Sarcopenia is the loss of muscle mass associated with aging and advanced disease. In the nonhospitalized elderly population, sarcopenia has been independently associated with cognitive impairment, inability to perform activities of daily living, and limited community involvement.1 The condition occurs in up to 24% of patients in their 60s and is an independent predictor of hospital-acquired infection and all-cause mortality in hospitalized elderly patients.2–5
Sarcopenia increases institutionalization and health care demands. It has been estimated that a 10% reduction in the prevalence of sarcopenia could amount to health care cost savings of $1.1 billion per year in the United States.6 With Medicare spending for lumbar spine surgery dramatically increasing in the setting of an increasingly aging population, sarcopenia may be a useful clinical measure in the preoperative assessment of this patient population.7
Although sarcopenia has been identified as an independent predictor of mortality in patients undergoing organ transplants and those undergoing surgery for pancreatic and colorectal cancer, there is a dearth of evidence regarding the effect of sarcopenia on orthopedic surgical outcomes.8–12 In addition, sarcopenia is associated with osteoporosis and an increased risk of osteoporotic fractures, which are factors that may also compromise clinical outcomes following thoracolumbar spine surgery.13–16
In this investigation, the authors examined the correlation of sarcopenia with morbidity and mortality following thoracolumbar spinal surgery. They hypothesized that sarcopenia would be associated with an increase in postoperative complications, length of hospital stay, and overall mortality in thoracolumbar spine surgery patients.
Materials and Methods
After obtaining institutional review board approval, hospital records of 46 patients undergoing thoracolumbar decompression or decompression with fusion from 2003 to September 2015 were analyzed. The sample size was determined by the number of available patients with complete data. Patients were included if they were older than 55 years, if there was a perioperative computed tomography (CT) scan available for measuring psoas muscle cross-sectional area (performed an average of 4.3 months from date of surgery; range, 0–21.4 months), and if both inpatient and outpatient clinic follow-up data were available. No minimum follow-up time was required in an effort to include all instances of mortality, including those who died shortly following surgery. In addition, clinical follow-up data were cross-referenced with public death records to confirm all incidences of death up to December 2015. Patients were excluded if a CT scan had been performed greater than 2 years from the patient's surgery date or if the patient's postoperative clinical follow-up was unavailable, insufficient, or poorly documented. All thoracolumbar spine diagnoses and surgical indications were included.
Preoperative Charlson Comorbidity Index (CCI) was calculated for each patient and used to assess baseline comorbidity burden and health status.17 The CCI accounts for medical comorbidities including end organ disease (eg, end-stage renal disease) and presence of malignancy (localized and metastatic).
The Mirza Surgical Invasiveness Index was calculated for each procedure to account for surgical procedure variability on the patient.18 The Mirza Surgical Invasiveness Index was developed to rate spine surgical procedures based on the type and complexity of intervention involved in the procedure. This invasiveness index has been validated for spine procedures by its association with estimated blood loss (EBL) and operative time.18
Measurement of Sarcopenia
To assess sarcopenia, the cross-sectional areas of the left and right psoas muscles at the level of the transverse process of L4 were measured on axial CT scan (Figure 1) using OsiriX imaging software (Pixmeo, Geneva, Switzerland).11 This software is readily available online at no cost and has been shown to have high interrater reliability with reliability coefficients between 0.77 and 0.99.11 The cross-sectional areas were then summed to find the L4 total psoas area, a commonly used metric of sarcopenia in the surgical population.12 Patients falling into the lowest third for their sex-specific L4 total psoas area were deemed sarcopenic.
Measurement of L4 total psoas area for a sarcopenic psoas (left) and normal psoas (right).
