Abstract
Keywords
Introduction to Sarcopenia in Adult Spinal Deformity
Adult spinal deformity (ASD) surgery is challenged by high rates of postoperative complications and unplanned reinterventions, becoming unacceptable in value-driven healthcare systems. ASD is defined as structural spinal abnormalities in adults that cause physical distress. 1 Its high prevalence, cost of surgery, and rate of morbidity are straining healthcare systems worldwide.
Predictive ASD models are used to supplement clinical practice, largely driven by the massive physiological burden of deformity correction.2,3 Traditionally, these models have incorporated data on patient demographics, medical co-morbidities, and spinal alignment.4,5 Recently, hip axis measurements have been used to guide optimal sagittal alignment and minimize post-operative mechanical failures. 6 Use of artificial intelligence (AI), deep learning (DL), and incorporation of the paraspinal soft tissue have further increased the predictive power of these models.7,8 For example, positive soft-tissue injury findings per magnetic resonance imaging (MRI) predicted the need for surgery in pediatric cervical trauma patients. 9 Further incorporation of machine learning yielded improved predictive accuracy of proximal junction kyphosis (PJK) when using models incorporating raw MRIs compared to similar models fed radiographic data. 10 Analogous studies evaluating pre-operative soft tissue compromise in the form of senescent degeneration within relevant paraspinal muscles to predict operative outcomes would hold great utility.
For example, the co-existence of sarcopenia and osteoporosis, or “osteosarcopenia,” has been associated with increased falls, fractures, hospital/skilled nursing facility admission, and mortality risks. 13 Concurrent sarcopenia and obesity, or “sarcopenic obesity,” has been implicated with clinical consequences like cardiovascular disease, metabolic syndromes, falls, cognitive impairment, and overall mortality. 14 In an aging population with increasingly sedentary lifestyles, a multifactorial approach considering relevant comorbidities is crucial to the management of multifactorial sarcopenia. With the rising popularity of weight-loss medications like GLP-1 agonists promoting weight loss at the expense of lean muscle mass, more research is required to elucidate the relative benefits and dangers of these single-pronged approaches. 15
A distinction between “general” and “spine-specific” sarcopenia has been proposed. 16 General, or global, sarcopenia refers to a metric of low muscle strength, quantity, and/or physical performance. Notably, this definition does not specify muscle group but instead reports systemic muscle patency. Alternatively, the spine-specific or spinal sarcopenia distinction was implemented to narrow the scope of muscle patency to that of paraspinal musculature. 16 While this grouping of sarcopenia has not been adopted widely, early studies have distinguished between their respective associations to spinal parameters in facet-joint arthropathy, foraminal stenosis, and lumbar spinal stenosis. 16 These two conditions are frequently dissociated; significant spinal sarcopenia may be present despite preserved systemic muscle mass. Recognition of this distinction is essential for accurate prognostication in ASD.
Clinical definition of sarcopenia is also ill-defined. Various measurement modalities have been applied to diagnosing sarcopenia, ranging from functional examination of patient mobility via whole body performance to radiographic analysis of representative muscles.12,17 These efforts have evolved over time, and several modifiable characteristics have been identified to improve perioperative outcomes in ASD correction. 12
Large financial incentives exist for sarcopenia management. 10%-16% of elderly people are affected by general sarcopenia globally, with even greater prevalence among diabetic patients. 18 The total annual cost of hospitalization in the United States in 2014 was $40.4 billion for patients with sarcopenia. 19 The average cost per person was $260, with greatest burden for Hispanic women ($548/person) and elderly patients (>65 years; $375/person). 19 A nearly 2-fold greater odds of hospitalization was found for individuals with sarcopenia with an average 0.18 more hospital stays, costing an additional $2316. 19 Greater understanding of sarcopenia may serve to alleviate not only the total societal financial burden of treating sarcopenic patients, but also the financial discrepancies between different racial and age groups.
In 2023, the Scoliosis Research Society (SRS) developed a senescence task force to evaluate the current knowledge of sarcopenia: tools of assessment, potential avenues of treatment, and how sarcopenia may contribute to ASD complications. In response, we discuss the variability between sarcopenia and surgical outcomes for ASD, propose methods to assess global and spine-specific sarcopenia assessment, provide recommendations for optimization of ASD patients with sarcopenia undergoing surgery, and opine about the future of spine-specific sarcopenia.
Screening, Diagnosis and Quantification
EWGSOP2 Definition of Sarcopenia: Table Reproduced From Cruz-Jentoft et al 2018 With Permission 17
Fulfillment of criterion 1 suggests probable sarcopenia; additional fulfillment of criterion 2 suggests confirmed sarcopenia, and fulfillment of all 3 criteria suggests severe sarcopenia.
