the diagnosis of OP, and that psoas muscle index is a better indicator of OP compared to skeletal muscle index. They also demonstrated that both visceral and subcutaneous fatty infiltration and visceral-to-subcutaneous ratio of the fat area do not help in OP diagnosis.

Yang et al. (46) reported that fatty infiltration of paraspinal muscles, especially multifidus and erector spinae muscle, increases with both age and declining lumbar spine MBD in both sexes. They also demonstrated that paraspinal muscles CSA is not correlated with either age or BMD at any region; this result contradicts with other studies, such as the previously mentioned by Sollman et al. (40), where CSA was found to be associated with lumbar BMD.

Zhang et al. (47), in their postmenopausal women-based study, showed that a decrease in height, weight, BMI, bilateral psoas area and muscle index were associated with OP. They also observed that psoas muscle index of non-osteoporotic patients with vertebral fractures was lower compared to non-osteoporotic patients with non-vertebral fractures; they did not find a significant difference regarding psoas muscle index in osteoporotic patients with or without vertebral fractures. The study group suggests that sarcopenia may be a risk factor for non-OVF.

Zhou et al. (48) demonstrated that fatty infiltration of paraspinal muscles, specifically erector spinae, multifidus, and psoas muscle, measured using dual energy CT (DECT) had a negative correlation with lumbar BMD after controlling for age, sex, and BMI. Erector spinae and multifidus muscle fat content was found to have a stronger correlation with lumbar BMD compared to psoas fatty infiltration.

Liu et al. (49) also conducted a study using DECT to evaluate the fatty infiltration of erector spinae and psoas muscles. They showed that lumbar BMD is significantly correlated with CSA and fatty infiltration of paraspinal muscles, therefore these parameters have a role in the progression of OP.

Research studies have explored the relationship between paraspinal muscle morphology and bone BMD or OP. Findings include significant correlations between lumbar BMD and paraspinal muscle area, with variations between muscle types, gender differences in muscle characteristics, and associations between muscle indices and BMD or fracture risk. Additionally, studies using imaging techniques like MRI and CT reveal correlations between fatty infiltration of paraspinal muscles and lumbar BMD, suggesting potential implications for OP assessment and prediction.

Paraspinal muscles and fractures

Over the last few years, several studies focused on the correlation linking paraspinal muscles degeneration and fractures in patients with or without OP (Figure 3). The major characteristics of these studies are summarized in Table 3.

Figure 3 Association between osteoporosis and vertebral fracture. Sagittal T1-weighted (A), sagittal T2-weighted (B) with fat suppression, and axial T2-weighted MRI (C) of a 75-year-old woman. Non-recent vertebral osteoporotic fracture at L3 [star in (A) and (B)] is detected together with fatty degeneration of paraspinal muscles [arrows in (A), (B) and (C)].

The first study regarding this matter is the one conducted by Kim et al. (50) in postmenopausal women. They demonstrated that the mean CSA of erector spinae, psoas and paraspinal muscles were smaller in patients with osteoporotic vertebral compression fractures (OVCF) compared to patients without fractures, however multifidus muscle CSA was not significantly smaller in the former group. In addition, more severe grades of muscle fatty infiltration were more common in patients with OVCF.

Byun et al. (51) based their study on a population of patients with hip fracture and showed that lower psoas CSA was correlated with a higher 1-year mortality risk. They also showed that psoas CSA had a moderate association with appendicular lean mass in both genders.

Huang et al. (52) reported that a decrease in psoas muscle mass was more common in patients with OVCF when compared to age-matched osteoporotic controls, but no significant correlation was found with increased psoas fatty infiltration.

Similar to Byun et al. (51), Touban et al. (53) studied the possible correlation between psoas muscle morphology and the survival rate in orthopedic trauma patients; they showed that male patients presenting with higher psoas CSA had a decreased 1-year all-cause mortality risk, but they were not able to find a significant correlation in female patients.

Takahashi et al. (54) analyzed the changes in paraspinal muscles after OVF; they observed a progressive increase in the fatty infiltration, but not in the muscle CSA. The study group also observed a delayed union after OVF in patients with an increased paraspinal FF.

