- Email: [email protected]
Sarcopenia does not affect clinical outcomes following lumbar fusion
Journal of Clinical Neuroscience 64 (2019) 150–154
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical study
Sarcopenia does not affect clinical outcomes following lumbar fusion James C. McKenzie ⇑, Scott C. Wagner, Arjun Sebastian, David S. Casper, John Mangan, Justin Stull, Alan S. Hilibrand, Alexander R. Vaccaro, Christopher Kepler Rothman Institute at Thomas Jefferson University Hospital, Philadelphia, PA, USA
a r t i c l e
i n f o
Article history: Received 20 January 2019 Accepted 8 March 2019
Keywords: Sarcopenia Degenerative spondylisthesis Lumbar fusion
a b s t r a c t Sarcopenia, defined as decreased skeletal muscle mass or function, has recently been found to have increased perioperative morbidity and mortality. The relationship between sarcopenia and clinical outcomes in patients undergoing lumbar fusion has not been examined. This study investigates whether sarcopenia affects fusion rates and outcomes following single-level lumbar decompression and fusion. A retrospective analysis was undertaken of 97 consecutive patients who underwent a single level lumbar fusion for degenerative spondylolisthesis. Demographics, perioperative data, and patient reported clinical outcomes were collected. Measurements of paraspinal muscle CSA were made using a standardized protocol at the level of the L3-4 disc space on a preoperative lumbar MRI. Univariate analysis was used to compare cohorts with regards to demographics, comorbidities, and clinical outcomes. Of 97 patients, 16 patients (15.8%) were in the sarcopenic cohort utilizing a threshold of 986.1 mm2/m2. Reoperation rates were not significantly different between the two groups (0% vs 3.6%, p = .451). The sarcopenia cohort had lower BMI (28.1 vs 31.8, p = .017) and less male patients (6.3% vs 55.6%, p < .001). Mean follow-up was 18.3 months. There was no significant difference in postoperative Oswestry Disability Index (ODI) (24.7 vs 23.2, p = .794) Short Form 12 Physical (38.0 vs. 40.4, p = .445) Mental scores (55.5 vs. 53.6, p = .503), or visual analog scale (VAS) back pain scores (3.4 vs. 3.3, p = .818). No significant difference was found with regards to outcomes when comparing sarcopenic to non-sarcopenic patients undergoing lumbar fusion. Sarcopenia does not impact the clinical success of lumbar fusion for degenerative spondylolisthesis. Ó 2019 Elsevier Ltd. All rights reserved.
1. Introduction Lumbar paraspinal muscles are responsible for maintaining posture, spine mobility, and protecting the integrity of intervertebral discs, facet joints, and adjacent structures. Several studies have demonstrated the importance of lumbar paraspinal muscle cross-sectional surface area (CSA) and morphometry in predicting lumbago and disability [1–6]. Decreased paraspinal CSA and multifidus fat infiltration may occur as a normal aging process, result from underlying lumbar pathology, and contribute to structural pathology including low back pain [3,4,7]. Sarcopenia is defined as a progressive loss of skeletal muscle mass and function with resultant disability [8]. Sarcopenia, diagnosed by computerized tomography (CT) or magnetic resonance imaging (MRI) paraspinal or abdominal muscle CSA, may be a sign of malnutrition, limited mobility, and overall poor functional status. Low muscle mass is
⇑ Corresponding author at: Rothman Institute, 925 Chestnut St., 5th Floor, Philadelphia, PA 19107, USA. E-mail address: [email protected] (J.C. McKenzie). https://doi.org/10.1016/j.jocn.2019.03.015 0967-5868/Ó 2019 Elsevier Ltd. All rights reserved.
associated with several detrimental health effects including; increased fall risk, osteoporosis, morbidity, and increased mortality [9–11]. A recent retrospective study demonstrated increased 1-year mortality among elderly patients with sarcopenia suffering from orthopaedic pelvic trauma compared to a non-sarcopenic cohort [9]. In this study, there was no difference between the Charlson Comorbidity Index (CCI) or ASA (American Society of Anesthesiologists) Class in the sarcopenia and non sarcopenic groups, suggesting that sarcopenia may be an independent marker of overall frailty not accounted for by other risk stratification methods. Investigation into the relationship between generalized sarcopenia and clinical outcomes in patients undergoing spine surgery is limited. One retrospective study evaluated the association between sarcopenia and perioperative complications, including mortality, in 102 patients over the age of 65 undergoing elective thoracolumbar surgery for degenerative pathology. In this study, sarcopenia, defined by total axial psoas area at mid L3 level on preoperative CT, was not predictive of perioperative complications, length of stay, or in-hospital mortality in this group [12]. The
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authors concluded that sarcopenia, as measured by psoas cross sectional area, may not be an appropriate predictor of adverse events after elective spine procedures [12]. To our knowledge, there are no studies specifically evaluating the effect of sarcopenia on clinical and patient reported outcomes after lumbar fusion. The purpose of this study, therefore, was to determine the effects of sarcopenia on patient reported Health Related Quality of Life outcomes and clinical outcomes of patients undergoing single level lumbar decompression and fusion for degenerative spondylolisthesis, with the hypothesis that sarcopenia would adversely affect all outcome measures post-operatively.
