Factors affecting the prognosis of recovery of motor power and ambulatory function after surgery for metastatic epidural spinal cord compression

Sehan ParkDepartment of Orthopedic Surgery, Dongguk University Ilsan Hospital, Goyang-si;

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Jae Woo ParkDepartment of Orthopedic Surgery, Gangneung Asan Hospital, University of Ulsan College of Medicine, Gangneung-si; and

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Jin Hoon ParkDepartments of Neurosurgery and

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Choon Sung LeeOrthopedic Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea

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Dong-Ho LeeOrthopedic Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea

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Chang Ju HwangOrthopedic Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea

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Jae Jun YangDepartment of Orthopedic Surgery, Dongguk University Ilsan Hospital, Goyang-si;

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Jae Hwan ChoOrthopedic Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea

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OBJECTIVE

Metastatic epidural spinal cord compression (MESCC) causes neurological deficits that may hinder ambulation. Understanding the prognostic factors associated with increased neurological recovery and regaining ambulatory functions is important for surgical planning in MESCC patients with neurological deficits. The present study was conducted to elucidate prognostic factors of neurological recovery in MESCC patients.

METHODS

A total of 192 patients who had surgery for MESCC due to preoperative neurological deficits were reviewed. A motor recovery rate ≥ 50% and ambulatory function restoration were defined as the primary favorable endpoints. Factors associated with a motor recovery rate ≥ 50%, regaining ambulatory function, and patient survival were analyzed.

RESULTS

About one-half (48.4%) of the patients had a motor recovery rate ≥ 50%, and 24.4% of patients who were not able to walk due to MESCC before the surgery were able to walk after the operation. The factors “involvement of the thoracic spine” (p = 0.015) and “delayed operation” (p = 0.041) were associated with poor neurological recovery. Low preoperative muscle function grade was associated with a low likelihood of regaining ambulatory functions (p = 0.002). Furthermore, performing the operation ≥ 72 hours after the onset of the neurological deficit significantly decreased the likelihood of regaining ambulatory functions (p = 0.020). Postoperative ambulatory function significantly improved patient survival (p = 0.048).

CONCLUSIONS

Delayed operation and the involvement of the thoracic spine were poor prognostic factors for neurological recovery after MESCC surgery. Furthermore, a more severe preoperative neurological deficit was associated with a lesser likelihood of regaining ambulatory functions postoperatively. Earlier detection of motor weaknesses and expeditious surgical interventions are necessary, not only to improve patient functional status and quality of life but also to enhance survival.

ABBREVIATIONS

AIS = ASIA Impairment Scale; ASIA = American Spinal Injury Association; KPS = Karnofsky Performance Status; MESCC = metastatic epidural spinal cord compression; RT = radiation therapy; SINS = Spine Instability Neoplastic Score.

OBJECTIVE

Metastatic epidural spinal cord compression (MESCC) causes neurological deficits that may hinder ambulation. Understanding the prognostic factors associated with increased neurological recovery and regaining ambulatory functions is important for surgical planning in MESCC patients with neurological deficits. The present study was conducted to elucidate prognostic factors of neurological recovery in MESCC patients.

METHODS

A total of 192 patients who had surgery for MESCC due to preoperative neurological deficits were reviewed. A motor recovery rate ≥ 50% and ambulatory function restoration were defined as the primary favorable endpoints. Factors associated with a motor recovery rate ≥ 50%, regaining ambulatory function, and patient survival were analyzed.

RESULTS

About one-half (48.4%) of the patients had a motor recovery rate ≥ 50%, and 24.4% of patients who were not able to walk due to MESCC before the surgery were able to walk after the operation. The factors “involvement of the thoracic spine” (p = 0.015) and “delayed operation” (p = 0.041) were associated with poor neurological recovery. Low preoperative muscle function grade was associated with a low likelihood of regaining ambulatory functions (p = 0.002). Furthermore, performing the operation ≥ 72 hours after the onset of the neurological deficit significantly decreased the likelihood of regaining ambulatory functions (p = 0.020). Postoperative ambulatory function significantly improved patient survival (p = 0.048).

CONCLUSIONS

Delayed operation and the involvement of the thoracic spine were poor prognostic factors for neurological recovery after MESCC surgery. Furthermore, a more severe preoperative neurological deficit was associated with a lesser likelihood of regaining ambulatory functions postoperatively. Earlier detection of motor weaknesses and expeditious surgical interventions are necessary, not only to improve patient functional status and quality of life but also to enhance survival.