Sim et al. (55) evaluated the association between preoperative psoas-to-lumbar index (PLVI), used to estimate sarcopenia, and mortality in elderly patients who underwent hip fracture surgery; they reported an increased 1-year and overall mortality in patients with low PLVI, therefore in patients with a reduced psoas muscle mass and sarcopenia.

Habibi et al. (56) observed that patients with an increased fatty infiltration of the paraspinal musculature had a much higher persistence of low back pain after OVF and a higher risk of new OVF in the thoracolumbar region. They did not find a significant correlation between paraspinal musculature and severe compression fracture or delayed union. No significant correlation was found regarding psoas CSA because CSA is not likely to reflect early muscle changes compared with the fatty infiltration; this result is consistent with other studies like the one by Takahashi et al. (54).

Kawakami et al. (57) studied patients with intertrochanteric fracture and demonstrated that patients with a decreased psoas muscle area had a significantly higher risk of developing a contralateral femoral fracture in the two years following the initial fracture.

Zhao et al. (58) analyzed patients who underwent percutaneous kyphoplasty after OVF and observed that patients who sustained new vertebral fractures after the surgery had a decreased paraspinal muscle CSA.

Si et al. (59) conduced a similar study on patients after percutaneous kyphoplasty and observed that multifidus, psoas, and erector spinae muscles fatty infiltration was correlated with the occurrence of new OVCF after undergoing the procedure. They also observed that the CSA difference index between multifidus muscle and psoas muscle represented a risk factor for the recurrence of OVCF.

Okuwaki et al. (60) reported that erector spinae CSA was correlated with vertebral instability in patients with OVCF, therefore with the severity of the OVCF; this was not valid for the CSA of multifidus and psoas muscles, which were reported to be correlated to BMD only.

Shah et al. (61) revealed a statistically significant correlation between vertebral insufficiency fractures in the elderly and the reduction of CSA in the psoas and multifidus muscles. They also observed a reduction in the multifidus to psoas muscle CSA ratio depending on the number of fractures.

Backhauß et al. (62) reported that fatty infiltration of the autochthonous muscle, especially the erector spinae muscle, is associated with non-traumatic vertebral body fractures in the lower thoracic spine and their severity; no significant association was found in the lumbar spine.

Huang et al. (63) demonstrated that a higher degree of fatty in filtration in the paraspinal muscles was related to the severity of OVCF in postmenopausal women.

Lee et al. (64) showed a significant association between multifidus muscle percentage of muscle fibre and OVF al L4/L5–L5/S1, but not with multifidus muscle CSA which appeared to be higher in the fracture group when compared to the control group. According to this study group the fatty infiltration of the paraspinal muscle, rather than the muscle CSA, significantly affect the risk of OVF.

Studies on postmenopausal women indicate a correlation between smaller erector spinae, psoas, and paraspinal muscle CSA and OVCF. Additionally, associations are found between lower psoas CSA and higher 1-year mortality risk in hip fracture patients. Other investigations highlight the impact of psoas muscle morphology on survival rates, increased fatty infiltration after OVF, and the role of paraspinal muscle CSA in predicting new vertebral fractures. Findings underscore the significance of muscle characteristics in assessing fracture risk and outcomes in OP-related conditions.

Conclusions

This paper provides an overview of the changes observed in the paraspinal musculature in patients with osteopenia/OP and fractures. The current evidence suggests that paraspinal muscle degeneration, intended as atrophy and fatty infiltration of the muscles, plays an important role in the occurrence of osteopenia/OP and fractures. Assessing the paraspinal musculature may be a useful tool in the identification of patients that may be at high-risk for these conditions, therefore it can be useful to prevent a worsening of the quality of life of these patients. Further studies are needed to understand the possible role of paraspinal musculature in the prevention of OP and fractures.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-23-1770/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-23-1770/coif). C.A.M. serves as an unpaid editorial board member of Quantitative Imaging in Medicine and Surgery. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