2. Patients and methods After institutional review board (IRB) approval was obtained, a retrospective review of outpatient medical records was performed for patients with degenerative lumbar spondylolisthesis who underwent a single level posterior lumbar fusion. Patients were separated into Sarcopenia or Non-Sarcopenia cohorts based on individual measurement of the paraspinal muscle index, defined as the ratio between total paraspinal (iliocostalis, longissimus, multifidus, and psoas) muscle CSA and patient height squared. Patients who were one standard deviation below the average paraspinal muscle index, which was defined as 986.1 mm2/m2, were placed into the Sarcopenia cohort. The data were collected from seven surgeons between January and December 2014, with all procedures performed at a single institution. Pre-and postoperative patient-reported outcomes scores, including the Oswestry Disability Index (ODI), Short Form 12 Physical (SF-12 P), Short Form 12 Mental (SF-12 M) and back pain VAS scores, were included for analysis. Mean follow-up was 18.3 months. Demographic data, including age, BMI, smoking status, history of coronary artery disease and/or congestive heart failure, were also recorded. Inclusion criteria were any patient above the age of 18 at our institution diagnosed with degenerative lumbar spondylolisthesis, based on the ICD-9 code 721.42, with a preoperative lumbar spine MRI and completed preoperative patient-reported outcome scores. Patients under the age of 18 years, those lacking a preoperative lumbar spine MRI or completed preoperative patient-reported outcome scores, or those with a diagnosis other than degenerative lumbar spondylolisthesis (such as spinal cord injury, epidural hematoma or abscess, or metastatic disease) were excluded from the study. T1-weighted axial MRI images were evaluated independently by two reviewers, both blinded to their respective measurements. Using Sectra Liteview PACS Imaging measurement software, the CSA of the posterior paraspinal musculature (multifidus, iliocostalis, and longissimus), as well as the psoas CSA, were measured. The measurements were taken through the same axial cut at the midpoint of the L3-4 vertebral disc space (Fig. 1). To improve inter-observer reliability, the average of the two measurements was then recorded as the CSA for that muscle. Postoperative patient reported outcomes were collected from the latest postoperative outpatient visit. Incidence of reoperation, defined as any return to the operating room such as surgical site infection, wound dehiscence, hardware failure, or pseudarthrosis specific to the one-level lumbar fusion was also recorded. Due to its retrospective nature, some postoperative patient reported outcomes were not available for analysis. Four patients did not have any postoperative reported outcomes and were excluded from the study. Data analysis was performed using SPSS software (Version 22.0 IBM Armonk, NY). Categorical data were analyzed with the Chi Square Test and continuous data with the two-tailed Student
Fig. 1. Representative Cross Sectional MRI image at the L3-4 Disc Space showing the example of measuring the Cross Sectional Area (CSA) of the paralumbar musculature.
Sarcopenia Group Lumbar Level Fused
13%
6%
6%
L1-2 12%
L2-3 L3-4 L4-5 L5-S1
63%
Fig. 2. Pie Chart showing the Lumbar Levels Fused in the Sarcopenia Group. A majority of the Sarcopenia Group was fused at the L4-5 Lumbar Level.
t-test. Statistical significance was set with an alpha of 0.05 and power with a beta value of 0.80. The primary outcome was Health Related Quality of Life and clinical outcomes.
3. Results Ninety-seven medical records met inclusion criteria and were reviewed. Sixteen patients (15.8%) were identified as having sarcopenia utilizing a threshold of 986.1 mm2/m2. Eighty-one patients
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Non-Sarcopenia Group Lumbar Level Fused
15%
2%
L1-2
16%
L2-3 L3-4 L4-5 L5-S1 67%
Fig. 3. Pie chart showing the Lumbar level fused in the Non-Sarcopenia Group. Again, the most common level fused in the Lumbar spine is the L4-5 Level.
copenia and non-Sarcopenia group respectively (Figs. 2. and 3). Reoperation rates were not significantly different between the two groups (0% vs 3.6%, p = .530) (Table 1). With regards to ODI scores, there was no significant difference preoperatively (47.9 vs 46.6, p = .767), postoperatively (24.7 vs 23.2, p = .794), or in magnitude of change (23.4 vs 22.5, p = .877). SF-12 mental component scores showed no differences preoperatively (47.5 vs 46.6, p = .772), postoperatively (55.5 vs 53.6, p = .503), or in magnitude of change (6.9 vs 5.6, p = .732). SF-12 physical component scores also showed no difference preoperatively (28.9 vs 29.0, p = .973), postoperatively (38.0 vs 40.4, p = .445), or in magnitude of change (8.6 vs 10.0, p = .687). Similar findings were also found with regards to VAS back scores showing no significant differences preoperatively (7.4 vs 6.9, p = .451), postoperatively (3.4 vs 3.3, p = .878), or in magnitude of change (3.9 vs 3.2, p = .418) (Table 2) (Fig. 4).