Metastatic epidural spinal cord compression (MESCC) can cause neurological deficits that may significantly adversely affect patient quality of life and survival.1,2 It is estimated that MESCC occurs in 5%–10% of cancer patients, with breast, prostate, and lung cancers being the most frequent primary cancers.3,4 Because of recent advances in systemic medical therapy, life expectancy is increasing for patients with multiple metastatic cancer. However, active management is required for MESCC patients to benefit from these treatments.1 Although the role of radiation therapy (RT) has been emphasized in the treatment of MESCC, patients with established neurological deficits frequently require surgical decompression to preserve motor and ambulatory functions.57 Maintaining patient ambulation is also a prerequisite for further systemic therapy, further supporting the importance of preservation and restoration of neurological functions.8,9

Despite the importance of early surgical intervention, making the decision of whether or not to perform surgery in MESCC patients is often challenging.7 Most of these patients are elderly and have multiple comorbidities and short life expectancies.10 In addition, MESCC surgery is often associated with more morbidities than degenerative spine disease surgery because of the greater extent of resection required and higher amounts of bleeding in MESCC patients.1013 Critical complications may occur in this vulnerable patient group and adversely affect patient survival.11,14,15 Although previous studies have demonstrated the positive impact (regarding neurological function and performance status) of decompressive surgeries in MESCC patients,16,17 in other reported studies MESCC surgery in patients aged > 65 years was not beneficial with respect to regain of ambulatory function.18,19 Because not all patients fully recover from their neurological deficits (even after surgery), knowing the prognostic factors for the recovery of ambulatory functions is important when planning surgery. Risks and benefits should be carefully weighed and expected prognoses thoroughly assessed before MESCC surgery is performed.8,9 Therefore, the present study was conducted to evaluate the surgical prognosis of MESCC patients with neurological deficits and elucidate the factors associated with patient survival and recovery of motor power and ambulatory functions.

Methods

Study Design and Patient Characteristics

This retrospective study was approved by the Asan Medical Center Institutional Review Board. Informed consent was waived due to the retrospective nature of the study. This study was designed and reported in accordance with the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement for cohort studies. A total of 332 patients who underwent surgery for metastatic spine cancer between March 2014 and January 2020 were retrospectively reviewed. Patients who had epidural spinal cord compression with a Bilsky grade20 of 2 or 3 and who demonstrated preoperative neurological deficits (American Spinal Injury Association [ASIA]21 Impairment Scale [AIS] grade D or worse) were included. Patients who were without neurological deficits or were operated on because of axial pain were excluded.

The decision to operate was based on a consensus between medical oncologists and spine surgeons and took into consideration factors such as patient life expectancy, performance, symptoms, and future systemic treatment plans. Although some cases were discussed in a multidisciplinary consultation forum involving medical oncologists, radiation oncologists, general surgeons, and spine surgeons, many cases could not be discussed in this forum given that all patients had preoperative neurological deficits that required urgent interventions. Operations were performed by three spine surgeons (J.H.C., J.W.P., and J.H.P.). The surgical strategies were individualized and were based on patient general health status, location of metastasis, and spread of the tumor (Figs. 1 and 2). Patients who were able to walk despite their neurological deficits, including those who were able to walk only with the help of walking sticks or walkers, were classified as the ambulatory group, and patients who were unable to walk were classified as the nonambulatory group.

FIG. 1.
FIG. 1.

Illustrative case 1. A 60-year-old female patient visited the emergency department due to lower-extremity weakness. Her initial motor grade was assessed as grade 4 at the hip flexor and knee extensor muscles bilaterally, and she was not able to walk. A: Preoperative gadolinium-enhanced MR image revealing a circumferential mass at T10. B: Axial MR image showing epidural cord compression by the mass. C and D: Emergency posterior T7–L1 decompression and instrumentation and T10 corpectomy were performed. The mass was later identified to be a metastasis of breast cancer. She completely recovered from the neurological deficit 1 week after surgery and was able to ambulate without support.

FIG. 2.
FIG. 2.

Illustrative case 2. A 40-year-old female patient with a history of breast cancer visited the emergency department due to lower-extremity weakness and severe back pain. Her initial motor grade was assessed as grade 3 throughout the bilateral lower extremities. A: Preoperative sagittal MR image demonstrating pathologic compression and cord compression by a metastatic mass at T9. B: Axial MR image showing significant spinal cord compression by an epidural mass. C: Separation surgery was performed by laminectomy and tumor removal. T7–11 pedicle screw fixation was also performed. D: Postoperative RT was performed considering the separation surgery. At 1 month after surgery the patient’s motor function was restored to AIS grade 3.

Variables

Demographic factors, operative methods, Bilsky grades, Spine Instability Neoplastic Score (SINS),22 Karnofsky Performance Status (KPS) score, pre- and postoperative motor function grades, pre- and postoperative ambulatory functions, and survival periods of the patients were recorded. The assessment of ambulatory function status considered was that performed 3 months after the operation or, for patients who did not survive for more than 3 months after the surgery, during the last follow-up.

Motor power (function) was assessed using the AIS scale (graded from 0 to 5). Every key muscle of the lower extremity defined in the AIS scale was examined, and the best motor function preserved was used for analysis. For example, when the right hip flexor was assessed as grade 3 and the remaining muscles were assessed as grade 2, the motor power grade considered for that patient was grade 3. The motor recovery rate was defined as [(postoperative muscle function grade – preoperative muscle function grade)/(5 – preoperative muscle function grade)] × 100 (%). Good functional recovery was defined as a motor recovery rate ≥ 50%.