References

1. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA 2001;285:785-95.
2. Expert Panel on Musculoskeletal Imaging. Ward RJ, Roberts CC, Bencardino JT, Arnold E, Baccei SJ, Cassidy RC, Chang EY, Fox MG, Greenspan BS, Gyftopoulos S, Hochman MG, Mintz DN, Newman JS, Reitman C, Rosenberg ZS, Shah NA, Small KM, Weissman BN. ACR Appropriateness Criteria® Osteoporosis and Bone Mineral Density. J Am Coll Radiol 2017;14:S189-S202.
3. Kazakia GJ, Carballido-Gamio J, Lai A, Nardo L, Facchetti L, Pasco C, Zhang CA, Han M, Parrott AH, Tien P, Krug R. Trabecular bone microstructure is impaired in the proximal femur of human immunodeficiency virus-infected men with normal bone mineral density. Quant Imaging Med Surg 2018;8:5-13. [Crossref] [PubMed]
4. Cheng X, Yuan H, Cheng J, Weng X, Xu H, Gao J, Huang M, Wáng YXJ, Wu Y, Xu W, Liu L, Liu H, Huang C, Jin Z, Tian WBone and Joint Group of Chinese Society of Radiology, Chinese Medical Association (CMA), Musculoskeletal Radiology Society of Chinese Medical Doctors Association, Osteoporosis Group of Chinese Orthopedic Association, Bone Density Group of Chinese Society of Imaging Technology, CMA. Chinese expert consensus on the diagnosis of osteoporosis by imaging and bone mineral density. Quant Imaging Med Surg 2020;10:2066-77. [Crossref] [PubMed]
5. Seeman E, Hopper JL, Young NR, Formica C, Goss P, Tsalamandris C. Do genetic factors explain associations between muscle strength, lean mass, and bone density? A twin study. Am J Physiol 1996;270:E320-7. [PubMed]
6. Nguyen TV, Howard GM, Kelly PJ, Eisman JA. Bone mass, lean mass, and fat mass: same genes or same environments? Am J Epidemiol 1998;147:3-16. [Crossref] [PubMed]
7. Ramírez-Villada JF, León-Ariza HH, Argüello-Gutiérrez YP, Porras-Ramírez KA. Effect of high impact movements on body composition, strength and bone mineral density on women over 60 years. Rev Esp Geriatr Gerontol 2016;51:68-74. [PubMed]
8. Kim JY, Kim HJ, Hong JY, Park DH, Kim CS. Characteristics of nutrient intakes, basal physical fitness and serum markers in elderly women with osteopenia. J Exerc Nutrition Biochem 2015;19:217-24. [Crossref] [PubMed]
9. Ma HT, Griffith JF, Xu L, Leung PC. The functional muscle-bone unit in subjects of varying BMD. Osteoporos Int 2014;25:999-1004. [Crossref] [PubMed]
10. Grote C, Reinhardt D, Zhang M, Wang J. Regulatory mechanisms and clinical manifestations of musculoskeletal aging. J Orthop Res 2019;37:1475-88. [Crossref] [PubMed]
11. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, Cooper C, Landi F, Rolland Y, Sayer AA, Schneider SM, Sieber CC, Topinkova E, Vandewoude M, Visser M, Zamboni M. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019;48:16-31. [Crossref] [PubMed]
12. He H, Liu Y, Tian Q, Papasian CJ, Hu T, Deng HW. Relationship of sarcopenia and body composition with osteoporosis. Osteoporos Int 2016;27:473-82. [Crossref] [PubMed]
13. Guerri S, Mercatelli D, Aparisi Gómez MP, Napoli A, Battista G, Guglielmi G, Bazzocchi A. Quantitative imaging techniques for the assessment of osteoporosis and sarcopenia. Quant Imaging Med Surg 2018;8:60-85. [Crossref] [PubMed]