4. Discussion Table 1 Patient Demographics.
N (%) Male Gender (%) ASA Class 3 (%) Mean Age [SD] Mean BMI [SD] Diabetes Mellitus (%) Smoking (%) Cardiac Disease (%) Reoperation (%)
Sarcopenia
Non-Sarcopenia
P value
16 (16.5%) 1 (6.3%) 2 (12.5%) 64.56 [16.943] 28.11 [4.456] 4 (25.0%) 3 (18.8%) 4 (25.0%) 0 (0%)
81 (83.5%) 45 (55.6%) 7 (8.4%) 61.58 [13.342] 31.80 [5.929] 9 (10.8%) 23 (30.1%) 13 (16.9%) 2 (3.6%)
NA <.001* .626 .219 .017* .145 .417 .395 .530
SD-Standard Deviation. * And bolded values are statistically significant (p < .05).
were included in the non-Sarcopenia group. The average time of lumbar spine MRI to outpatient evaluation was 3.6 months. The average postoperative score follow-up was 18.3 months. The Sarcopenia group had a lower mean BMI (28.11 vs. 31.8, p = .017) and less male patients (6.3% vs. 55.6%, p < .001) in comparison to the non-Sarcopenia group. There was no significant difference between the Sarcopenia and non-Sarcopenia group with regards to ASA class 3 (12.5% vs 8.4%, p = .626), smoking (18.8% vs 30.1% p = .417), diabetes mellitus (25% vs. 16.9%, p = .395) and heart disease (25% vs 16.9%, p = .395). There was no significant difference in lumbar level fused with 63% and 67% at L4-5 in the Sar-
In an aging population, the incidence of chronic LBP and degenerative lumbar disease is increasing [13,14]. One of the possible etiologies of chronic LBP and degenerative lumbar spondylolisthesis comes from the atrophy and fatty infiltration of paraspinal musculature, and has been shown to increase complications following injury, especially in acute trauma [9,15]. The atrophy of paraspinal musculature leads to worsening core balance, posture, and ambulatory dysfunction which places a significant mechanical disadvantage throughout the vertebral column. Paraspinal sarcopenia has been associated with osteoporotic lumbar vertebral fractures, which can also lead to degeneration of the lumbar spine and subsequent LBP and lower extremity radiculopathy [16]. Sarcopenia is an important comorbidity to assess and recognize when evaluating elderly patients with lumbar degeneration and LBP. Sarcopenia has been established as a risk factor for perioperative morbidity following thoracolumbar surgery. Bokshan et al assessed 46 patients for sarcopenia undergoing thoracolumbar spine surgery via L4 psoas muscle CSA on preoperative CT scan. 16 patients were sarcopenic and found to have 1.7 times longer hospital length of stay, threefold increase in perioperative complications including deep venous thrombosis and wound drainage, along with increased non-home discharge from the hospital [17]. Similarly, Zakaria et al. evaluated 395 patients undergoing posterior lumbar laminectomy, decompression and/or fusion and measured L4 psoas muscle CSA via MRI. Patients in the lowest third of psoas CSA were found to have increased risk of postoperative
Table 2 Patient Reported Outcome Scores.
Mean Mean Mean Mean Mean Mean Mean Mean Mean Mean Mean Mean
Preop ODI [SD] Postop ODI [SD] D ODI [SD] Preop SF-12 Mental [SD] Postop SF-12 Mental [SD] D SF-12 Mental [SD] Preop SF-12 Physical [SD] Postop SF-12 Physical [SD] D SF-12 Physical [SD] Preop VAS Back Pain [SD] Postop VAS Back Pain [SD] D VAS Back Pain [SD]
SD-Standard Deviation. D-‘‘Change In”. ODI-Oswestry Disability Index. VAS-Visual Analog Scale. SF-12-Short Form 12 Questionnaire.
Sarcopenia
Non-Sarcopenia
P value
47.9 [46.557] 24.7 [23.241] 23.4 [ 22.530] 47.5 [46.585] 55.5 [53.640] 6.9 [5.602] 28.9 [29.014] 38.0 [40.421] 8.6 [10.013] 7.4 [6.894] 3.4 [3.275] 3.9 [ 3.214]
46.6 [16.493] 23.2 [20.195] 22.5 [ 19.333] 46.6 [11.769] 53.6 [8.761] 5.6 [12.843] 29.0 [6.958] 40.4 [10.343] 10.0 [12.089] 6.9 [2.427] 3.3 [2.509] 3.2 [ 2.856]
.767 .794 .877 .772 .503 .732 .973 .445 .687 .451 .878 .418
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Sarcopenia versus Non-Sarcopenia Group Pre- and Postoperave Paent Reported Outcomes 70 60 50 40
30 20 10 0 -10
Preop ODI Postop ODIPreop SF12 Postop Preop SF12 Postop Preop VAS Postop VAS Mental SF12 Physical SF12 back pain back pain Mental Physical Sarcopenia Group
Non-Sarcopenia Group
Fig. 4. Bar Graph comparing the Sarcopenia Group and Non-Sarcopenia Group in pre and postoperative patient reported outcomes. None of the outcomes were significantly different between the two groups pre- or postoperatively.