Statistical Analyses

Comparisons were performed between the preoperative ambulatory and nonambulatory groups. All variables were tested for normality using the Shapiro-Wilk test. Continuous variables were analyzed using the Student t-test and categorical variables using the chi-square test. Factors correlated with good functional recovery and recovery of ambulatory function (in the preoperative nonambulatory group) were analyzed with logistic regression analysis. Additional subgroup analyses were performed to further verify factors associated with good functional recovery and recovery of ambulatory functions. Kaplan-Meier analysis was used to visualize and compare patient survival across subgroups. Age (≥ 60 vs < 60 years), time between the onset of neurological deficits and operation (≥ 72 vs < 72 hours), local recurrence, preoperative KPS score (≥ 70 vs < 70), and pre- and postoperative ambulatory functions were evaluated in the survival analyses. Cox regression analysis was used to evaluate the hazard ratio (HR). Statistical analysis was performed using IBM SPSS version 21.0.0 (IBM Corp.); p values < 0.05 were considered statistically significant.

Results

Patient Characteristics

The study included 192 patients who met the inclusion criteria. In the ambulatory group, we had 106 patients (55.2%) (mean age 58.5 ± 12.7 years, male/female ratio 76:30), while 86 patients (44.8%) were included in the nonambulatory group (mean age 58.4 ± 12.7, male/female ratio 50:36). Lung cancer was the most common primary etiology in both groups (16.0% and 22.1%, respectively). The preoperative muscle function grade and preoperative KPS score (both p < 0.001) were significantly higher in the ambulatory group compared with the nonambulatory group. Muscle function grade significantly improved after the operation in both groups (both p < 0.001), and postoperative muscle function grade was significantly higher in the ambulatory group (4.2 ± 1.0 vs 3.2 ± 1.3; p < 0.001) (Fig. 3A). In the ambulatory group, 92.5% (98/106) of the patients retained their ambulatory function postoperatively. However, 8 patients (7.5%) were no longer able to walk after the operation because of deterioration of general condition, axial pain, or impaired muscle function. In the nonambulatory group, 21 patients (24.4%) regained ambulatory functions postoperatively (Fig. 3B). Other demographic factors, Bilsky grade, SINS, and surgery-related factors did not significantly differ between the two groups (Tables 1 and 2).

FIG. 3.
FIG. 3.

Motor grade and muscle function change after the operation and Kaplan-Meier curve of survival analysis. A: Motor function change after the operation in both groups. *Significant difference between the two groups; †significant difference compared with preoperative assessment. B: Number of ambulatory and nonambulatory patients after the operation. C: Number of patients who were ambulatory after the operation in the nonambulatory group according to preoperative AIS muscle function grade. D: Kaplan-Meier curve demonstrating survival according to the postoperative ambulatory state.

TABLE 1.

Patient characteristics according to preoperative ambulatory status

Pt Ambulatoryp Value*
YesNo
No. of pts10686
Age, yrs58.5 ± 12.758.4 ± 12.70.950
Sex ratio, M/F76 (71.7%):

30 (28.3%)
50 (58.1%):

36 (41.9%)
0.066
BMI22.9 ± 3.523.5 ± 5.30.403
Survival, mos12.4 ± 15.212.5 ± 12.80.955
Comorbidities
 DM34 (32.1%)17 (19.8%)0.126
 HTN38 (35.8%)28 (32.6%)0.650
Major organ metastasis0.118
 None57 (53.8%)58 (67.4%)
 Resectable4 (3.8%)1 (1.2%)
 Nonresectable45 (42.5%)27 (31.4%)
Primary cancer0.296
 Lung17 (16.0%)19 (22.1%)
 Breast7 (6.6%)5 (5.8%)
 Prostate8 (7.5%)9 (10.5%)
 Renal13 (12.3%)3 (3.5%)
 Thyroid1 (0.9%)1 (1.2%)
 Hepatic19 (17.9%)7 (8.1%)
 Stomach, colon8 (7.5%)5 (5.8%)
 Others33 (31.1%)37 (43.0%)

DM = diabetes mellitus; HTN = hypertension; pt = patient.

Values are presented as mean ± SD or number of patients (%) unless otherwise indicated.

Statistical significance set at p < 0.05. The Student t-test was used to analyze age, BMI, and survival. The chi-square test was used to analyze sex, diabetes mellitus, hypertension, major organ metastasis, and primary tumor origin.

TABLE 2.