The outcome variables assessed for each patient included the number of total postoperative complications classified according to the Clavien-Dindo system (Table 1), the length of hospital stay, and mortality. Additional outcome measures included the number of severe postoperative complications (defined as Clavien-Dindo grade IV or V) and the patient's disposition destination (skilled nursing facility, inpatient rehabilitation, or home).19
Clavien-Dindo System for Classifying Postoperative Complications
Student's t test was used to compare mean differences in length of hospital stay and number of complications for patients with sarcopenia vs those without. Differences in disposition were compared with chi-square testing. Analysis of variance (ANOVA) was used to measure differences across thirds. A Kaplan-Meier analysis along with log rank testing was used to measure differences in mortality over time. A P value of .05 was considered significant for all tests (SPSS version 21 statistical software package; IBM, Armonk, New York).
A total of 46 patients met the study inclusion criteria. Indications for surgery included spinal stenosis in 32 patients, degenerative scoliosis in 4, epidural abscess or diskitis in 5, acute fracture requiring operative fixation in 3, and radiculopathy in 2. Average follow-up time was 5.2 years (range, 6 days [died in hospital] to 12.7 years). Sixteen patients of 46 (8 men and 8 women) fell into the lowest third for L4 total psoas area (TSA) and were deemed sarcopenic (Table 2).
Patient Demographics Broken Down by L4 Total Psoas Area Thirds
Patients with sarcopenia were significantly older than those without sarcopenia, with a mean age of 76.4 vs 69.9 years, respectively (P=.01). There was no statistically significant difference in mean CCI (3.3 vs 2.0; P=.32) or mean Mirza Surgical Invasiveness Index (7.1 vs 7.0; P=.49) between patients with sarcopenia and those without (Table 3).
Demographics of Patients With Sarcopenia Versus Patients Without Sarcopenia
As shown in Table 4, mean length of stay for patients with sarcopenia was 1.7-fold longer than that for patients without sarcopenia (8.1 vs 4.7 days; P=.02). In addition, patients with sarcopenia had a 3-fold increase in the mean number of total complications (1.2 vs 0.4; P=.02) and a 10-fold increase in major complications (0.3 vs 0.03; P=.04) vs patients without sarcopenia. Five of the 6 major complications in this cohort occurred in patients with sarcopenia. Patients with sarcopenia were also more likely to be discharged to a skilled nursing facility or inpatient rehabilitation facility (81.2% vs 43.3%; P=.006).
Postoperative Morbidity in Patients With Sarcopenia
Patients with sarcopenia had a significantly lower cumulative survival over time when compared with patients without sarcopenia (log rank=0.007) (Figure 2). All 4 patients in this cohort who died following surgery had sarcopenia.
Kaplan-Meier curve showing a significantly lower postoperative survival (log rank=0.007) for patients with sarcopenia (red) vs patients without sarcopenia (blue).
Sarcopenia has previously been shown to be a predictor of complications and mortality in patients undergoing emergency general surgery, surgical oncology, and organ transplant.9–12 To the current authors' knowledge, this study is the first to demonstrate a correlation between sarcopenia and postoperative morbidity and mortality following spinal surgery. Despite having nonstatistically different comorbidity and surgical invasiveness scores, patients with sarcopenia patients had 1.7-fold longer hospital stays and a 3-fold higher complication rate compared with patients without sarcopenia.
These findings are particularly salient given the pervasiveness of sarcopenia among orthopedic patients. A cross-sectional study by Ji et al20 examining patients undergoing hip fracture surgery and joint arthroplasty reported a 44.1% rate of sarcopenia in the orthopedic patient population compared with a 33.2% rate in control patients in an outpatient department. In a study by Hida et al16 comparing skeletal muscle mass in patients with osteoporotic vertebral fracture vs those without, sarcopenia was an independent risk factor for osteoporotic vertebral fracture. Although both of these studies suggest that sarcopenia may be an important consideration in patients undergoing orthopedic surgery, neither study assessed patient outcomes.
In the current study, the authors found that sarcopenia had a poorer cumulative survival over time, with all 4 deaths in the study occurring among patients with sarcopenia. Furthermore, in the small study population, 5 of the 6 major complications occurred in patients with sarcopenia. These findings are similar to those previously reported for patients undergoing surgery in general fields.7–12
This study had several potential limitations. The relatively small sample size of the study population is a potential limitation, and larger prospective investigations will be needed to further assess the usefulness of sarcopenia in predicting outcomes following thoracolumbar spine surgery. In addition, this study includes several preoperative indications for undergoing thoracolumbar decompression and possible fusion. Although it is possible that this introduced additional variability to the study, this list of indications was collected as a representative sample of cases performed at a large tertiary center and is therefore reflective of a spine practice in an academic setting.