Abbreviations: HGS, hand-grip strength; CSA, cross-sectional area; MRI, magnetic resonance imaging; CT, computed tomography; DEXA, dual-energy X-ray absorptiometry; BIA, bioelectrical impedance analysis; SPPB, short physical performance battery; TUG, timed up-and-go.
Muscle Strength
Measured via hand grip strength (HGS) or the “chair stand test.”12,17,21-23 HGS is measured with a calibrated dynamometer, while the “chair stand test” measures the time required for a patient to stand five times from a seated position without use of their arms.
Muscle Mass (Normalized for BMI)
Reported as total skeletal muscle mass, appendicular muscle mass, or as a cross-sectional area of relevant muscle groups. These values are measured primarily by MRI or CT but can also be reported from dual-energy X-ray absorptiometry (DEXA) or Bioelectrical Impedance Analysis (BIA) with various frequency settings/calculations (SF, MF, BIASergi).12,17,24,25
Physical Performance
Assessed by a series of timed tests measuring the completion of standardized tasks, including gait speed, the Short Physical Performance Battery (SPPB), and the Timed Up-and-Go test (TUG).12,17,26,27 Gait speed is recorded as with ambulation of 4 meters. Alternatively, the SPPB accounts for a combination of gait speed, balance, and chair stand. The TUG test measures a similar combination of activities, including rising from a chair, walking 3 meters to a defined object, returning to the chair, and returning to a seated position. Conveniently, each of these performance tests may be readily performed in most clinical settings.
Rate of Low (Positive) Criteria for Sarcopenia, and Sensitivity/Specificity Among the Same Cohort of 503 Colorectal Cancer Patients by Different Measurement Modalities as Reported by Berg et al, 2024 25
Abbreviations: HGS, hand-grip strength; CT, computed tomography; DEXA, dual-energy X-ray absorptiometry; BIA, bioelectrical impedance analysis; SF, single frequency; MF, multifrequency.
aDEXA used as reference standard for sensivity and specificity calculations.
bHGS data used with DEXA measurements for confirmed sarcopenia diagnosis calculation.
cChair-Stand data used with MF-BIA measurements for confirmed sarcopenia diagnosis calculation.
Screening tools, while not possessing the same sensitivity as EWGSOP2 criteria, are convenient for daily practice.28,29 For example, the SARC-F screening tool is a questionnaire eliciting subjective information about strength (S), walking assistance (A), rising from a chair (R), climbing stairs (C), and falls (F) with good internal reliability and positive correlations to parallel sarcopenia criteria, instrumental activity of daily living (IADL) deficits, and mortality.28,30 Alternatively, the d3-isotope creatine dilution test may be used to screen sarcopenia, in which methyl-d3 creatine concentrations are measured after an oral dose of d3 creatine A. 11 This test accurately estimated whole-body muscle mass in strength training and has predicted disability and mortality of older adults.31,32 Although these initial results are promising, they have yet to be translated into clinical decision-making.
To fully appreciate the impact of sarcopenia on ASD, elucidating a reliable and accurate diagnostic parameter of sarcopenia that is derived from imaging modalities that are part of standard clinical care is paramount.
Predictive and Prognostic Value
An analysis of 235 patients who underwent thoracolumbar fusions for ASD found that patients with sarcopenia had similar outcomes to patients without sarcopenia. 23 Patients with sarcopenia, defined as the lowest quartile psoas muscle cross-sectional area at L3 and L4 (normalized for height), did not differ from controls when examining global balance, levels of fusion, mechanical failures, anesthetic duration, estimated blood loss, blood transfusion requirements, initiation of walking, hospital length of stay, aggregate complications, disposition, readmission rates, mortality, and revision surgeries. 23
In contrast, other studies have reported results suggesting direct correlations between sarcopenia and poor clinical outcomes in ASD patients. A study of 196 patients found that the lowest quartile sarcopenic patients (defined by the total psoas surface area at L3 divided by the total L3 vertebral body area) had longer ICU length of stay (1.2 ± 1.5 days vs 0.8 ± 1.1 days) and greater total postoperative blood transfusion volumes (573 ± 715 mL vs 269 ± 453 mL).
33
Another study of 73 patients who underwent pedicle subtraction osteotomy (PSO) found that sarcopenia, as defined by the psoas-lumbar vertebral index (PLVI) (Figure 1), was associated with increased total complication rate.
34
Specifically, a dose response between sarcopenia magnitude and complication rate was reported. Furthermore, PLVI below threshold values were associated with significantly elevated rates of PJK (34% for PLVI <1.1), wound infections (12% for PLVI <0.8), and dural tears (14% for PLVI <0.8).