complications including 30 and 90 day hospital readmission, DVT/ PE, and surgical site infection [18]. The goal of our study was to evaluate preoperative and postoperative patient-reported outcomes in lumbar fusion surgery for patients with sarcopenia. To our knowledge, this is the first study in the literature to specifically evaluate clinical outcomes both preoperatively and long term (>1 year) following spine fusion surgery. We found no difference in ODI, SF-12 physical or mental scores, or VAS back pain scores between the Sarcopenia and non-Sarcopenia groups either pre- or postoperatively. There was also no difference in reoperation rates for surgical site infection, pseudarthrosis, or hardware failure. It is important to note that both the Sarcopenia and non-Sarcopenia group had a similar improvement in all four patient-reported outcome scores at long term follow-up suggesting that sarcopenia does not impact overall recovery following lumbar fusion surgery. We did find a significant difference in gender and BMI between cohorts, with female patients with lower BMI more likely to have sarcopenia. Women tend to have a lower total muscle mass overall especially in comparison of elderly women versus their male counterparts, which can explain our finding [19]. Lower BMI has also been cited as a risk factor for sarcopenia in multiple studies [12,15]. It is unknown whether differences in baseline muscular morphology, hormonal changes with aging, or differential inflammatory responses lead to this gender discrepancy in sarcopenia, further study is needed. There is no standardized measurement or diagnosis of sarcopenia. Sarcopenia can be defined functionally based on hand-grip strength or quantitatively by evaluating the CSA via CT or MRI of lean muscle or skeletal muscle depending on the anatomic region being measured [20,21]. Our focus was on establishing a biomechanical measurement of paraspinal CSA via MRI which would likely have the best sensitivity of measuring muscular morphology. We also decided to use a paraspinal muscular index to evaluate all four paraspinal muscles as a unit and normalize for patient height. We chose our threshold of 986.1 mm2/m2 to strictly define sarcopenia within our study population as the lowest quartile of paraspinal muscular index and 1 standard deviation below the mean. The strengths of this study include pre- and postoperative patient-reported outcome scores with follow up beyond the imme-
diate postoperative period of 90 days. We utilized an established method of measuring the CSA of the paraspinal musculature and had two independent measurements of CSA that were averaged to reduce bias. The study cohorts had represented a general population of patients with prior advanced imaging who were seeking surgical consultation for lumbar spondylolisthesis. The limitations of this study include its retrospective nature, which can lead to potential collection, observer, and recall bias. Additionally, our study population is limited in size, particularly the sarcopenic cohort, but this was intentional based on our relatively strict definition of sarcopenia. There was a significant difference in BMI and female gender in the Sarcopenic cohorts, which could potentially affect outcomes, but likely represents a population likely to have sarcopenia. Lumbar spine MRIs were performed at separate locations with different machines, and this could potentially affect image quality and CSA measurements. However, all the imaging data were uploaded into our software system to standardize the measurement process and limit this weakness. Sarcopenia as defined by CSA of the paraspinal musculature may be an important risk factor for perioperative morbidity during thoracolumbar spine surgery. However, there was no long-term difference in patient-reported clinical outcomes or reoperation rates between patients with and without sarcopenia. Women with lower BMI are likely at higher risk for sarcopenia and further study is needed to best optimize these patients for lumbar surgery to limit perioperative morbidity, but may have equivocal outcomes at longer term clinical followup. Conflict of interest statement No funds were received in support of this work. The authors disclose no direct or indirect conflicts of interest in the preparation of this manuscript. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Ethical board review statement This study was approved by the Institutional Review Board at Thomas Jefferson University Hospital. Each author certifies that
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our institution approved the human protocol for this investigation and that all investigations were conducted in conformity with ethical principles of research. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.jocn.2019.03.015. References [1] Kjaer P, Bendix T, Sorensen JS, Korsholm L, Leboeuf-Yde C. Are MRI-defined fat infiltrations in the multifidus muscles associated with low back pain? BMC Med 2007;5:2. https://doi.org/10.1186/1741-7015-5-2. [2] Parkkola R, Rytökoski U, Kormano M. Magnetic resonance imaging of the discs and trunk muscles in patients with chronic low back pain and healthy control subjects. Spine 1993;18(7):830–6. [3] Shahidi B, Parra CL, Berry DB, et al. Contribution of lumbar spine pathology and age to paraspinal muscle size and fatty infiltration. Spine 2017;42(8):616–23. https://doi.org/10.1097/BRS.0000000000001848. [4] Kalichman L, Hodges P, Li L, Guermazi A, Hunter DJ. Changes in paraspinal muscles and their association with low back pain and spinal degeneration: CT study. Eur Spine J 2010;19(7):1136–44. [5] Danneels LA, Vanderstraeten GG, Cambier DC, Witvrouw EE, De Cuyper HJ. CT imaging of trunk muscles in chronic low back pain patients and healthy control subjects. Eur Spine J 2000;9(4):266–72. [6] Teichtahl AJ, Urquhart DM, Wang Y, et al. Fat infiltration of paraspinal muscles is associated with low back pain, disability, and structural abnormalities in community-based adults. Spine J 2015;15(7):1593–601. https://doi.org/ 10.1016/j.spinee.2015.03.039. [7] Crawford RJ, Volken T, Valentin S, Melloh M, Elliott JM. Rate of lumbar paravertebral muscle fat infiltration versus spinal degeneration in asymptomatic populations: an age-aggregated cross-sectional simulation study. Scoliosis Spinal Disord 2016;11:21. https://doi.org/10.1186/s13013016-0080-0. [8] Cruz-Jentoft AJ, Baeyens JP, Bauer JM, et al. Sarcopenia: European consensus on definition and diagnosis: report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010;39(4):412–23. https://doi.org/10.1093/ ageing/afq034.