An additional potential limitation is that only L4 psoas area was used to define sarcopenia, although there are numerous other methods currently used to assess sarcopenia in clinical research. Researchers have used Hounsfield units to assess psoas density, quadriceps area, dual energy X-ray absorptiometry (DEXA), and bioelectrical impedance analysis to assess muscle amount and quality. However, DEXA and bioelectrical impedance analysis are less specific for sarcopenia than measurements of cross-sectional area.21–23 In addition, measures of muscle strength (eg, handgrip, knee flexion/extension, and peak expiratory flow) and physical performance (eg, Short Physical Performance Battery, gait speed, timed get-up-and-go test, and the stair-climb power test) have also been evaluated but are not possible to assess retrospectively, and furthermore may be inaccurate measures in patients undergoing spinal surgery due to neurological compression and spinal malalignment.23–46 Currently, no single definition of sarcopenia has been shown to be most clinically useful, and additional studies to compare these methods are required. The current authors chose total psoas area in an effort to assess a clinically relevant and potentially clinically useful measure. Spine surgeons with access to preoperative CT and magnetic resonance imaging scans can measure psoas area, which may help in preoperative assessment of risk.
The results of this study indicate that sarcopenia may be an important consideration in patient selection for thoracolumbar spine surgery. Identifying patients at higher risk for poor outcomes could aid both physicians and patients in decision making. Screening for sarcopenia may be a useful tool in determining which patients are at high risk of morbidity and mortality following spinal surgery. This form of preoperative assessment could potentially conserve valuable health care system resources by reducing complications and readmissions. Further prospective investigation is needed to assess sarcopenia as a novel method of predicting morbidity and mortality in patients undergoing spinal surgery.
- Chan OY, van Houwelingen AH, Gussekloo J, Blom JW, den Elzen WP. Comparison of quadriceps strength and handgrip strength in their association with health outcomes in older adults in primary care. Age (Dordr). 2014; 36(5):9714. doi:10.1007/s11357-014-9714-4 [CrossRef]
- Grimby G, Saltin B. The ageing muscle. Clin Physiol. 1983; 3(3):209–218. doi:10.1111/j.1475-097X.1983.tb00704.x [CrossRef]
- Baumgartner RN, Koehler KM, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998; 147(8):755–763. doi:10.1093/oxfordjournals.aje.a009520 [CrossRef]
- Cosquéric G, Sebag A, Ducolombier C, Thomas C, Piette F, Weill-Engerer S. Sarcopenia is predictive of nosocomial infection in care of the elderly. Br J Nutr. 2006; 96(5):895–901. doi:10.1017/BJN20061943 [CrossRef]
- Batsis JA, Mackenzie TA, Barre LK, Lopez-Jimenez F, Bartels SJ. Sarcopenia, sarcopenic obesity and mortality in older adults: results from the National Health and Nutrition Examination Survey III. Eur J Clin Nutr. 2014; 68(9):1001–1007. doi:10.1038/ejcn.2014.117 [CrossRef]