14. Messina C, Maffi G, Vitale JA, Ulivieri FM, Guglielmi G, Sconfienza LM. Diagnostic imaging of osteoporosis and sarcopenia: a narrative review. Quant Imaging Med Surg 2018;8:86-99. Erratum in: Quant Imaging Med Surg 2018;8:372. [Crossref] [PubMed]
15. Mallio CA, Vadalà G, Russo F, Bernetti C, Ambrosio L, Zobel BB, Quattrocchi CC, Papalia R, Denaro V. Novel Magnetic Resonance Imaging Tools for the Diagnosis of Degenerative Disc Disease: A Narrative Review. Diagnostics (Basel) 2022;12:420. [Crossref] [PubMed]
16. Beasley LE, Koster A, Newman AB, Javaid MK, Ferrucci L, Kritchevsky SB, Kuller LH, Pahor M, Schaap LA, Visser M, Rubin SM, Goodpaster BH, Harris TB. Health ABC study. Inflammation and race and gender differences in computerized tomography-measured adipose depots. Obesity (Silver Spring) 2009;17:1062-9. [Crossref] [PubMed]
17. Engelke K, Museyko O, Wang L, Laredo JD. Quantitative analysis of skeletal muscle by computed tomography imaging-State of the art. J Orthop Translat 2018;15:91-103. [Crossref] [PubMed]
18. Wáng YXJ. A modified semi-quantitative (mSQ) grading scheme for osteoporotic vertebral fracture in elderly women. Quant Imaging Med Surg 2019;9:146-50. [Crossref] [PubMed]
19. Wáng YXJ, Che-Nordin N. Some radiographically 'occult' osteoporotic vertebral fractures can be evidential if we look carefully. Quant Imaging Med Surg 2019;9:1992-5. [Crossref] [PubMed]
20. Cooper C, Atkinson EJ, Jacobsen SJ, O'Fallon WM, Melton LJ 3rd. Population-based study of survival after osteoporotic fractures. Am J Epidemiol 1993;137:1001-5. [Crossref] [PubMed]
21. Tosteson AN, Gabriel SE, Grove MR, Moncur MM, Kneeland TS, Melton LJ 3rd. Impact of hip and vertebral fractures on quality-adjusted life years. Osteoporos Int 2001;12:1042-9. [Crossref] [PubMed]
22. Hodges PW, Danneels L. Changes in Structure and Function of the Back Muscles in Low Back Pain: Different Time Points, Observations, and Mechanisms. J Orthop Sports Phys Ther 2019;49:464-76. [Crossref] [PubMed]
23. Mallio CA, Zobel BB, Quattrocchi CC. Evaluating rehabilitation interventions in Parkinson's disease with functional MRI: a promising neuroprotective strategy. Neural Regen Res 2015;10:702-3. [Crossref] [PubMed]
24. Hori Y, Hoshino M, Inage K, Miyagi M, Takahashi S, Ohyama S, et al. ISSLS PRIZE IN CLINICAL SCIENCE 2019: clinical importance of trunk muscle mass for low back pain, spinal balance, and quality of life-a multicenter cross-sectional study. Eur Spine J 2019;28:914-21. [Crossref] [PubMed]
25. Wojdasiewicz P, Poniatowski ŁA, Kotela A, Skoda M, Pyzlak M, Stangret A, Kotela I, Szukiewicz D. Comparative Analysis of the Occurrence and Role of CX3CL1 (Fractalkine) and Its Receptor CX3CR1 in Hemophilic Arthropathy and Osteoarthritis. J Immunol Res 2020;2020:2932696. [PubMed]
26. Kubaszewski Ł, Wojdasiewicz P, Rożek M, Słowińska IE, Romanowska-Próchnicka K, Słowiński R, Poniatowski ŁA, Gasik R. Syndromes with chronic non-bacterial osteomyelitis in the spine. Reumatologia 2015;53:328-36. [Crossref] [PubMed]
27. Mallio CA, Greco F, Gaudino F, Beomonte Zobel B, Quattrocchi CC. Computed tomography density changes of bone metastases after concomitant denosumab. Skeletal Radiol 2023;52:1567-75. [Crossref] [PubMed]
