Abstract
Background:
Sarcopenia is a clinical syndrome of diminished muscle mass and function associated with disability, poor surgical outcomes, and mortality. Open fractures of the tibia and ankle have a high risk for complications including nonunion and surgical site infection (SSI). The purpose of this study is to determine if sarcopenia is associated with SSI and nonunion in individuals that sustain open fractures of the tibia and ankle.
Methods:
111 consecutive adults who underwent operative fixation of open fractures of the tibia or ankle from 2006-2017 with preoperative CT of the abdomen and pelvis were retrospectively identified at a single institution. Eleven patients were lost to follow-up. The psoas index (PI = (RPA+LPA)/ height2 (cm2/m2)) was calculated from bilateral psoas cross sectional areas measured on axial CT scans at the L3 pedicle. Patients were stratified by the presence of sarcopenia as defined by established gender specific PI cut-offs of <3.85 cm2/m2 (women) and <5.45 cm2/m2 (men). Records were also abstracted for comorbidities to determine a Charlson Comorbidity Index (CCI) score and postoperative complications including fracture nonunion and SSI. Logistic regression was used to model the relationships between complications, sarcopenia and other factors.
Results:
16/100 (16%) patients met gender specific criteria for the diagnosis of sarcopenia by PI. There was no difference in gender, age, or burden of medical comorbidity according to CCI between the sarcopenic and non-sarcopenic groups (all p>0.05). Nonunion occurred in 6 patients with sarcopenia (38%) and 12 without sarcopenia (18%) (Relative risk=2.42, 95%C!=1.08-5.43, p=0.0314). No association was found between sarcopenia and SSI, BMI, smoking status, ISS, and Gustilo and Anderson (GA) classification of open fracture (all p>0.2). GA classification was strongly associated with infection, with each successive classification having a nearly 3-fold increase in risk (p=0.0217).
Conclusion:
Sarcopenia is an independent risk factor for fracture nonunion following operative fixation of open tibia or ankle fracture, but is not predictive of surgical site infection. Gustilo Anderson classification is strongly associated with SSI risk. Psoas index is a straightforward and objective method of identifying sarcopenia in patients with open fractures. Diagnosing sarcopenia in these individuals can inform medical decision making and patient counseling regarding risk for nonunion. Further work is needed to identify effective interventions to improve outcomes in these patients.
Level of Evidence: III
Keywords: non-union, malnutrition, open fractures, psoas index, sarcopenia
Introduction
Sarcopenia is an age-related condition of diminished skeletal muscle mass and physical function,1 that leads to functional impairment secondary to decreased strength, slow gait speed, poor balance, and loss of independence in completing daily life activities.2,3 Sarcopenia is part of the clinical spectrum of frailty, and can be assessed by direct measurement of skeletal muscle mass, functional strength (i.e. handgrip dynamometry) or functional assessment (i.e. walking speed).1,4,5 Previous research has identified sarcopenia as an independent risk factor for adverse outcomes in critically-ill patients, trauma patients, transplant patients, and patients undergoing oncologic surgery.3,6-11
Within the realm of orthopaedics, assessment of sarcopenia-related outcomes has been limited to geriatric patients with fractures of the proximal femur or acetabulum. In this population, sarcopenia has been identified in one-fifth of patients and has been linked to increased fracture risk, prolonged hospitalization, and increased one-year mortality.6,12-18 There is a paucity of information on the relationship between sarcopenia and post-operative outcomes in patients following high energy orthopedic trauma. Fractures sustained during high energy trauma, particularly open fractures, are independently associated with an increased risk of surgical site infection and nonunion.19 The purpose of this study was to assess the association of sarcopenia with postoperative surgical site infection and fracture nonunion in a cohort of patients following operative fixation of acute open fractures of the tibia or ankle, and to evaluate the use of CT-measured muscle mass as a risk stratification tool within orthopaedic trauma.