[9] Deren ME, Babu J, Cohen EM, Machan J, Born CT, Hayda R. Increased mortality in elderly patients with sarcopenia and acetabular fractures. J Bone Joint Surg Am 2017;99(3):200–6. https://doi.org/10.2106/JBJS.16.00734. [10] Ebbeling L, Grabo DJ, Shashaty M, et al. Psoas:lumbar vertebra index: central sarcopenia independently predicts morbidity in elderly trauma patients. Eur J Trauma Emerg Surg 2014;40(1):57–65. https://doi.org/10.1007/s00068-0130313-3. [11] Tarantino U, Piccirilli E, Fantini M, Baldi J, Gasbarra E, Bei R. Sarcopenia and fragility fractures: molecular and clinical evidence of the bone-muscle interaction. J Bone Joint Surg Am 2015;97(5):429–37. https://doi.org/ 10.2106/JBJS.N.00648. [12] Charest-Morin R, Street J, Zhang H, et al. Frailty and sarcopenia do not predict adverse events in an elderly population undergoing non-complex primary elective surgery for degenerative conditions of the lumbar spine. Spine J 2017. https://doi.org/10.1016/j.spinee.2017.07.003. [13] Goubert D, De Pauw R, Meeus M, et al. Lumbar muscle structure and function in chronic versus recurrent low back pain: a cross-sectional study. Spine J 2017. https://doi.org/10.1016/j.spinee.2017.04.025. [14] Sions JM, Elliott JM, Pohlig RT, Hicks GE. Trunk muscle characteristics of the multifidi, erector spinae, psoas, and quadratus lumborum in older adults with and without chronic low back pain. J Orthop Sports Phys Ther 2017;47 (3):173–9. https://doi.org/10.2519/jospt.2017.7002. [15] Park S, Kim HJ, Ko BG, et al. The prevalence and impact of sarcopenia on degenerative lumbar spinal stenosis. Bone Joint J 2016;98-B(8):1093–8. https://doi.org/10.1302/0301-620X.98B8.37623. [16] Hida T, Shimokata H, Sakai Y, et al. Sarcopenia and sarcopenic leg as potential risk factors for acute osteoporotic vertebral fracture among older women. Eur Spine J 2016;25(11):3424–31. https://doi.org/10.1007/s00586-015-3805-5. [17] Bokshan SL, Han AL, DePasse JM, et al. Effect of sarcopenia on postoperative morbidity and mortality after thoracolumbar spine surgery. Orthopedics 2016;39(6):e1159–64. https://doi.org/10.3928/01477447-20160811-02. [18] Zakaria HM, Schultz L, Mossa-Basha F, Griffith B, Chang V. Morphometrics as a predictor of perioperative morbidity after lumbar spine surgery. Neurosurg Focus 2015;39(4):E5. https://doi.org/10.3171/2015.7.FOCUS15257. [19] Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18–88 yr. J Appl Physiol 2000;89 (1):81–8. [20] Francis P, Lyons M, Piasecki M, Mc Phee J, Hind K, Jakeman P. Measurement of muscle health in aging. Biogerontology 2017. https://doi.org/10.1007/s10522017-9697-5. [21] Kim M, Shinkai S. Prevalence of muscle weakness based on different diagnostic criteria in community-dwelling older adults: a comparison of grip strength dynamometers. Geriatr Gerontol Int 2017. https://doi.org/10.1111/ggi.13027.
Contents lists available at ScienceDirect
Journal of Clinical Neuroscience journal homepage: www.elsevier.com/locate/jocn
Clinical study
Sarcopenia does not affect clinical outcomes following lumbar fusion James C. McKenzie ⇑, Scott C. Wagner, Arjun Sebastian, David S. Casper, John Mangan, Justin Stull, Alan S. Hilibrand, Alexander R. Vaccaro, Christopher Kepler Rothman Institute at Thomas Jefferson University Hospital, Philadelphia, PA, USA
a r t i c l e
i n f o
Article history: Received 20 January 2019 Accepted 8 March 2019
Keywords: Sarcopenia Degenerative spondylisthesis Lumbar fusion
a b s t r a c t Sarcopenia, defined as decreased skeletal muscle mass or function, has recently been found to have increased perioperative morbidity and mortality. The relationship between sarcopenia and clinical outcomes in patients undergoing lumbar fusion has not been examined. This study investigates whether sarcopenia affects fusion rates and outcomes following single-level lumbar decompression and fusion. A retrospective analysis was undertaken of 97 consecutive patients who underwent a single level lumbar fusion for degenerative spondylolisthesis. Demographics, perioperative data, and patient reported clinical outcomes were collected. Measurements of paraspinal muscle CSA were made using a standardized protocol at the level of the L3-4 disc space on a preoperative lumbar MRI. Univariate analysis was used to compare cohorts with regards to demographics, comorbidities, and clinical outcomes. Of 97 patients, 16 patients (15.8%) were in the sarcopenic cohort utilizing a threshold of 986.1 mm2/m2. Reoperation rates were not significantly different between the two groups (0% vs 3.6%, p = .451). The sarcopenia cohort had lower BMI (28.1 vs 31.8, p = .017) and less male patients (6.3% vs 55.6%, p < .001). Mean follow-up was 18.3 months. There was no significant difference in postoperative Oswestry Disability Index (ODI) (24.7 vs 23.2, p = .794) Short Form 12 Physical (38.0 vs. 40.4, p = .445) Mental scores (55.5 vs. 53.6, p = .503), or visual analog scale (VAS) back pain scores (3.4 vs. 3.3, p = .818). No significant difference was found with regards to outcomes when comparing sarcopenic to non-sarcopenic patients undergoing lumbar fusion. Sarcopenia does not impact the clinical success of lumbar fusion for degenerative spondylolisthesis. Ó 2019 Elsevier Ltd. All rights reserved.