Neoplastic, functional, and treatment-related factors for ambulatory versus nonambulatory patients

Pt Ambulatoryp Value
YesNo
Bilsky grade (preop)2.5 ± 0.72.6 ± 0.60.232
SINS (preop)10.9 ± 3.410.3 ± 3.10.215
KPS score (preop)63.0 ± 12.050.5 ± 13.6<0.001*
AIS motor grade
 Preop3.8 ± 0.62.4 ± 1.2<0.001*
 Postop4.2 ± 1.03.2 ± 1.3<0.001*
Postop ambulation98 (92.5%)21 (24.4%)<0.001*
RT
 Preop58 (54.7%)32 (37.2%)0.020*
 Postop64 (60.4%)42 (48.8%)0.144
Op procedures0.624
 Decompression only6 (5.7%)6 (7.0%)
 Fixation only1 (0.9%)0 (0.0%)
 Decompression & fixation75 (70.8%)65 (75.6%)
 Corpectomy or en bloc resection24 (22.6%)15 (17.4%)
No. of operated levels1.9 ± 1.02.0 ± 1.40.631

Values are presented as mean ± SD or number of patients (%) unless otherwise indicated.

p < 0.05.

The Student t-test was used to analyze the Bilsky grade, SINS, KPS, initial motor grade, postoperative motor grade, and number of operative levels. The chi-square test was used to analyze the postoperative ambulatory state, RT, and operative procedures.

Surgical Complications

Fifteen patients (7.8%) died within 1 month of surgery (8 due to pneumonia, 3 due to coagulopathy causing brain hemorrhage or massive hemoptysis, 2 due to cardiac arrest of unknown cause, 1 due to brain metastasis causing respiratory failure, and 1 due to surgery-related hemorrhagic shock). When we compared patients who died within 1 month of surgery with patients with longer survival times, factors including age (p = 0.418), sex (p > 0.99), BMI (p = 0.179), smoking status (p = 0.075), preoperative KPS score (p = 0.208), Bilsky grade (p = 0.746), SINS (p = 0.984), major organ metastasis (p = 0.181), operative method (p = 0.993), and postoperative ambulatory function (p = 0.177) were not significantly different between the two groups. Revision surgery was required in 32 patients (16.1%): 17 patients with tumor recurrence, 4 with infection, 2 with hematoma, 2 with wound problems, and 2 patients with neurological deterioration, and 5 patients underwent additional surgery for other reasons.

Factors Associated With Good Functional Recovery and Recovery of Ambulatory Function

Ninety-three patients (48.4%) experienced ≥ 50% motor recovery postoperatively. From the regression analysis, SINS (p = 0.031), undergoing surgery involving only decompression procedures (p = 0.039), and the time interval from neurological deficits to surgery (p = 0.049) were significantly associated with good functional improvement. SINS (OR 1.099, 95% CI 1.001–1.208; p = 0.049) and time interval from neurological deficits to surgery (OR 0.911, 95% CI 0.832–0.996; p = 0.041) were significantly associated with good functional improvement in multivariate logistic regression analysis (Table 3). When we analyzed each factor involved in the SINS, involvement of the thoracic spine level (OR 2.042, 95% CI 1.149–3.630; p = 0.015) was significantly associated with functional recovery (Table 4). Furthermore, in subgroup analysis, patients with thoracic spine involvement (39/98, 39.8%) experienced significantly lower rates of good functional improvement compared with patients with MESCC at other levels (54/94, 57.4%; p = 0.021).

TABLE 3.

Factors associated with good functional improvement

OR95% CIp Value
Univariate analysis
 Demographic factors
  Age0.9920.971–1.0150.500
  Sex0.6880.378–1.2520.221
  BMI1.0310.963–1.1040.378
  KPS score (preop)1.0050.985–1.0260.594
  Motor grade (preop)0.9760.765–1.2450.846
 Neoplastic factors
  No. of levels requiring op1.2270.949–1.5860.118
  Anterior dural compression1.6220.728–3.6110.237
  Posterolat involvement0.6140.214–1.7620.364
  Pathologic vertebral compression fracture0.7600.386–1.4970.428
  Bilsky grade (preop)1.0810.706–1.6540.720
  SINS (preop)1.1031.009–1.2050.031*
 Treatment-related factors
  Op method
   Decompression only5.1121.089–23.9920.039*
   Fixation onlyNANANA
   Decompression & fixation1.1270.600–2.1170.710
   Corpectomy or en bloc resection0.7620.376–1.5420.450
  Preop RT0.8890.504–1.5680.684
  Postop RT0.7340.415–1.3000.289
  Symptom onset to op interval 0.9180.843–1.0000.049*
  Preop embolization0.5840.329–1.0370.066
Multivariate analysis
 SINS (preop)1.0991.001–1.2080.049*
 Decompression only4.2230.875–20.3800.073
 Symptom onset to op interval0.9110.832–0.9960.041*

NA = not applicable.

p < 0.05.

All analyses performed using logistic regression analysis.

TABLE 4.

Factors associated with a good functional improvement within SINS criteria

OR95% CIp Value
Factors included w/in the SINS
 Location1.410 1.028–1.9340.033*
 Mechanical pain1.1830.913–1.5350.204
 Bone lesion1.3080.849–2.0180.224
 Radiographic spinal alignment1.2330.936–1.6230.136
 Vertebral body collapse1.1130.812–1.5270.505
 Posterolat involvement0.9580.741–1.2390.743
Analysis by each location
 Junctional region (cervico-occipital, cervicothoracic, thoracolumbar)0.627 0.344–1.1420.127
 Mobile (cervical, lumbar)0.559 0.247–1.2660.163
 Semirigid (thoracic)2.042 1.149–3.6300.015*
 Rigid (sacrum)0.939NA0.665

p < 0.05.