34
Psoas-Lumbar Vertebral Index (PLVI) Equation Based on the Cross-Sectional Areas (CSA) of the Psoas and L4 Vertebral Body
An association between spinal sarcopenia and PJK after long thoracolumbar fusion to the pelvis was found in a cohort of 29 ASD patients >50 years old. 24 Greater average fatty infiltration percentage was found in the regions above the upper instrumented vertebra in patients with PJK (25.0 ± 6.5%) compared to patients without PJK (15.3 ± 4.8%). Hounsfield units and bone mineral density of the vertebral body at the same levels were not significantly different between PJK and non-PJK populations, suggesting that sarcopenia may be a better metric for predicting PJK than osteopenia. 24 Similar analyses of adjacent segment disease following spinal fusions with pelvic fixation in ASD patients consistently found positive correlations between metrics of sarcopenia and development of adjacent segment disease. Two retrospective studies found that the strongest predictor of PJK and proximal junction failure was psoas CSA in ASD patients after thoraco-pelvic fusions and short posterior lumbar fusions.35,36 Similarly, CSA (L3-4) and fatty infiltration (L4-5) of the lower lumbar multifidus was correlated with development of adjacent segment disease in a study of patients with posterior lumbar fusion. 37 Another correlation was revealed between adjacent segment disease and the combined lean muscle CSA (FCSA) of the multifidus, erector spinae, and psoas. Patients with adjacent segment disease were found to have a smaller FCSA (3681 mm2 vs 4268 mm2) and smaller FCSA/total CSA ratio (53.3% vs 58.6%). 38 These studies demonstrate the potential value of using spinal muscular mass and quality metrics to predict underlying bony disease in spine surgery.
One study found that only the degree of fatty infiltration of the erector spinae (and not that of the multifidus and psoas muscles at L4/L5) differed between patients who suffered PJK and those who did not. 39 A separate study contrarily found that patients with scoliosis had a smaller CSA of both multifidus and psoas muscles compared to patients with lumbar spinal stenosis. 40 Interestingly, it also found that HGS and DXA-measured whole-body composition were not different among these patients, which further calls into question the accuracy of global strength as a measure of sarcopenia. 40 These examples highlight how varying definitions and diagnostic tools for sarcopenia within and between the studies can result in a mixed picture regarding sarcopenia’s relationship with ASD. Future studies may be needed to help elucidate whether fatty infiltration or total muscle area have a greater contribution to the negative effect.
Beyond prognostication for operative complications in ASD correction, spinal sarcopenia has been implicated as a causative variable for ASD development. A cohort study found a smaller CSA index (CSA/height2; 12.6 cm2/m2 vs 15.1 cm2/m2), decreased lumbar extensor strength index (lumbar extensor strength/body weight; 0.5 Nm/kg vs 0.8 Nm/kg), and greater fat infiltration rate (20.1% vs 16.3%) in ASD patients with sagittal imbalance compared to non-ASD controls. 41 Interestingly, there was no difference in global sarcopenia metrics such as total appendicular skeletal muscle mass and HGS. These results suggest that correction of sarcopenia components specific to spinal musculature (CSA index, lumbar extensor strength, or lumbar fat infiltration) may prevent development of deformity in non-ASD patients as well as increase prognostic outcomes for ASD correction.
Summary of Studies Evaluating Predictive and Prognostic Value of Sarcopenia in ASD
Abbreviations: ASD, adult spinal deformity; CSA, cross sectional area; HGS, hand grip strength; PJK, proximal junctional kyphosis; PJF, proximal junctional failure.
aSarcopenia in this study was represented as a combined metric with components from both general and spine-specific sarcopenia.
Modifiable Targets
A multi-disciplinary approach may be taken to limit and/or reverse sarcopenia to decrease its associated complications. Several approaches have collectively endorsed that (1) consuming high-quality protein may limit loss of muscle strength and function in sarcopenia; (2) resistance exercise may slow loss of skeletal muscle oxidative capacity and stimulate hypertrophy to prevent and/or reverse sarcopenia.12,20 Other interventions are explored in research but require further development before incorporation into clinical care. 12 It should be noted that the following interventions are directed at general sarcopenia and may not adequately address localized spinal muscle degeneration (eg, fatty infiltration of paraspinal muscle). Further research must investigate targeted management of spinal sarcopenia before sufficient evidence is available for clinical recommendation.