Methods
Study Population
Surgical records were queried at a level I academic trauma center to identify individuals 18 years and older indicated for operative fixation of traumatic open fractures of the tibia and ankle between June 2006 and September 2017. Patients without preoperative computed tomography (CT) scan including the lumbar spine as part of their trauma work up were excluded. 111 patients met inclusion criteria. Eleven patients were lost to follow-up, leaving 100 patients in the final cohort. For each patient, demographics including age, sex, height, weight, body mass index (BMI, kg/m2), smoking status, and Charlson Comorbidity Index (CCI)20 were abstracted from electronic medical records.21 Fracture-specific variables including Gustilo-Anderson (GA) Open Fracture Classification and Injury Severity Score (ISS) were recorded.22,23 Primary outcomes assessed included postoperative fracture nonunion and surgical site infection. Fracture nonunion was defined as lack of bridging callus at least six months following treatment with clinical evidence such as pain or gross mobility at the fracture site. Surgical site infections were documented based upon the CDC definition of nosocomial surgical site infection.24
Measurement of Sarcopenia
Sarcopenia was assessed by measuring axial cross-sectional area of bilateral psoas muscles at the level of the L3 vertebral body (Figure 1). Psoas area (PA) was estimated as the product of the greatest anterior to posterior and transverse muscle diameters. The psoas index (PI) was calculated as the sum of the right (RPA) and left psoas area (LPA), followed by normalizing by the square of the patient’s height (PI = (RPA+LPA)/height2 in cm2/m2).15 Patients were classified as either sarcopenic or nonsarcopenic based on gender specific thresholds of 3.85 cm2/m2 for women and 5.45 cm2/m2 for men as established by an international consensus group on the diagnosis of cachexia in the presence of cancer.25
Figure 1.
Psoas muscle cross-sectional area measured at the level of L3 pedicle using freehand region of interest. To assess for sarcopenia, the Psoas Index is measured as the sum of right and left psoas areas, normalized by patient height (PI = (right psoas area+left psoas area)/height2 (cm2/m2). Sarcopenia was defined according to gender specific thresholds of PI ≤ 3.85 cm2/m2 for women and ≤ 5.45 cm2/m2 for men.
Statistical Analysis
Preoperative demographics were compared between sarcopenic and non-sarcopenic groups using chi-square or exact tests for categorical variables, as appropriate, and Wilcoxon Rank Sum tests for continuous variables. The relationships between demographics, sarcopenia, fracture characteristics, and postoperative SSI or nonunion were modeled with logistic regression. Analyses were completed using SAS statistical software version 9.4 (SAS Institute, Inc., Cary, NC) and a p-value <0.05 was considered statistically significant.
Results
Patient Characteristics
A total of 100 individuals (67% male) who underwent operative fixation for traumatic open fractures below the knee who received a preoperative CT scan as part of their trauma work up were identified. The average ISS at presentation was 19.9. The median follow-up time was 20 months (range 3 to 97 months). All patients with follow-up between three and six months had radiographic evidence of a healed fracture at the most recent clinic visit, except for one patient that underwent union surgery at three months for failed hardware (4-month total follow-up).
A total of 16 (16.0%) individuals met gender-specific criteria for sarcopenia. As shown in Table 1, the sarcopenic and non-sarcopenic groups were slightly older but did not significantly differ, respectively, in age (53.5 (22-73) vs 37 (18-90) yrs), BMI (26.7(18.9-43.9) vs 30.6 (18.8-51.5)kg/m2), CCI (1.5 (0-8) vs 0 (0-7)), GA Class (56.3% vs 47.6% class 3), gender distribution (62.5% vs 67.9% men), ISS (12 (4-38) vs 17 (4-50)) or smoking history (43.8% vs 33.3%) (all p>0.05).
Table 1.
General Patient Characteristics Within the Orthopaedic Trauma Cohort
| Total Cohort (n=100) | Sarcopenic by PI(n=16) | Nonsarcopenic by PI(n=84) | P value | |
|---|---|---|---|---|
| Age (years)** | 43.3 (17.4) | 53.5 (22-73) | 37 (18-90) | 0.056 |
| BMI (kg/m2)** | 30.2 (6.9) | 28.7 (7.3) | 30.5 (6.8) | 0.340 |
| Sex (no. male)+ | 67 (67%) | 10 (62.5%) | 57 (67.8%) | 0.676 |
| Current Smoker+ | 35 (35%) | 7 (43.8%) | 28 (33.3%) | 0.423 |
| ISS** | 19.86 (12.8) | 16.31 (10.6) | 20.54 (13.2) | 0.248 |
| GA* Class** | 2.41 (0.63) | 2.50 (0.61) | 2.39 (0.64) | 0.814 |
| CCI** | 86.6 (24.8) | 76.6 (34.3) | 88.5 (22.1) | 0.066 |
* Gustilo and Anderson
^ Psoas Index
** these values are given as the mean with standard deviation in parentheses
+ these values are given as number of patients with percentage in parentheses
Postoperative Outcomes
Within our cohort, 18 patients (18.0%) developed nonunion following surgical fixation. and 6 of those were sarcopenic (Table 2). A total of 19 patients (19.0%) developed post-operative SSI, and three of these patients were sarcopenic. Sarcopenia as determined by psoas index was associated with in increased risk of nonunion following operative fixation (Table 2). No association was noted between sarcopenia and the development of SSI post-operatively (Table 2). Other factors, including age, BMI, smoking history, gender, ISS, CCI, and GA class were evaluated for their potential relationship with nonunion or SSI (Table 3, Table 4). GA classification was strongly associated with infection, with each successive class having a nearly 3-fold increase in risk of developing postoperative SSI (p=0.0217).