- Janssen I, Shepard DS, Katzmarzyk PT, Roubenoff R. The healthcare costs of sarcopenia in the United States. J Am Geriatr Soc. 2004; 52(1):80–85. doi:10.1111/j.1532-5415.2004.52014.x [CrossRef]
- Weinstein JN, Lurie JD, Olson PR, Bronner KK, Fisher ES. United States' trends and regional variations in lumbar spine surgery: 1992–2003. Spine (Phila Pa 1976). 2006; 31(23):2707–2714. doi:10.1097/01.brs.0000248132.15231.fe [CrossRef]
- Friedman J, Lussiez A, Sullivan J, Wang S, Englesbe M. Implications of sarcopenia in major surgery. Nutr Clin Pract. 2015; 30(2):175–179. doi:10.1177/0884533615569888 [CrossRef]
- Du Y, Karvellas CJ, Baracos V, Williams DC, Khadaroo RGAcute Care and Emergency Surgery (ACES) Group. Sarcopenia is a predictor of outcomes in very elderly patients undergoing emergency surgery. Surgery. 2014; 156(3):521–527. doi:10.1016/j.surg.2014.04.027 [CrossRef]
- Reisinger KW, van Vugt JL, Tegels JJ, et al. Functional compromise reflected by sarcopenia, frailty, and nutritional depletion predicts adverse postoperative outcome after colorectal cancer surgery. Ann Surg. 2015; 261(2):345–352. doi:10.1097/SLA.0000000000000628 [CrossRef]
- Fortin M, Battié M. Quantitative paraspinal muscle measurements: inter-software reliability and agreement using OsiriX and ImageJ. Phys Ther. 2012; 92(6):853–864. doi:10.2522/ptj.20110380 [CrossRef]
- Englesbe MJ, Patel SP, He K, et al. Sarcopenia and mortality after liver transplantation. J Am Coll Surg. 2010; 211(2):271–278. doi:10.1016/j.jamcollsurg.2010.03.039 [CrossRef]
- Evans WJ, Campbell WW. Sarcopenia and age-related changes in body composition and functional capacity. J Nutr. 1993; 123(2 suppl):465–468.
- Landi F, Liperoti R, Russo A, et al. Sarcopenia as a risk factor for falls in elderly individuals: results from the ilSIRENTE study. Clin Nutr. 2012; 31(5):652–658. doi:10.1016/j.clnu.2012.02.007 [CrossRef]
- Kelly TL, Wilson KE, Heymsfield SB. Dual energy x-ray absorptiometry body composition reference values from NHANES. PLoS One. 2009; 4(9):e7038. doi:10.1371/journal.pone.0007038 [CrossRef]
- Hida T, Shimokata H, Sakai Y, et al. Sarcopenia and sarcopenic leg as potential risk factors for acute osteoporotic vertebral fracture among older women [published online ahead of print February 18, 2015]. Eur Spine J. doi:10.1007/s00586-015-3805-5 [CrossRef]
- Charlson ME, Pompei P, Ales KL, MacKenzie CR. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis.1987; 40(5):373–383. doi:10.1016/0021-9681(87)90171-8 [CrossRef]
- Mirza SK, Deyo RA, Heagerty PJ, et al. Development of an index to characterize the “invasiveness” of spine surgery: validation by comparison to blood loss and operative time. Spine (Phila Pa 1976). 2008; 33(24):2651–2661. doi:10.1097/BRS.0b013e31818dad07 [CrossRef]
- Clavien PA, Barkun J, de Oliveira ML, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg. 2009; 250(2):187–196. doi:10.1097/SLA.0b013e3181b13ca2 [CrossRef]
- Ji HM, Won YY, Kang BM, Park YS, Han MH. Sarcopenia in patients scheduled to undergo orthopaedic surgery. Poster presented at: European Calcified Tissue Society Congress 2014. ; May 17–20, 2014. ; Prague, Czech Republic. .