All analyses were performed using logistic regression analysis.

Twenty-one patients (24.4%) in the preoperative nonambulatory group regained ambulatory functions postoperatively. In logistic regression analysis, preoperative muscle function grade (OR 2.477, 95% CI 1.414–4.338; p = 0.002) was the only factor associated with recovery of ambulatory functions (Table 5). None of the patients with a preoperative AIS motor grade of 0 (0/8) or 1 (0/15) regained ambulatory function postoperatively. In the preoperative nonambulatory group, 33.3% (6/18), 18.5% (5/27), and 55.6% (10/18) of patients with preoperative motor grades of 2, 3, and 4, respectively, regained ambulation after the operation (Fig. 3C). Although the association between the time interval between symptom onset and operation was not significant in the logistic regression analysis (p = 0.098), subgroup analysis comparing patients who underwent surgery < 72 hours from symptom onset and those who underwent surgery ≥ 72 hours from neurological deficit occurrence demonstrated that patients who underwent surgery within 72 hours following the onset of symptoms (20/46, 43.5%) demonstrated significantly higher rates of ambulatory function recovery compared with patients who had surgery ≥ 72 hours from neurological deficit occurrence (1/20, 5.0%; p = 0.020).

TABLE 5.

Factors associated with postoperative regaining of ambulatory function

OR95% CIp Value
Demographic factors
 Age0.9690.932–1.0080.123
 Sex0.5680.211–1.5310.264
 BMI0.8920.764–1.0420.149
 KPS score (preop)1.0350.997–1.0730.070
 Motor grade (preop)2.4771.414–4.3380.002*
Neoplastic factors
 No. of levels requiring op1.1510.816–1.6240.421
 Anterior dural compression1.6760.449–6.2560.442
 Posterolat involvement0.8720.167–4.5630.871
 Pathologic vertebral compression fracture0.3750.099–1.4190.149
 Bilsky grade (preop)0.6130.281–1.3390.220
 SINS (preop)1.0440.888–1.2280.600
Treatment-related factors
 Op method
  Decompression onlyNANANA
  Fixation onlyNANANA
  Decompression & fixation0.4350.114–1.6580.223
  Corpectomy or en bloc resection1.3580.344–5.3650.662
 Preop RT0.7300.268–1.9900.539
 Postop RT0.4960.181–1.3580.172
 Symptom onset to op interval0.8050.622–1.0410.098
 Preop embolization0.7030.226–2.1850.543

p < 0.05.

All analyses were performed using logistic regression analysis.

Survival

Overall, patients survived 18.3 ± 1.5 months (median 15.0 months, 95% CI 11.4–18.6, range 0–74 months) after the operation. The estimated survival rates at 3, 6, 12, and 24 months postoperatively were 83.8%, 66.4%, 57.5%, and 32.3%, respectively. Age (p = 0.758), sex (p = 0.670), KPS (p = 0.129), postoperative RT (p = 0.215), preoperative ambulatory function (p = 0.056), good functional recovery (p = 0.308), and local recurrence (p = 0.563) did not affect patient survival. However, postoperative ambulatory function (p = 0.048) was significantly associated with patient survival in the Kaplan-Meier survival analysis (Fig. 3D). The median survival times were 8.0 months (95% CI 4.8–13.0, range 0–72 months) in patients who could not ambulate postoperatively and 17.0 months (95% CI 15.3–18.6, range 0–74 months) in patients who could ambulate. Cox regression analysis demonstrated that patients who were ambulatory postoperatively survived 1.57 times longer than patients who were not ambulatory (HR 1.574, 95% CI 1.003–2.166; p = 0.048).

Discussion

In this study, 48.4% of patients experienced a motor recovery rate ≥ 50%. Involvement of the thoracic spine and delayed operation were associated with poor neurological recovery. About one-fourth (24.4%) of the patients who were not able to walk due to MESCC before surgery regained ambulation postoperatively. A lower preoperative muscle function grade was associated with a lower probability of regaining ambulatory function postoperatively. Furthermore, undergoing surgery ≥ 72 hours after the onset of neurological deficits significantly decreased the likelihood of regaining ambulatory function. Moreover, regaining ambulatory function postoperatively significantly improved patient survival. Although previous studies have reported similar results,8,9,11,23 the present study provides more solid evidence of the prognostic factors of postoperative neurological recovery for MESCC in a relatively large cohort of patients.