28. Mallio CA, Bernetti C, Agostini F, Mangone M, Paoloni M, Santilli G, Martina FM, Quattrocchi CC, Zobel BB, Bernetti A, Advanced MR. Imaging for Knee Osteoarthritis: A Review on Local and Brain Effects. Diagnostics (Basel) 2022;13:54. [Crossref] [PubMed]
29. Greco F, Panunzio A, Tafuri A, Bernetti C, Pagliarulo V, Zobel BB, Scardapane A, Mallio CA. CT-Based Radiogenomics of P4HA3 Expression in Clear Cell Renal Cell Carcinoma. Acad Radiol 2024;31:902-8. [Crossref] [PubMed]
30. Dallaway A, Kite C, Griffen C, Duncan M, Tallis J, Renshaw D, Hattersley J. Age-related degeneration of the lumbar paravertebral muscles: Systematic review and three-level meta-regression. Exp Gerontol 2020;133:110856. [Crossref] [PubMed]
31. Urrutia J, Besa P, Lobos D, Campos M, Arrieta C, Andia M, Uribe S. Lumbar paraspinal muscle fat infiltration is independently associated with sex, age, and inter-vertebral disc degeneration in symptomatic patients. Skeletal Radiol 2018;47:955-61. [Crossref] [PubMed]
32. Fortin M, Yuan Y, Battié MC. Factors Associated With Paraspinal Muscle Asymmetry in Size and Composition in a General Population Sample of Men. 2013. Phys Ther 2013;93:1540-50. [Crossref] [PubMed]
33. Seyedhoseinpoor T, Taghipour M, Dadgoo M, Sanjari MA, Takamjani IE, Kazemnejad A, Khoshamooz Y, Hides J. Alteration of lumbar muscle morphology and composition in relation to low back pain: a systematic review and meta-analysis. Spine J 2022;22:660-76. [Crossref] [PubMed]
34. Park MS, Moon SH, Kim TH, Oh J, Lee SJ, Chang HG, Shin JH. Paraspinal Muscles of Patients with Lumbar Diseases. J Neurol Surg A Cent Eur Neurosurg 2018;79:323-9. [Crossref] [PubMed]
35. Suo M, Zhang J, Sun T, Wang J, Liu X, Huang H, Li Z. The association between morphological characteristics of paraspinal muscle and spinal disorders. Ann Med 2023;55:2258922. [Crossref] [PubMed]
36. He K, Head J, Mouchtouris N, Hines K, Shea P, Schmidt R, Hoelscher C, Stricsek G, Harrop J, Sharan A. The Implications of Paraspinal Muscle Atrophy in Low Back Pain, Thoracolumbar Pathology, and Clinical Outcomes After Spine Surgery: A Review of the Literature. Global Spine J 2020;10:657-66. [Crossref] [PubMed]
37. Lee DY, Yang JH, Ki CH, Ko MS, Suk KS, Kim HS, Lee HM, Moon SH. Relationship between Bone Mineral Density and Spinal Muscle Area in Magnetic Resonance Imaging. J Bone Metab 2015;22:197-204. [Crossref] [PubMed]
38. Ekin EE, Altunrende ME. The association of reduced bone density with paraspinal muscle atrophy and adipose tissue in geriatric patients: a cross-sectional CT study. Turk J Med Sci 2019;49:538-42. [Crossref] [PubMed]
39. Zhao Y, Huang M, Serrano Sosa M, Cattell R, Fan W, Li M, Chen J, Gao M, Zhou Q, Li S, Zhang X, Huang C. Fatty infiltration of paraspinal muscles is associated with bone mineral density of the lumbar spine. Arch Osteoporos 2019;14:99. [Crossref] [PubMed]
40. Sollmann N, Franz D, Burian E, Löffler MT, Probst M, Gersing A, Schwaiger B, Pfeiffer D, Kirschke JS, Baum T, Riederer I. Assessment of paraspinal muscle characteristics, lumbar BMD, and their associations in routine multi-detector CT of patients with and without osteoporotic vertebral fractures. Eur J Radiol 2020;125:108867. [Crossref] [PubMed]