- Pahor M, Manini T, Cesari M. Sarcopenia: clinical evaluation, biological markers and other evaluation tools. J Nutr Health Aging. 2009; 13(8):724–728. doi:10.1007/s12603-009-0204-9 [CrossRef]
- Rajaee SS, Bae HW, Kanim LE, Delamarter RB. Spinal fusion in the United States: analysis of trends from 1998 to 2008. Spine (Phila Pa 1976). 2012; 37(1):67–76. doi:10.1097/BRS.0b013e31820cccfb [CrossRef]
- Lauretani F, Russo CR, Bandinelli S, et al. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol (1985). 2003; 95(5):1851–1860. doi:10.1152/japplphysiol.00246.2003 [CrossRef]
- Bean JF, Kiely DK, Herman S, et al. The relationship between leg power and physical performance in mobility-limited older people. J Am Geriatr Soc. 2002; 50(3):461–467. doi:10.1046/j.1532-5415.2002.50111.x [CrossRef]
- Suzuki T, Bean JF, Fielding RA. Muscle power of the ankle flexors predicts functional performance in community-dwelling older women. J Am Geriatr Soc. 2001; 49(9):1161–1167. doi:10.1046/j.1532-5415.2001.49232.x [CrossRef]
- Foldvari M, Clark M, Laviolette LC, et al. Association of muscle power with functional status in community-dwelling elderly women. J Gerontol A Biol Sci Med Sci. 2000; 55(4):M192–M199. doi:10.1093/gerona/55.4.M192 [CrossRef]
- Bassey EJ, Short AH. A new method for measuring power output in a single leg extension: feasibility, reliability and validity. Eur J Appl Physiol Occup Physiol. 1990; 60(5):385–390. doi:10.1007/BF00713504 [CrossRef]
- Edwards RH, Young A, Hosking GP, Jones DA. Human skeletal muscle function: description of tests and normal values. Clin Sci Mol Med. 1977; 52(3):283–290.
- Feiring DC, Ellenbecker TS, Derscheid GL. Test-retest reliability of the Biodex isokinetic dynamometer. J Orthop Sports Phys Ther. 1990; 11(7):298–300. doi:10.2519/jospt.19220.127.116.118 [CrossRef]
- Hartmann A, Knols R, Murer K, de Bruin ED. Reproducibility of an isokinetic strength-testing protocol of the knee and ankle in older adults. Gerontology. 2009; 55(3):259–268. doi:10.1159/000172832 [CrossRef]
- Brown M, Sinacore DR, Binder EF, Kohrt WM. Physical and performance measures for the identification of mild to moderate frailty. J Gerontol A Biol Sci Med Sci. 2000; 55(6):M350–M355. doi:10.1093/gerona/55.6.M350 [CrossRef]
- Callahan D, Phillips E, Carabello R, Frontera WR, Fielding RA. Assessment of lower extremity muscle power in functionally-limited elders. Aging Clin Exp Res. 2007; 19(3):194–199. doi:10.1007/BF03324689 [CrossRef]
- Neder JA, Nery LE, Shinzato GT, Andrade MS, Peres C, Silva AC. Reference values for concentric knee isokinetic strength and power in nonathletic men and women from 20 to 80 years old. J Orthop Sports Phys Ther. 1999; 29(2):116–126. doi:10.2519/jospt.1918.104.22.168 [CrossRef]
- Goodpaster BH, Carlson CL, Visser M, et al. Attenuation of skeletal muscle and strength in the elderly: the Health ABC Study. J Appl Physiol (1985). 2001; 90(6):2157–2165.
- Newman AB, Haggerty CL, Goodpaster B, et al. Health Aging And Body Composition Research Group. Strength and muscle quality in a well-functioning cohort of older adults: the Health, Aging and Body Composition Study. J Am Geriatr Soc. 2003; 51(3):323–330. doi:10.1046/j.1532-5415.2003.51105.x [CrossRef]
- Chen HI, Kuo CS. Relationship between respiratory muscle function and age, sex, and other factors. J Appl Physiol (1985). 1989; 66(2):943–948.