This study demonstrates that timely detection of MESCC-induced neurological deficits and expeditious intervention are of utmost importance for the recovery of motor function and walking ability. Previous studies have consistently indicated that the time duration between the onset of neurological deficits and surgery adversely affected the probability of neurological improvement.8,9,11 In a retrospective analysis involving 50 patients who underwent surgery due to spinal metastasis secondary to lung cancer, Park et al. reported that patients who had surgery within 72 hours after the onset of neurological deficits had an increased chance of regaining ambulation postoperatively.11 Chaichana et al. demonstrated that performing the surgery within the first 48 hours after the onset of symptoms independently increased, by 2.9-fold, the likelihood of regaining ambulatory functions.9 The need for decompressive surgeries in MESCC patients is always urgent; however, multiple factors, including preoperative evaluation, embolization, and correction of comorbidities, could delay the timing of the operation.8 Although the steps that lead to delay are needed to ensure patient safety, the findings of the present study suggest that the time spent on preoperative patient evaluation and management may lead to a decreased possibility of regaining ambulatory functions.8 Therefore, cancer centers should have preestablished protocols for MESCC patients with neurological deficits in order to expedite the timing of operations. Preoperative optimization or evaluation could be omitted when these steps delay the operation significantly enough to hinder efficacy. However, the urgency of surgical decompression must be weighed against the need to minimize perioperative morbidity by considering factors that affect individual safety and efficacy.8 Furthermore, preoperative steroid treatment should be considered when surgery is inevitably delayed.24,25 Stabilization or improvement of motor function in MESCC patients with steroid treatment has been reported previously.24,25 In the present study, because the preoperative motor grade was significantly associated with the chance of regaining ambulatory function postoperatively, the delay of motor function aggravation with preoperative steroid treatment may also have benefitted postoperative outcomes.

Although SINS was associated with good functional recovery in regression analysis, further analysis demonstrated that it was rather the location of the MESCC, and not the SINS itself, that was associated with neurological recovery. The results of a retrospective study by Wänman et al. also suggested that although SINS is helpful in assessing spinal instability when selecting patients for surgery, it does not predict survival or neurological outcomes.22 In the present study, thoracic spine metastasis was related to poor postoperative neurological recovery. Chaichana et al. also reported a possible significant association between the level of compression and ambulation recovery, with patients with thoracic levels of compression being less likely to regain ambulation, although this association did not reach statistical significance in their study (p = 0.07).9 The results of other studies have also suggested that the thoracic level is correlated with worse neurological outcomes for degenerative or traumatic pathologies.26,27 The spinal canal at the thoracic level is narrower than at the other levels, making the spinal cord more prone to injury at this location.9 Because the thoracic spine has fewer radiculomedullary arteries and poor collaterals, the blood supply is poorer than in other spinal levels, potentially diminishing the capacity to recover lost cord function after injury.2830 Furthermore, the anterior spinal artery in the thoracic spine is significantly impaired during ischemic insults.28 Resolving anterior dural compression with more extensive surgery may be required to recover the anterior spinal artery blood flow, which could potentially lead to better neurological outcomes, although this possibility requires further clarification.28

Patients with lower preoperative motor function grades had lower likelihoods of recovering ambulation. In fact, no patient with a preoperative lower-extremity AIS motor grade of 0 or 1 recovered ambulatory function postoperatively. Likewise, the results of an evaluation of 102 MESCC patients reported by Park and Jeon indicated that patients with grade 3 or greater muscle strength were much more likely to ambulate 48 hours after surgery than patients with more profound weakness (OR 49.2; p < 0.001).31 Hessler et al. also demonstrated that patients with Frankel grades of C or D were much more likely to ambulate postoperatively.32 The association between the severity of preoperative neurological deficits and the possibility of regaining ambulatory function postoperatively highlights the need to educate patients with metastatic spine cancers by instructing them to seek medical attention as soon as they detect even slight changes in motor function. Furthermore, the decision to surgically treat MESCC patients should be personalized according to the remaining motor function of each patient. The present study indicates that patients with a preoperative motor grade of 0 or 1 will benefit less from surgery as they are less likely to regain ambulatory function with surgery. The importance of surgery decreases in patients with multiple comorbidities and poor general condition if they have no chance of recovering ambulatory function. However, patients with better preoperative motor grades should be more actively treated with decompressive surgery because they have a greater chance of being able to walk after surgery. Furthermore, because postoperative ambulatory function was associated with longer survival in the present study, surgical management of patients with relatively preserved motor power may also increase life expectancy.

Among perioperative factors, ambulatory function was the only factor associated with patient survival. Similarly, Kim et al. reported that patients for whom ambulatory function was restored survived 1.97 times longer than those who were nonambulatory postoperatively.16 A better postoperative functional status and ambulatory function would increase patient motivation to receive intensive oncological therapies that could prolong life.17 Functional status may also be an important factor considered during decision-making by oncologists and may directly influence patient survival.11,17 Chong et al. demonstrated that postoperative KPS scores above 70 increased the probability of patients receiving systemic treatments.23

Our study had limitations. First, due to insufficient information in the medical records, we could not analyze factors such as postoperative duration of ambulation, bladder function, and reasons for delayed operation. Second, although the postoperative systemic therapy varied among the MESCC patients, medical factors that could affect patient survival could not be assessed in detail. Third, timing and operative methods could not be completely controlled. Many factors including location and extent of pathology, patient general health status, patient’s desire, neurological deficiency, and axial pain should be considered in operative planning, and this makes it difficult to apply a uniform algorithm in surgical decision-making for MESCC patients. Fourth, no factors demonstrated significant differences between patients who died within 1 month of the operation and those with longer survival, which limits the capacity to clarify the risk factors of early death after surgery in patients with MESCC, possibly because of the small number of patients with early death in the current study, a finding that warrants further evaluation. Finally, the inherent bias of the retrospective nature of the analysis should also be considered.