General Sarcopenia Treatment Modalities and Quality of Evidence, Stratified by Treatment Setting. Table Reproduced From Dent et al 2021 With Permission 20
Only resistance exercise has been consistently shown to increase muscle performance and body composition in sarcopenic patients.11,20,26,27,42 2018 guidelines strongly recommended physical activity as first-line treatment for and primary prevention of general sarcopenia.11,20 A published trial measured various sarcopenic biomarkers and functional abilities in elderly patients undergoing an 8-week body weight resistance program without further supplementation. 26 Improvements in functional tests for the training cohort were found compared to the control group. Muscle specific biomarker concentrations also changed for the training group compared to the control group to suggest decreased sarcopenic burden. 26 A separate study further explored the effects of resistance training with additional supplementation on sarcopenia. 27 After 12 weeks of training and β-hydroxy-β-methyl butyrate supplementation in post-acute care geriatric patients, improvements were noted in performance [+1.8 points on short physical performance battery (SPPB) test], balance (+1.0 points), and chair stand (+0.7 points) when compared to a control group with a placebo supplement. While HGS significantly improved at 12 weeks for both the intervention (+3.7 kg) and placebo (+1.0 kg) groups, only the intervention group sustained increased strength at 1 year follow-up (+4.2 kg). 27 A 12 week resistance training program with collagen peptide supplement in sarcopenic subjects also found benefit. 42 After normalization by diet, the authors found supplemented and placebo cohorts significantly differed with respect to increased fat-free mass (FFM) (4.2 kg vs 2.9 kg) fat loss (5.5 kg vs 3.5 kg), and muscle strength increase (16.1 Nm vs 7.4 Nm). 42
Optimizing nutrition decrease muscle atrophy in aging populations has also shown promising results as a second-line treatment option. 20 An association of diet quality with handgrip weakness as a proxy for sarcopenia had been found in a multiethnic Asian human cohort. 21 Applying the dietary quality index-international (DQI-I) scale for grading diet variety, adequacy, moderation, and balance, researchers found increased HGS in patients within higher quartile DQI-I’s (+1.1 kg HGS in highest vs lowest quartile). A 15% lower odds ratio of handgrip weakness for each quartile increase in DQI-I was identified. Diet adequacy in the DQI-I was most correlated to strength. Interestingly, a caloric restriction has also been found to improve muscle function while attenuating age-related decline. Through molecular mechanisms like that of muscle activation, caloric restriction activates enzymes involved in lipid, protein, and mitochondrial function to decrease oxidant emission and hence decrease oxidative damage to DNA and proteins. 43 The balance between sufficient, diverse nutrients and caloric restriction reiterates a complicated, multifactorial network contributing to development of sarcopenia.
Pharmacologic supplementation actively researched for sarcopenia management but has yet to demonstrate consistent benefit in practice, despite promising initial results. 11 In one study, patients supplemented with L-carnitine had improvements of 12.4% greater HGS and 31.5% smaller frailty index scores compared to controls with no improvement at 10 weeks, though with no differences in frailty biomarkers (IL-6, TNF-α, and IGF-1). 44 A similar study found that diets with high vitamin D, E, and whey protein content improved skeletal muscle mass (+0.2 kg/m2), HGS (+2.7 kg), and favorable biomarkers such as IGF-1 (+14.3 ng/mL) and IL-2 (−575.3 pg/mL) in adults with sarcopenia after 6 months. 45 Other investigated drugs in literature have found minor benefits in older patients. 11
In summary, these experiments suggest that pre- and post-operative physical rehabilitation with a focus primarily on resistance exercise, and situationally nutritional fortification, may improve outcomes for adults with spinal deformity undergoing surgical intervention.
Surgical Decision-Making Considerations
Implementing the ideal corrective strategy for ASD patients remains challenging. Lower surgical invasiveness may yield lower surgical costs, decreased risks of complications and morbidity, and earlier postoperative mobilization than longer-segment fusions. 46 Alternatively, greater surgical invasiveness may facilitate greater deformity correction while yielding higher overall complication rates, longer operative and recovery times, and increased financial burdens. 46 The utility of accurate preoperative assessment of sarcopenia may lie in guiding surgeon’s decisions with respect to appropriate degree of surgical invasiveness. Consideration of global sarcopenia could tip the decision-making scale towards less invasive operations due to the larger physiologic stress associated with more invasive operations. Meanwhile muscle degeneration above the desired upper-instrumented vertebrae (UIV) or otherwise limited paraspinal function could influence the surgeon to proceed with different UIV based on stability potential and decreased risk of PJK at levels with robust paraspinal musculature. 39
Future Steps to Standardize Sarcopenia
Recommendations for the Next Steps in Advancing the Use of Sarcopenia in ASD
Abbreviations: ASD, adult spinal deformity; HGS, hand-grip strength; MRI, magnetic resonance imaging.
