Our primary objective was to investigate the relationships between sarcopenia, its components, and osteoporosis as defined by The National Bone Health Alliance Working Group. The key findings are that sarcopenia, defined by the EWGSOP2, and its components were significantly associated with osteoporosis, particularly handgrip strength, SPPB and gait speed. We also observed significant correlations between the components of sarcopenia and BMD at all sites or with TBS.
Our cohort was composed of community-dwelling elderly women with a low level of frailty. The observed prevalence of sarcopenia was 9.2% according to the EWGSOP2 definition, which is higher compared to the prevalence described using the same criteria in a recent meta-analysis by Petermann-Rocha et al. However, these authors also noted that the prevalence of sarcopenia can vary greatly, ranging from 0.3–91.2% in women, depending on the diagnostic criteria used. There is still no universally accepted definition of sarcopenia, leading to large differences in the results of various sarcopenia studies (19).
The operational definition of osteoporosis, based on the WHO criteria, includes subjects with a BMD T-score ≤ − 2.5 SD compared to the mean value for young female adults, at the hip, femoral neck, or lumbar spine. In our study, despite ongoing debate about the recommended definition of osteoporosis, we decided to use the more inclusive definition of osteoporosis previously described by Siris et al., which includes patients with a fragility MOF or a high predicted fracture risk (3). Although this definition is not universally accepted, the American College of Endocrinology recently proposed similar diagnostic criteria to define osteoporosis in postmenopausal women (20). As expected, the prevalence of osteoporosis in our subjects also varied depending on the criteria used; in our study, 35.6% of the subjects were classified as osteoporotic based on a BMD T-score ≤ − 2.5, history of MOF(s) or high fracture risk, whereas only 23.6% would be diagnosed with osteoporosis based solely on low BMD, highlighting and confirming the risk of underdiagnosis and undertreatment when BMD alone is considered as the diagnostic criterion.
Indeed, it is well-known that at least 50% of fragility fractures occur in patients who present a T-score greater than − 2.5 and even superior to -1.0. Furthermore, BMD alone is insufficient to correctly predict fracture risk. Numerous other CRFs have been described, including age, corticosteroid treatment, parental history of hip fracture or a personal history of fragility fracture, which are notably used in the FRAX score or in the fracture prediction models we recently developed (10, 12, 21, 22).
In addition, pharmacological treatments, particularly bisphosphonates, have been proven to be useful in significantly reducing fracture risk and increasing BMD in osteopenic patients without prior fractures (23). This raises questions about the use of the standard osteoporosis definition and justifies our use of the clinical definition by the National Bone Health Alliance Working Group (3).
In our cohort, a significant association between sarcopenia and its individually assessed components was observed with the presence of osteoporosis. After adjustment for confounding variables, only handgrip strength, SPPB, and gait speed remained significantly associated with osteoporosis. A colinear relationship was found between age, BMI, and sarcopenia components. Nevertheless, as in most previous studies, we decided to keep these covariates in the multivariate models due to their significant relationship with BMD and clinical osteoporosis. In agreement with our results, other investigators have demonstrated a significant independent association between poor muscle strength, gait speed, and fracture risk (24, 25, 26). Poor physical performance, defined by a low gait speed but also a low SPPB score has been shown to be associated with femoral neck and total hip BMD in a cohort of Chinese postmenopausal women (27).
Furthermore, low handgrip strength combined with slow gait speed has been associated with incident falls, mobility limitations, hip fractures, and death in a large American cohort study (28). Handgrip strength has also been shown to predict fracture-free survival in women with a normal BMD in a 15-year follow-up study of Finnish women. Those women demonstrating handgrip strength results in the lowest quartile showed a lower fracture-free survival compared to the highest quartile (29).
All these observations suggest that handgrip strength and gait speed are strong predictors of increased fracture risk. Their easy assessment, availability, and inexpensiveness should make them useful and practical tools for detecting and preventing fractures in routine clinical practice.