Conclusions

The results of this study indicated that increased time intervals between symptom onset and surgery and involvement of the thoracic spine were associated with a decreased likelihood of postoperative neurological recovery in MESCC patients. Furthermore, more severe preoperative neurological deficits were associated with lower likelihood of regaining ambulatory functions. Earlier detection of motor weakness and expeditious surgical interventions are necessary not only to improve functional status and quality of life but also to enhance patient survival.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Cho, S Park. Acquisition of data: Cho, S Park, JH Park, DH Lee, Hwang, Yang. Analysis and interpretation of data: Cho, S Park, JW Park. Drafting the article: Cho, S Park, JW Park. Statistical analysis: CS Lee.

References

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    Chang SY, Mok S, Park SC, Kim H, Chang BS. Treatment strategy for metastatic spinal tumors: a narrative review. Asian Spine J. 2020;14(4):513525.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Kumar N, Patel R, Tan JH, et al. Symptomatic construct failure after metastatic spine tumor surgery. Asian Spine J. 2021;15(4):481490.

  • 3

    Walsh GL, Gokaslan ZL, McCutcheon IE, et al. Anterior approaches to the thoracic spine in patients with cancer: indications and results. Ann Thorac Surg. 1997;64(6):16111618.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Bakar D, Tanenbaum JE, Phan K, et al. Decompression surgery for spinal metastases: a systematic review. Neurosurg Focus. 2016;41(2):E2.

  • 5

    Versteeg AL, Hes J, van der Velden JM, et al. Sparing the surgical area with stereotactic body radiotherapy for combined treatment of spinal metastases: a treatment planning study. Acta Oncol. 2019;58(2):251256.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Khan M, Garg R, Gui C, et al. Neuroimaging and stereotactic body radiation therapy (SBRT) for spine metastasis. Top Magn Reson Imaging. 2019;28(2):8596.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Spratt DE, Beeler WH, de Moraes FY, et al. An integrated multidisciplinary algorithm for the management of spinal metastases: an International Spine Oncology Consortium report. Lancet Oncol. 2017;18(12):e720e730.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Laufer I, Zuckerman SL, Bird JE, et al. Predicting neurologic recovery after surgery in patients with deficits secondary to MESCC: systematic review. Spine (Phila Pa 1976). 2016;41(suppl 20):S224-S230.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Chaichana KL, Woodworth GF, Sciubba DM, et al. Predictors of ambulatory function after decompressive surgery for metastatic epidural spinal cord compression. Neurosurgery. 2008;62(3):683692.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Finkelstein JA, Zaveri G, Wai E, Vidmar M, Kreder H, Chow E. A population-based study of surgery for spinal metastases. Survival rates and complications. J Bone Joint Surg Br. 2003;85(7):10451050.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Park SJ, Lee CS, Chung SS. Surgical results of metastatic spinal cord compression (MSCC) from non-small cell lung cancer (NSCLC): analysis of functional outcome, survival time, and complication. Spine J. 2016;16(3):322328.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Kumar N, Patel R, Tan BWL, et al. Asymptomatic construct failure after metastatic spine tumor surgery: a new entity or a continuum with symptomatic failure? Asian Spine J. 2021;15(5):636649.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Hinojosa-Gonzalez DE, Roblesgil-Medrano A, Villarreal-Espinosa JB, et al. Minimally invasive versus open surgery for spinal metastasis: a systematic review and meta-analysis. Asian Spine J. 2022;16(4):583597.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Quraishi NA, Arealis G, Salem KM, Purushothamdas S, Edwards KL, Boszczyk BM. The surgical management of metastatic spinal tumors based on an Epidural Spinal Cord Compression (ESCC) scale. Spine J. 2015;15(8):17381743.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Chen YJ, Chang GC, Chen HT, et al. Surgical results of metastatic spinal cord compression secondary to non-small cell lung cancer. Spine (Phila Pa 1976). 2007;32(15):E413E418.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Kim CH, Chung CK, Jahng TA, Kim HJ. Resumption of ambulatory status after surgery for nonambulatory patients with epidural spinal metastasis. Spine J. 2011;11(11):10151023.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Itshayek E, Candanedo C, Fraifeld S, et al. Ambulation and survival following surgery in elderly patients with metastatic epidural spinal cord compression. Spine J. 2018;18(7):12111221.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Foster JA, Salinas GD, Mansell D, Williamson JC, Casebeer LL. How does older age influence oncologists’ cancer management? Oncologist. 2010;15(6):584592.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Chi JH, Gokaslan Z, McCormick P, Tibbs PA, Kryscio RJ, Patchell RA. Selecting treatment for patients with malignant epidural spinal cord compression-does age matter? Results from a randomized clinical trial. Spine (Phila Pa 1976). 2009;34(5):431435.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Bilsky MH, Laufer I, Fourney DR, et al. Reliability analysis of the epidural spinal cord compression scale. J Neurosurg Spine. 2010;13(3):324328.