The relationship between global sarcopenia and spine-specific sarcopenia is less closely related than previously considered. 16 Patients undergoing lumbar spinal fusion for degenerative spinal pathologies had poorly correlated measures of general sarcopenia (tested with SPPB, HGS, and psoas index) compared to spine-specific sarcopenia (measured with fatty infiltration of the multifidus and erector spinae). 16 A separate study found that HGS could not distinguish between spinal deformity and spinal stenosis as opposed to spine-specific cross-sectional measurements, which were capable. Therefore, specific tests of spine-related muscles such as maximal voluntary exertion (MVE) and endurance time (ET) of paravertebral muscles may more accurately elucidate the degree of sarcopenia relevant to spinal deformity. 52 It is possible that global sarcopenia may be used as a parameter to indicate general frailty in patient selection while spine-specific sarcopenia is used in construct length planning.
Despite the relatively weak prognosticating evidence for general sarcopenia, proposed interventions are relatively safe and may provide benefits with minimal risks. Resistance exercise, supplemented by properly balanced nutrition, has consistently demonstrated significantly improved performance.26,27,42 Supplements like collagen, L-carnitine, vitamin D/E, whey protein and HMB are commercially available at an affordable rate with relatively benign side effect profiles.53,54 Additionally, a protein-rich diet with sufficient nutrients and food groups with variety, moderation, and adequacy have several beneficial outcomes, including reduced risk of metabolic syndrome and reduced sarcopenia prevalence.
21
Thus, we recommend providing a formal nutritional assessment and consult to safely implement proper dietary and supplement targets as part of a preoperative optimization strategy for ASD patients screened positive for sarcopenia. We do
Other considerations for the limited clinical utility of sarcopenia in ASD may include (1) the heterogeneity of ASD, (2) unconsidered sarcopenia magnitude, and (3) unexplored sarcopenia types. Spinal deformity encompasses a wide variety of etiologies that may differ in pathophysiology. 1 The studies in this review that have found inconclusive relationships between sarcopenia and surgical outcomes have selected patients based on surgical procedures. Analysis based on distinct pathophysiology of ASD may elucidate currently obscured relationships. For example, the relationship between sarcopenia and ASD from hereditary degenerative features may differ from that between sarcopenia and ASD from trauma/iatrogenic causes. Sarcopenia has also been commonly reported categorically, so an analysis of sarcopenia as a continuous variable may also reveal correlations lost in discrete analysis. Finally, as the intersections of sarcopenia with other pathologies such as sarcopenic obesity, osteosarcopenia and spinal sarcopenia are increasingly studied, their potential correlations in adult spinal deformity must also be explored.
Limitations
By nature of narrative reviews, the authors’ viewpoints are expressed, which increased subjectivity with interpretation of the literature used in this study. Additionally, this study did not employ a systematic review protocol to ensure a comprehensive overview of the evidence regarding sarcopenia and spinal deformity. Instead, it relied on the authors’ collective experiences to compile references (Figure 2). This approach may decrease the study’s reproducibility and introduce selection biases, potentially favoring pre-existing viewpoints. Relevant studies may have been missed, particularly if published in other languages or less prominent journals. Modified PRISMA Diagram Illustrating How Articles Were Gathered for This Review. Articles Were Subjectively Selected by Relevance as Nature of a Narrative Review
Conclusions
Sarcopenia is a nascent framework for studying ASD with no universal standard in clinical and research use. Previous attempts to define the phenomenon were highly variable, obscuring the true relationship between sarcopenia and ASD and stunting its implementation. Despite this variability, certain groups have successfully shown significant relationships between paraspinal atrophy and adverse outcomes following ASD correction. Pre-operative prevention and reversal of muscle atrophy in general sarcopenia seems prudent through a combination of resistance exercising and nutritional supplementation. Future studies should distinguish between general and spine specific sarcopenia and determine if more accurate sarcopenia assessment and pre-operative optimization would dictate surgical decision making, decrease complications, and improve patient outcomes following operations for ASD.
Footnotes
Acknowledgments
Scoliosis Research Society Senescence Task Force.
ORCID iDs
Author Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Tim Bui, Karan Joseph, and Camilo Molina. The first draft of the manuscript was written by Tim Bui and all authors commented on previous versions of the manuscript. All authors read and approved of the final manuscript.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Disclosure
No financial support was provided for this study; this study was conceived in response to the Scoliosis Research Society’s call for research, so it may include implicit biases aligned with those of the society. CAM (corresponding author) serves as a consultant for Kuros, Augmedics, SMAIO, Baxter Health, and SI-Bone.