We did not find a significant association between ALMI and osteoporosis after adjusting for various confounding covariates. The influence of body composition on osteoporosis and fracture risk is still debated due to inconsistent results. Various studies have reported similar findings to ours. In 114 postmenopausal Brazilian women, ALMI did not remain significantly associated with BMD after adjustment for age, BMI, and race (30). Kapus et al. also found no association between muscle mass or muscle strength and BMD, but they suggested an effect of fat mass on hip BMD (31). In the subgroup of frail subjects of the Women’s Health Initiative Observational Study, both lean mass and fat mass were associated with hip BMD, but only higher fat mass was independently associated with a lower rate of hip fracture (32).
In contrast, other authors, such as Jang et al. (33) and Sjoblom et al., (34) reported that low muscle mass was significantly associated with osteoporosis in women, a finding consistent with the pathophysiological notion that bone anabolism is supported by the mechanical strain resulting from muscle contractions (5).
BMI could also interact with the association between lean mass and BMD. Zhu et al. reported that lean mass had a weaker association with BMD in the higher BMI tertile, particularly for BMD at the spine, suggesting an influence of fat mass, which is more closely correlated to BMI compared to lean mass (35).
These inconsistent results could also be explained by the fact that DXA is not an ideal technique for measurement of muscle mass since it includes water and fibrotic tissue. The lack of association of DXA-measured lean mass with adverse health outcomes explains why it is not included in the Sarcopenia Definitions and Outcomes Consortium (SDOC) definition of sarcopenia, which only considers muscle slowness and weakness. Our results support this choice. However, muscle mass measured by more precise techniques such as D3- creatine dilution has demonstrated an association with significant health outcomes (28), leaving the question unresolved.
The association of criteria used to define sarcopenia with BMD and fracture risk has been extensively studied, but conflicting results persist in the literature. In a longitudinal study of almost 500 adults in The Netherlands, no association was found between sarcopenia defined according to the FNIH or EGWSOP, or sarcopenia components, and fracture incidence. However, only 60 subjects experienced a fracture during their follow-up, and the low statistical power to detect an association is probably an explanation for these results. Furthermore, contrary to our study, their cohort included 50% of men, though it is well known that women are more at risk of developing osteoporosis (36).
On the other hand, in agreement with our results, lower values in the components of sarcopenia were strongly associated with osteoporosis in the postmenopausal women of The Osteoporosis Risk Factor and Prevention - Fracture Prevention Study (OSTPRE-FPS) study (34).
A recent meta-analysis reported a significant association between sarcopenia and low BMD, as well as a high risk of fractures, which also supports the role of sarcopenia in assessing osteoporosis and emphasizes the importance of implementing sarcopenia prevention strategies alongside osteoporosis treatment (37).
Lastly, we found a significant correlation between sarcopenia components and TBS, which is a textural analysis of lumbar spine DXA images reflecting bone microarchitecture. The TBS is a risk factor for fracture, independent of BMD, in osteopenic patients. An elevated TBS value indicates stronger bones and a lower risk of fracture. Our findings align with most previous results indicating an association of sarcopenia with TBS, reinforcing the importance of detecting sarcopenia when assessing fracture risk (38, 39).
Our study has several limitations. First, its cross-sectional nature makes it impossible to establish a causal relationship between sarcopenia or its components and osteoporosis. The study sample mainly consisted of nonfrail, community-dwelling women willing to be included a second time in the FRISBEE study, limiting the generalizability of our findings to frail and/or male subjects. Lastly, the FRAX score partly used to define clinical osteoporosis was the score determined at baseline, which could underestimate the proportion of osteoporotic subjects in our cohort.
Our study also has some strengths. This study is based on data from a well-followed cohort, the FRISBEE study cohort. All fractures, declared or not by the study participants, were validated. To our knowledge, this is the first study to evaluate the association between sarcopenia and its components with a definition of osteoporosis extended to patients with a high fracture risk in the presence of normal or osteopenic BMD.