1. Introduction Lumbar paraspinal muscles are responsible for maintaining posture, spine mobility, and protecting the integrity of intervertebral discs, facet joints, and adjacent structures. Several studies have demonstrated the importance of lumbar paraspinal muscle cross-sectional surface area (CSA) and morphometry in predicting lumbago and disability [1–6]. Decreased paraspinal CSA and multifidus fat infiltration may occur as a normal aging process, result from underlying lumbar pathology, and contribute to structural pathology including low back pain [3,4,7]. Sarcopenia is defined as a progressive loss of skeletal muscle mass and function with resultant disability [8]. Sarcopenia, diagnosed by computerized tomography (CT) or magnetic resonance imaging (MRI) paraspinal or abdominal muscle CSA, may be a sign of malnutrition, limited mobility, and overall poor functional status. Low muscle mass is
⇑ Corresponding author at: Rothman Institute, 925 Chestnut St., 5th Floor, Philadelphia, PA 19107, USA. E-mail address: [email protected] (J.C. McKenzie). https://doi.org/10.1016/j.jocn.2019.03.015 0967-5868/Ó 2019 Elsevier Ltd. All rights reserved.
associated with several detrimental health effects including; increased fall risk, osteoporosis, morbidity, and increased mortality [9–11]. A recent retrospective study demonstrated increased 1-year mortality among elderly patients with sarcopenia suffering from orthopaedic pelvic trauma compared to a non-sarcopenic cohort [9]. In this study, there was no difference between the Charlson Comorbidity Index (CCI) or ASA (American Society of Anesthesiologists) Class in the sarcopenia and non sarcopenic groups, suggesting that sarcopenia may be an independent marker of overall frailty not accounted for by other risk stratification methods. Investigation into the relationship between generalized sarcopenia and clinical outcomes in patients undergoing spine surgery is limited. One retrospective study evaluated the association between sarcopenia and perioperative complications, including mortality, in 102 patients over the age of 65 undergoing elective thoracolumbar surgery for degenerative pathology. In this study, sarcopenia, defined by total axial psoas area at mid L3 level on preoperative CT, was not predictive of perioperative complications, length of stay, or in-hospital mortality in this group [12]. The
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authors concluded that sarcopenia, as measured by psoas cross sectional area, may not be an appropriate predictor of adverse events after elective spine procedures [12]. To our knowledge, there are no studies specifically evaluating the effect of sarcopenia on clinical and patient reported outcomes after lumbar fusion. The purpose of this study, therefore, was to determine the effects of sarcopenia on patient reported Health Related Quality of Life outcomes and clinical outcomes of patients undergoing single level lumbar decompression and fusion for degenerative spondylolisthesis, with the hypothesis that sarcopenia would adversely affect all outcome measures post-operatively.
2. Patients and methods After institutional review board (IRB) approval was obtained, a retrospective review of outpatient medical records was performed for patients with degenerative lumbar spondylolisthesis who underwent a single level posterior lumbar fusion. Patients were separated into Sarcopenia or Non-Sarcopenia cohorts based on individual measurement of the paraspinal muscle index, defined as the ratio between total paraspinal (iliocostalis, longissimus, multifidus, and psoas) muscle CSA and patient height squared. Patients who were one standard deviation below the average paraspinal muscle index, which was defined as 986.1 mm2/m2, were placed into the Sarcopenia cohort. The data were collected from seven surgeons between January and December 2014, with all procedures performed at a single institution. Pre-and postoperative patient-reported outcomes scores, including the Oswestry Disability Index (ODI), Short Form 12 Physical (SF-12 P), Short Form 12 Mental (SF-12 M) and back pain VAS scores, were included for analysis. Mean follow-up was 18.3 months. Demographic data, including age, BMI, smoking status, history of coronary artery disease and/or congestive heart failure, were also recorded. Inclusion criteria were any patient above the age of 18 at our institution diagnosed with degenerative lumbar spondylolisthesis, based on the ICD-9 code 721.42, with a preoperative lumbar spine MRI and completed preoperative patient-reported outcome scores. Patients under the age of 18 years, those lacking a preoperative lumbar spine MRI or completed preoperative patient-reported outcome scores, or those with a diagnosis other than degenerative lumbar spondylolisthesis (such as spinal cord injury, epidural hematoma or abscess, or metastatic disease) were excluded from the study. T1-weighted axial MRI images were evaluated independently by two reviewers, both blinded to their respective measurements. Using Sectra Liteview PACS Imaging measurement software, the CSA of the posterior paraspinal musculature (multifidus, iliocostalis, and longissimus), as well as the psoas CSA, were measured. The measurements were taken through the same axial cut at the midpoint of the L3-4 vertebral disc space (Fig. 1). To improve inter-observer reliability, the average of the two measurements was then recorded as the CSA for that muscle. Postoperative patient reported outcomes were collected from the latest postoperative outpatient visit. Incidence of reoperation, defined as any return to the operating room such as surgical site infection, wound dehiscence, hardware failure, or pseudarthrosis specific to the one-level lumbar fusion was also recorded. Due to its retrospective nature, some postoperative patient reported outcomes were not available for analysis. Four patients did not have any postoperative reported outcomes and were excluded from the study. Data analysis was performed using SPSS software (Version 22.0 IBM Armonk, NY). Categorical data were analyzed with the Chi Square Test and continuous data with the two-tailed Student
Fig. 1. Representative Cross Sectional MRI image at the L3-4 Disc Space showing the example of measuring the Cross Sectional Area (CSA) of the paralumbar musculature.