41. Kajiki Y, Tsuji H, Misawa H, Nakahara R, Tetsunaga T, Yamane K, Oda Y, Takao S, Ozaki T. Psoas muscle index predicts osteoporosis and fracture risk in individuals with degenerative spinal disease. Nutrition 2022;93:111428. [Crossref] [PubMed]
42. Gassert FT, Glanz L, Boehm C, Stelter J, Gassert FG, Leonhardt Y, Feuerriegel GC, Graf M, Wurm M, Baum T, Braren RF, Schwaiger BJ, Makowski MR, Karampinos D, Gersing AS. Associations between Bone Mineral Density and Longitudinal Changes of Vertebral Bone Marrow and Paraspinal Muscle Composition Assessed Using MR-Based Proton Density Fat Fraction and T2* Maps in Patients with and without Osteoporosis. Diagnostics (Basel) 2022;12:2467. [Crossref] [PubMed]
43. Gurusamy P, Larsen BA, Allen RT, Ward SR, Allison MA, Hughes-Austin JM. Density and Fat Fraction of the Psoas, Paraspinal, and Oblique Muscle Groups Are Associated With Lumbar Vertebral Bone Mineral Density in a Multi-Ethnic Community-Living Population: The Multi-Ethnic Study of Atherosclerosis. J Bone Miner Res 2022;37:1537-44. [Crossref] [PubMed]
44. Han G, Zou D, Liu Z, Zhou S, Li W, Gong C, Sun Z, Li W. Paraspinal muscle characteristics on MRI in degenerative lumbar spine with normal bone density, osteopenia and osteoporosis: a case-control study. BMC Musculoskelet Disord 2022;23:73. [Crossref] [PubMed]
45. Huang CB, Lin DD, Huang JQ, Hu W. Based on CT at the third lumbar spine level, the skeletal muscle index and psoas muscle index can predict osteoporosis. BMC Musculoskelet Disord 2022;23:933. [Crossref] [PubMed]
46. Yang Q, Yan D, Wang L, Li K, Liang W, Zhang W, Liu YD, Li XM, Blake GM, Konerth N, Cheng X, Tian W, Hind K. Muscle fat infiltration but not muscle cross-sectional area is independently associated with bone mineral density at the lumbar spine. Br J Radiol 2022;95:20210371. [Crossref] [PubMed]
47. Zhang Y, Dilixiati Y, Jiang W, Cao X, Chen Y, Guo H. Correlation of Psoas Muscle Index with Fragility Vertebral Fracture: A Retrospective Cross-Sectional Study of Middle-Aged and Elderly Women. Int J Endocrinol 2022;2022:4149468. [Crossref] [PubMed]
48. Zhou S, Chen S, Zhu X, You T, Li P, Shen H, Gao H, He Y, Zhang K. Associations between paraspinal muscles fatty infiltration and lumbar vertebral bone mineral density - An investigation by fast kVp switching dual-energy CT and QCT. Eur J Radiol Open 2022;9:100447. [Crossref] [PubMed]
49. Liu Z, Zhang Y, Huang D, Ma X, Duan Y, Jiang Y. Quantitative Study of Vertebral Body and Paravertebral Muscle Degeneration Based on Dual-Energy Computed Tomography: Correlation With Bone Mineral Density. J Comput Assist Tomogr 2023;47:86-92. [Crossref] [PubMed]
50. Kim JY, Chae SU, Kim GD, Cha MS. Changes of paraspinal muscles in postmenopausal osteoporotic spinal compression fractures: magnetic resonance imaging study. J Bone Metab 2013;20:75-81. [Crossref] [PubMed]
51. Byun SE, Kim S, Kim KH, Ha YC. Psoas cross-sectional area as a predictor of mortality and a diagnostic tool for sarcopenia in hip fracture patients. J Bone Miner Metab 2019;37:871-9. [Crossref] [PubMed]
52. Huang CWC, Tseng IJ, Yang SW, Lin YK, Chan WP. Lumbar muscle volume in postmenopausal women with osteoporotic compression fractures: quantitative measurement using MRI. Eur Radiol 2019;29:4999-5006. [Crossref] [PubMed]