Table 2.
Post-Operative Outcomes Between Sarcopenic and Nonsarcopenic Patients
| Total Cohort (n=100) | Sarcopenic by PI (n=16) | Nonsarcopenic by PI (n=84) | P value | |
|---|---|---|---|---|
| Nonunion+ | 18 (18%) | 6 (37.5%) | 12 (14.3%) | 0.0267* |
| SSI+ | 19 (19%) | 3 (18.8%) | 16 (19.0%) | 0.978 |
* indicates statistical significance below α = 0.05
+ these values are given as number of patients with percentage in parentheses
Table 3.
Relationship Between Nonunion and Other Variables
| Nonunion (n=18) | Union (n=82) | P value | |
|---|---|---|---|
| Age (years)** | 42.4 (17.0) | 43.4 (17.4) | 0.817 |
| BMI (kg/m2)** | 29.6 (5.97) | 30.3 (7.14) | 0.826 |
| Current Smoker+ | 7 (38.9%) | 28 (34.1%) | 0.852 |
| Sex (no. male)+ | 11 (61.1%) | 56 (68.3%) | 0.351 |
| ISS** | 15.8 (11.36) | 20.8 (12.9) | 0.137 |
| CCI** | 1.47 (2.21) | 1.15 (1.69) | 0.482 |
| GA Class** | 2.53 (0.60) | 2.38 (0.64) | 0.377 |
** these values are given as the mean with standard deviation in parentheses
+ these values are given as number of patients with percentage in parentheses
Table 4.
Relationship Between Surgical Sight Infection and Other Variables
| SSI (n=19) | No SSI (n=81) | P value | |
|---|---|---|---|
| Age** | 44.3 (16.0) | 43.1 (17.6) | 0.880 |
| BMI** | 33.1 (7.99) | 29.7 (6.53) | 0.101 |
| Current Smoker+ | 9 (47.4%) | 26 (32.1%) | 0.213 |
| Sex (no. male)+ | 11 (57.9%) | 56 (69.1%) | 0.351 |
| ISS** | 22.9 (13.5) | 19.1 (12.5) | 0.247 |
| CCI** | 1.42 (1.60) | 1.16 (1.85) | 0.573 |
| GA Class** | 2.74 (0.44) | 2.33 (0.65) | 0.017* |
* indicates statistical significance below α = 0.05
** these values are given as the mean with standard deviation in parentheses
+ these values are given as number of patients with percentage in parentheses
Relationship between Nonunion and Sarcopenia:
| sarcopenia | Nonunion | RR | 95% CI | p-value |
|---|---|---|---|---|
| Yes n=16 | 6 (37.5%) | 2.42 | 1.08-5.43 | 0.0314 |
| No N=84 | 12 (14.3%) | referent |
Relationship between SSI and Sarcopenia:
| sarcopenia | Infection | RR | 95% CI | p-value |
|---|---|---|---|---|
| Yes n=16 | 3 (18.8%) | 0.98 | 0.25-3.85 | 0.9778 |
| No N=84 | 16 (19.1%) | referent |
Univariate logistic regression:
| Variable | Estimate (beta) | SE | p-value |
|---|---|---|---|
| Age | -0.00344 | 0.0149 | 0.8171 |
| BMI | -0.00818 | 0.0372 | 0.8258 |
| Smoking History (yes vs no) | 0.0495 | 0.2649 | 0.8517 |
| Gender (female vs male) | 0.2441 | 0.2616 | 0.3508 |
| ISS | -0.0359 | 0.0241 | 0.1370 |
| CCI | 0.0919 | 0.1308 | 0.4822 |
| GA Class | 0.3771 | 0.4265 | 0.3766 |
Univariate logistic regression:
| Variable | Estimate (beta) | SE | p-value |
|---|---|---|---|
| Age | 0.00220 | 0.0146 | 0.8803 |
| BMI | 0.0588 | 0.0359 | 0.1014 |
| Smoking History (yes vs no) | 0.3219 | 0.2587 | 0.2134 |
| Gender (female vs male) | 0.2441 | 0.2616 | 0.3508 |
| ISS | 0.0218 | 0.0188 | 0.2471 |
| CCI | 0.0746 | 0.1323 | 0.5730 |
| GA Class | 1.2589 | 0.5276 | 0.0170 |
RR for GA class-SSI relationship: RR=2.80 (1.16-6.76), p=0.0217
Discussion
The relationship between sarcopenia and postoperative complications in the setting of traumatic open tibia and ankle fracture has not been studied. We report sarcopenia is an independent risk factor for fracture nonunion following open tibia or ankle fracture in adults. Sarcopenia is a marker of frailty characterized by decreasing muscle mass, and has been associated with loss of functionality, poor surgical outcomes, morbidity, and mortality following injury and surgical treatment.3,6,14 Psoas index has been established as a reliable tool for identifying patients with sarcopenia.6 Unlike other diagnostic methods, cross sectional imaging provides a timely and objective measure of skeletal muscle mass, and sarcopenia has repeatedly been associated with adverse patient outcomes in other patient populations. Commonly used risk stratification tools including serum chemistries and nutrition screening questionnaires have inconsistent prognostic value in this population due to large fluctuations following trauma. For these reasons, sarcopenia has been proposed as a risk stratification tool in patients undergoing surgery.15 Previous studies among emergency general surgery, organ transplantation, and oncologic surgery patients have validated its use for this purpose.3,6-12,15,19