Sarcopenia Group Lumbar Level Fused
13%
6%
6%
L1-2 12%
L2-3 L3-4 L4-5 L5-S1
63%
Fig. 2. Pie Chart showing the Lumbar Levels Fused in the Sarcopenia Group. A majority of the Sarcopenia Group was fused at the L4-5 Lumbar Level.
t-test. Statistical significance was set with an alpha of 0.05 and power with a beta value of 0.80. The primary outcome was Health Related Quality of Life and clinical outcomes.
3. Results Ninety-seven medical records met inclusion criteria and were reviewed. Sixteen patients (15.8%) were identified as having sarcopenia utilizing a threshold of 986.1 mm2/m2. Eighty-one patients
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Non-Sarcopenia Group Lumbar Level Fused
15%
2%
L1-2
16%
L2-3 L3-4 L4-5 L5-S1 67%
Fig. 3. Pie chart showing the Lumbar level fused in the Non-Sarcopenia Group. Again, the most common level fused in the Lumbar spine is the L4-5 Level.
copenia and non-Sarcopenia group respectively (Figs. 2. and 3). Reoperation rates were not significantly different between the two groups (0% vs 3.6%, p = .530) (Table 1). With regards to ODI scores, there was no significant difference preoperatively (47.9 vs 46.6, p = .767), postoperatively (24.7 vs 23.2, p = .794), or in magnitude of change (23.4 vs 22.5, p = .877). SF-12 mental component scores showed no differences preoperatively (47.5 vs 46.6, p = .772), postoperatively (55.5 vs 53.6, p = .503), or in magnitude of change (6.9 vs 5.6, p = .732). SF-12 physical component scores also showed no difference preoperatively (28.9 vs 29.0, p = .973), postoperatively (38.0 vs 40.4, p = .445), or in magnitude of change (8.6 vs 10.0, p = .687). Similar findings were also found with regards to VAS back scores showing no significant differences preoperatively (7.4 vs 6.9, p = .451), postoperatively (3.4 vs 3.3, p = .878), or in magnitude of change (3.9 vs 3.2, p = .418) (Table 2) (Fig. 4).
4. Discussion Table 1 Patient Demographics.
N (%) Male Gender (%) ASA Class 3 (%) Mean Age [SD] Mean BMI [SD] Diabetes Mellitus (%) Smoking (%) Cardiac Disease (%) Reoperation (%)
Sarcopenia
Non-Sarcopenia
P value
16 (16.5%) 1 (6.3%) 2 (12.5%) 64.56 [16.943] 28.11 [4.456] 4 (25.0%) 3 (18.8%) 4 (25.0%) 0 (0%)
81 (83.5%) 45 (55.6%) 7 (8.4%) 61.58 [13.342] 31.80 [5.929] 9 (10.8%) 23 (30.1%) 13 (16.9%) 2 (3.6%)
NA <.001* .626 .219 .017* .145 .417 .395 .530
SD-Standard Deviation. * And bolded values are statistically significant (p < .05).
were included in the non-Sarcopenia group. The average time of lumbar spine MRI to outpatient evaluation was 3.6 months. The average postoperative score follow-up was 18.3 months. The Sarcopenia group had a lower mean BMI (28.11 vs. 31.8, p = .017) and less male patients (6.3% vs. 55.6%, p < .001) in comparison to the non-Sarcopenia group. There was no significant difference between the Sarcopenia and non-Sarcopenia group with regards to ASA class 3 (12.5% vs 8.4%, p = .626), smoking (18.8% vs 30.1% p = .417), diabetes mellitus (25% vs. 16.9%, p = .395) and heart disease (25% vs 16.9%, p = .395). There was no significant difference in lumbar level fused with 63% and 67% at L4-5 in the Sar-
In an aging population, the incidence of chronic LBP and degenerative lumbar disease is increasing [13,14]. One of the possible etiologies of chronic LBP and degenerative lumbar spondylolisthesis comes from the atrophy and fatty infiltration of paraspinal musculature, and has been shown to increase complications following injury, especially in acute trauma [9,15]. The atrophy of paraspinal musculature leads to worsening core balance, posture, and ambulatory dysfunction which places a significant mechanical disadvantage throughout the vertebral column. Paraspinal sarcopenia has been associated with osteoporotic lumbar vertebral fractures, which can also lead to degeneration of the lumbar spine and subsequent LBP and lower extremity radiculopathy [16]. Sarcopenia is an important comorbidity to assess and recognize when evaluating elderly patients with lumbar degeneration and LBP. Sarcopenia has been established as a risk factor for perioperative morbidity following thoracolumbar surgery. Bokshan et al assessed 46 patients for sarcopenia undergoing thoracolumbar spine surgery via L4 psoas muscle CSA on preoperative CT scan. 16 patients were sarcopenic and found to have 1.7 times longer hospital length of stay, threefold increase in perioperative complications including deep venous thrombosis and wound drainage, along with increased non-home discharge from the hospital [17]. Similarly, Zakaria et al. evaluated 395 patients undergoing posterior lumbar laminectomy, decompression and/or fusion and measured L4 psoas muscle CSA via MRI. Patients in the lowest third of psoas CSA were found to have increased risk of postoperative
Table 2 Patient Reported Outcome Scores.