- Kim J, Davenport P, Sapienza C. Effect of expiratory muscle strength training on elderly cough function. Arch Gerontol Geriatr. 2009; 48(3):361–366. doi:10.1016/j.archger.2008.03.006 [CrossRef]
- Working Group on Functional Outcome Measures for Clinical Trials. Functional outcomes for clinical trials in frail older persons: time to be moving. J Gerontol A Biol Sci Med Sci. 2008; 63(2):160–164. doi:10.1093/gerona/63.2.160 [CrossRef]
- Guralnik JM, Simonsick EM, Ferrucci L, et al. A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol. 1994; 49(2):M85–M94. doi:10.1093/geronj/49.2.M85 [CrossRef]
- Perera S, Mody SH, Woodman RC, Studenski SA. Meaningful change and responsiveness in common physical performance measures in older adults. J Am Geriatr Soc. 2006; 54(5):743–749. doi:10.1111/j.1532-5415.2006.00701.x [CrossRef]
- Kwon S, Perera S, Pahor M, et al. What is a meaningful change in physical performance? Findings from a clinical trial in older adults (the LIFE-P study). J Nutr Health Aging. 2009; 13(6):538–544. doi:10.1007/s12603-009-0104-z [CrossRef]
- Buchner DM, Larson EB, Wagner EH, Koepsell TD, de Lateur BJ. Evidence for a nonlinear relationship between leg strength and gait speed. Age Ageing. 1996; 25(5):386–391. doi:10.1093/ageing/25.5.386 [CrossRef]
- Guralnik JM, Ferrucci L, Pieper CF, et al. Lower extremity function and subsequent disability: consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery. J Gerontol A Biol Sci Med Sci. 2000; 55(4):M221–M231. doi:10.1093/gerona/55.4.M221 [CrossRef]
- Cesari M, Kritchevsky SB, Newman AB, et al. Added value of physical performance measures in predicting adverse health-related events: results from the Health, Aging and Body Composition Study. J Am Geriatr Soc. 2009; 57(2):251–259. doi:10.1111/j.1532-5415.2008.02126.x [CrossRef]
- Mathias S, Nayak US, Isaacs B. Balance in elderly patients: the “get-up and go” test. Arch Phys Med Rehabil. 1986; 67(6):387–389.
- Bean JF, Kiely DK, LaRose S, Alian J, Frontera WR. Is stair climb power a clinically relevant measure of leg power impairments in at-risk older adults?Arch Phys Med Rehabil. 2007; 88(5):604–609. doi:10.1016/j.apmr.2007.02.004 [CrossRef]
Clavien-Dindo System for Classifying Postoperative Complicationsa
|1||Any deviation from standard postoperative care without the need for pharmacologic, surgical, endoscopic, or radiological intervention; surgical wound debridement at the bedside|
|2||Complication requiring nonstandard pharmacological intervention, blood products, or total parenteral nutrition|
|3||Complication requiring surgical, endoscopic, or radiologic intervention|
|4||Multi-organ dysfunction; requirement of intensive care unit level of care; dialysis|
Patient Demographics Broken Down by L4 Total Psoas Area Thirds
|Demographic||Lowest Third (Sarcopenic)||Middle Third||Highest Third||P|
|Age, mean±SEM, y||76.4±2.2||69.8±2.5||70.1±1.4||.04|
|L4 total psoas area, mean±SEM, mm2||1477.1±147.7||1936.5±152.0||2635.1±202.1||<.001|
|Preoperative diagnosis, No.|
| Spinal stenosis||11||11||10|
| Degenerative scoliosis||0||2||2|
| Epidural abscess/diskitis||2||1||2|
| Acute fracture||2||0||1|
|Charlson Comorbidity Index, mean±SEM||3.3±0.8||2.8±0.5||2.9±0.4||.85|
|Surgical Invasiveness Index, mean±SEM||7.1±1.6||5.9±1.4||8.1±1.3||.59|
Demographics of Patients With Sarcopenia Versus Patients Without Sarcopenia
|Age, mean±SEM, y||76.4±2.2||69.9±2.0||.01|
|L4 total psoas area, mean±SEM, mm2||1477.1±147.7||2285.8±198.2||<.001|
|Charlson Comorbidity Index, mean±SEM||3.3±0.8||2.0±0.4||.32|
|Surgical Invasiveness Index, mean±SEM||7.1±1.6||7.0±1.4||.49|
Postoperative Morbidity in Patients With Sarcopenia
|Patient Outcome||Sarcopenia||No Sarcopenia||P|
|Length of hospital stay, mean±SEM, d||8.1±1.5||4.7±0.9||.02|
|Total postoperative complications, mean±SEM, No.||1.2±0.3||0.4±0.2||.02|
|Major postoperative complications, mean±SEM, No.||0.3±0.2||0.03±0.1||.04|
|Discharged to skilled nursing or rehabilitation facility||81.2%||43.3%||.006|