Within orthopaedics, recovery from operative fixation for traumatic open fractures requires a significant physiologic reserve. Previous efforts to evaluate the association of sarcopenia with outcomes following orthopedic injury have been limited to elderly patients with fractures of the proximal femur and acetabulum.6,14 The reported prevalence of sarcopenia in these studies ranged from 25-42%, with both studies reporting increased one year mortality among patients with sarcopenia. There was a lower prevalence of sarcopenia in the current cohort, which is expected given the current patient cohort had a mean age of 43 years compared to 70 and 74 years.
With this relationship established, assessing for sarcopenia using PI may improve preoperative risk stratification, allow for improved patient counseling regarding risk of fracture nonunion, and allow for identification of interventions to improve postoperative complications in this population.
We did not observe a relationship between sarcopenia and increasing age. Established as an age-related condition, it appears that other factors may be linked to the development of sarcopenia and frailty. Santilli et. al identified physical disuse and inactivity, malnourishment, chronic inflammatory states, cachexia, and malignancy as processes that contribute to the development of sarcopenia, all of which are not exclusive to the elderly population.1 Within our study population, sarcopenia as established by PI was found in patients as young as 22 years of age.
Our study supports a bimodal distribution of sarcopenia in relation to patient BMI. The average BMI of sarcopenic patients was 28.8 kg/m. Among patients with sarcopenia, five patients were classified as obese (BMI > 30), one of which was morbidly obese (BMI > 40). Sarcopenic obesity represents a distinct process in which both entities are present. The relationship between sarcopenia and obesity is complex, with a continuum between fat accumulation and loss of skeletal muscle mass; sarcopenia reduces physical activity which in turn decreases energy expenditure and increases the risk of obesity.25 Although the traditional clinical picture of an elderly, frail individual is not incorrect, we must also consider the young, obese and inactive patient to be at risk for sarcopenia. These orthopaedic trauma patients should not be excluded from preoperative risk stratification even if they do not fit the traditional clinical picture of an elderly and frail patient. Failure to identify these individuals and address modifiable risk factors at the time of surgery may increase their risk of adverse outcomes post-operatively.
This study is limited by the retrospective nature and cohort size. Our analysis is also limited by the inability to further depict the degree of soft-tissue injury and contamination at the time of surgery.26 Further support of the relationship between sarcopenia and outcomes within this population may be necessary, and could be accomplished with a larger, multi-centered prospective study. In addition, our study is limited by the broad range of traumatic open fractures assessed within this cohort. The physiologic requirement necessary to recover from different fracture types likely varies. Future studies comparing outcomes amongst specific fracture types may help elucidate the relationship between sarcopenia and outcomes after open fractures independent of soft tissue injury and wound contamination.
We report sarcopenia, as measured by psoas index, is an independent risk factor for fracture nonunion following open fracture of the tibia or ankle. Psoas index calculations are readily available from cross sectional imaging routinely employed in trauma patients and allows orthopedic surgeons to more accurately counsel patients regarding risk of adverse outcomes associated with sarcopenia. Further studies are warranted to elucidate the relationship of sarcopenia with outcomes following orthopedic trauma and identify perioperative interventions to mitigate the increased risk associated with sarcopenia.
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