53. Touban BM, Pavlesen S, Smoak JB, Sayegh MJ, Wang J, Zhao J, Anders MJ. Decreased Lean Psoas Cross-Sectional Area Is Associated With Increased 1-Year All-Cause Mortality in Male Elderly Orthopaedic Trauma Patients. J Orthop Trauma 2019;33:e1-e7. [Crossref] [PubMed]
54. Takahashi S, Hoshino M, Takayama K, Sasaoka R, Tsujio T, Yasuda H, Kanematsu F, Kono H, Toyoda H, Ohyama S, Hori Y, Nakamura H. The natural course of the paravertebral muscles after the onset of osteoporotic vertebral fracture. Osteoporos Int 2020;31:1089-95. [Crossref] [PubMed]
55. Sim JH, Lee SH, Kim JW, Koh WU, Kim HT, Ro YJ, Kim HJ. Low Psoas Lumbar Vertebral Index Is Associated with Mortality after Hip Fracture Surgery in Elderly Patients: A Retrospective Analysis. J Pers Med 2021;11:673. [Crossref] [PubMed]
56. Habibi H, Takahashi S, Hoshino M, Takayama K, Sasaoka R, Tsujio T, Yasuda H, Kanematsu F, Kono H, Toyoda H, Ohyama S, Hori Y, Nakamura H. Impact of paravertebral muscle in thoracolumbar and lower lumbar regions on outcomes following osteoporotic vertebral fracture: a multicenter cohort study. Arch Osteoporos 2021;16:2. [Crossref] [PubMed]
57. Kawakami T, Imagama T, Murakami T, Kaneoka T, Yamamoto M. Low psoas major muscle area as a risk factor for contralateral hip fracture following intertrochanteric fracture. J Musculoskelet Neuronal Interact 2021;21:495-500. [PubMed]
58. Zhao H, He Y, Yang JS, Bao W, Chen J, Liu JJ, Li QD, Liu P, Qian B, Zhao YT, Hao DJ. Can paraspinal muscle degeneration be a reason for refractures after percutaneous kyphoplasty? A magnetic resonance imaging observation. J Orthop Surg Res 2021;16:476. [Crossref] [PubMed]
59. Si F, Yuan S, Zang L, Fan N, Wu Q, Wang T, Wang A. Paraspinal Muscle Degeneration: A Potential Risk Factor for New Vertebral Compression Fractures After Percutaneous Kyphoplasty. Clin Interv Aging 2022;17:1237-48. [Crossref] [PubMed]
60. Okuwaki S, Funayama T, Ikumi A, Matsuura S, Kawamura H, Yamazaki M. Relationship between Vertebral Instability and the Cross-Sectional Area of Lumbar Muscles in Postmenopausal Acute Osteoporotic Vertebral Fractures. Spine Surg Relat Res 2021;6:51-7. [Crossref] [PubMed]
61. Shah A, Iyengar KP, Azzopardi C, Haleem S, Mehta J, Botchu R. Alteration in the Cross-sectional Area (CSA) Ratio of the Paraspinal Muscles following Vertebral Insufficiency Fractures. Indian J Radiol Imaging 2022;33:8-11. [PubMed]
62. Backhauß JC, Jansen O, Kauczor HU, Sedaghat S. Fatty Degeneration of the Autochthonous Muscles Is Significantly Associated with Incidental Non-Traumatic Vertebral Body Fractures of the Lower Thoracic Spine in Elderly Patients. J Clin Med 2023;12:4565. [Crossref] [PubMed]
63. Huang W, Cai XH, Li YR, Xu F, Jiang XH, Wang D, Tu M. The association between paraspinal muscle degeneration and osteoporotic vertebral compression fracture severity in postmenopausal women. J Back Musculoskelet Rehabil 2023;36:323-9. [Crossref] [PubMed]
64. Lee DG, Bae JH. Fatty infiltration of the multifidus muscle independently increases osteoporotic vertebral compression fracture risk. BMC Musculoskelet Disord 2023;24:508. [Crossref] [PubMed]