Mean Mean Mean Mean Mean Mean Mean Mean Mean Mean Mean Mean
Preop ODI [SD] Postop ODI [SD] D ODI [SD] Preop SF-12 Mental [SD] Postop SF-12 Mental [SD] D SF-12 Mental [SD] Preop SF-12 Physical [SD] Postop SF-12 Physical [SD] D SF-12 Physical [SD] Preop VAS Back Pain [SD] Postop VAS Back Pain [SD] D VAS Back Pain [SD]
SD-Standard Deviation. D-‘‘Change In”. ODI-Oswestry Disability Index. VAS-Visual Analog Scale. SF-12-Short Form 12 Questionnaire.
Sarcopenia
Non-Sarcopenia
P value
47.9 [46.557] 24.7 [23.241] 23.4 [ 22.530] 47.5 [46.585] 55.5 [53.640] 6.9 [5.602] 28.9 [29.014] 38.0 [40.421] 8.6 [10.013] 7.4 [6.894] 3.4 [3.275] 3.9 [ 3.214]
46.6 [16.493] 23.2 [20.195] 22.5 [ 19.333] 46.6 [11.769] 53.6 [8.761] 5.6 [12.843] 29.0 [6.958] 40.4 [10.343] 10.0 [12.089] 6.9 [2.427] 3.3 [2.509] 3.2 [ 2.856]
.767 .794 .877 .772 .503 .732 .973 .445 .687 .451 .878 .418
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Sarcopenia versus Non-Sarcopenia Group Pre- and Postoperave Paent Reported Outcomes 70 60 50 40
30 20 10 0 -10
Preop ODI Postop ODIPreop SF12 Postop Preop SF12 Postop Preop VAS Postop VAS Mental SF12 Physical SF12 back pain back pain Mental Physical Sarcopenia Group
Non-Sarcopenia Group
Fig. 4. Bar Graph comparing the Sarcopenia Group and Non-Sarcopenia Group in pre and postoperative patient reported outcomes. None of the outcomes were significantly different between the two groups pre- or postoperatively.
complications including 30 and 90 day hospital readmission, DVT/ PE, and surgical site infection [18]. The goal of our study was to evaluate preoperative and postoperative patient-reported outcomes in lumbar fusion surgery for patients with sarcopenia. To our knowledge, this is the first study in the literature to specifically evaluate clinical outcomes both preoperatively and long term (>1 year) following spine fusion surgery. We found no difference in ODI, SF-12 physical or mental scores, or VAS back pain scores between the Sarcopenia and non-Sarcopenia groups either pre- or postoperatively. There was also no difference in reoperation rates for surgical site infection, pseudarthrosis, or hardware failure. It is important to note that both the Sarcopenia and non-Sarcopenia group had a similar improvement in all four patient-reported outcome scores at long term follow-up suggesting that sarcopenia does not impact overall recovery following lumbar fusion surgery. We did find a significant difference in gender and BMI between cohorts, with female patients with lower BMI more likely to have sarcopenia. Women tend to have a lower total muscle mass overall especially in comparison of elderly women versus their male counterparts, which can explain our finding [19]. Lower BMI has also been cited as a risk factor for sarcopenia in multiple studies [12,15]. It is unknown whether differences in baseline muscular morphology, hormonal changes with aging, or differential inflammatory responses lead to this gender discrepancy in sarcopenia, further study is needed. There is no standardized measurement or diagnosis of sarcopenia. Sarcopenia can be defined functionally based on hand-grip strength or quantitatively by evaluating the CSA via CT or MRI of lean muscle or skeletal muscle depending on the anatomic region being measured [20,21]. Our focus was on establishing a biomechanical measurement of paraspinal CSA via MRI which would likely have the best sensitivity of measuring muscular morphology. We also decided to use a paraspinal muscular index to evaluate all four paraspinal muscles as a unit and normalize for patient height. We chose our threshold of 986.1 mm2/m2 to strictly define sarcopenia within our study population as the lowest quartile of paraspinal muscular index and 1 standard deviation below the mean. The strengths of this study include pre- and postoperative patient-reported outcome scores with follow up beyond the imme-
diate postoperative period of 90 days. We utilized an established method of measuring the CSA of the paraspinal musculature and had two independent measurements of CSA that were averaged to reduce bias. The study cohorts had represented a general population of patients with prior advanced imaging who were seeking surgical consultation for lumbar spondylolisthesis. The limitations of this study include its retrospective nature, which can lead to potential collection, observer, and recall bias. Additionally, our study population is limited in size, particularly the sarcopenic cohort, but this was intentional based on our relatively strict definition of sarcopenia. There was a significant difference in BMI and female gender in the Sarcopenic cohorts, which could potentially affect outcomes, but likely represents a population likely to have sarcopenia. Lumbar spine MRIs were performed at separate locations with different machines, and this could potentially affect image quality and CSA measurements. However, all the imaging data were uploaded into our software system to standardize the measurement process and limit this weakness. Sarcopenia as defined by CSA of the paraspinal musculature may be an important risk factor for perioperative morbidity during thoracolumbar spine surgery. However, there was no long-term difference in patient-reported clinical outcomes or reoperation rates between patients with and without sarcopenia. Women with lower BMI are likely at higher risk for sarcopenia and further study is needed to best optimize these patients for lumbar surgery to limit perioperative morbidity, but may have equivocal outcomes at longer term clinical followup. Conflict of interest statement No funds were received in support of this work. The authors disclose no direct or indirect conflicts of interest in the preparation of this manuscript. No benefits in any form have been or will be received from a commercial party related directly or indirectly to the subject of this manuscript. Ethical board review statement This study was approved by the Institutional Review Board at Thomas Jefferson University Hospital. Each author certifies that
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