  • 21

    Marino RJ, Leff M, Cardenas DD, et al. Trends in rates of ASIA Impairment Scale conversion in traumatic complete spinal cord injury. Neurotrauma Rep. 2020;1(1):192200.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Wänman J, Jernberg J, Gustafsson P, et al. Predictive value of the Spinal Instability Neoplastic Score for survival and ambulatory function after surgery for metastatic spinal cord compression in 110 patients with prostate cancer. Spine (Phila Pa 1976). 2021;46(8):550558.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Chong S, Shin SH, Yoo H, et al. Single-stage posterior decompression and stabilization for metastasis of the thoracic spine: prognostic factors for functional outcome and patients’ survival. Spine J. 2012;12(12):10831092.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Versteeg AL, Elkaim LM, Sahgal A, et al. Steroids in the management of preoperative neurological deficits in metastatic spine disease: results from the EPOSO study. Neurospine. 2022;19(1):4350.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Kumar A, Weber MH, Gokaslan Z, et al. Metastatic spinal cord compression and steroid treatment: a systematic review. Clin Spine Surg. 2017;30(4):156163.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Ronen J, Goldin D, Itzkovich M, et al. Outcomes in patients admitted for rehabilitation with spinal cord or cauda equina lesions following degenerative spinal stenosis. Disabil Rehabil. 2005;27(15):884889.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Cotton BA, Pryor JP, Chinwalla I, Wiebe DJ, Reilly PM, Schwab CW. Respiratory complications and mortality risk associated with thoracic spine injury. J Trauma. 2005;59(6):14001409.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Colman MW, Hornicek FJ, Schwab JH. Spinal cord blood supply and its surgical implications. J Am Acad Orthop Surg. 2015;23(10):581591.

  • 29

    Bassett G, Johnson C, Stanley P. Comparison of preoperative selective spinal angiography and somatosensory-evoked potential monitoring with temporary occlusion of segmental vessels during anterior spinal surgery. Spine (Phila Pa 1976). 1996;21(17):19962000.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Dommisse GF. The blood supply of the spinal cord. A critical vascular zone in spinal surgery. J Bone Joint Surg Br. 1974;56(2):225235.

  • 31

    Park JH, Jeon SR. Pre- and postoperative lower extremity motor power and ambulatory status of patients with spinal cord compression due to a metastatic spinal tumor. Spine (Phila Pa 1976). 2013;38(13):E798E802.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Hessler C, Burkhardt T, Raimund F, et al. Dynamics of neurological deficit after surgical decompression of symptomatic vertebral metastases. Spine (Phila Pa 1976). 2009;34(6):566571.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • View in gallery
    FIG. 1.

    Illustrative case 1. A 60-year-old female patient visited the emergency department due to lower-extremity weakness. Her initial motor grade was assessed as grade 4 at the hip flexor and knee extensor muscles bilaterally, and she was not able to walk. A: Preoperative gadolinium-enhanced MR image revealing a circumferential mass at T10. B: Axial MR image showing epidural cord compression by the mass. C and D: Emergency posterior T7–L1 decompression and instrumentation and T10 corpectomy were performed. The mass was later identified to be a metastasis of breast cancer. She completely recovered from the neurological deficit 1 week after surgery and was able to ambulate without support.

  • View in gallery
    FIG. 2.

    Illustrative case 2. A 40-year-old female patient with a history of breast cancer visited the emergency department due to lower-extremity weakness and severe back pain. Her initial motor grade was assessed as grade 3 throughout the bilateral lower extremities. A: Preoperative sagittal MR image demonstrating pathologic compression and cord compression by a metastatic mass at T9. B: Axial MR image showing significant spinal cord compression by an epidural mass. C: Separation surgery was performed by laminectomy and tumor removal. T7–11 pedicle screw fixation was also performed. D: Postoperative RT was performed considering the separation surgery. At 1 month after surgery the patient’s motor function was restored to AIS grade 3.

  • View in gallery
    FIG. 3.

    Motor grade and muscle function change after the operation and Kaplan-Meier curve of survival analysis. A: Motor function change after the operation in both groups. *Significant difference between the two groups; †significant difference compared with preoperative assessment. B: Number of ambulatory and nonambulatory patients after the operation. C: Number of patients who were ambulatory after the operation in the nonambulatory group according to preoperative AIS muscle function grade. D: Kaplan-Meier curve demonstrating survival according to the postoperative ambulatory state.

  • 1

    Chang SY, Mok S, Park SC, Kim H, Chang BS. Treatment strategy for metastatic spinal tumors: a narrative review. Asian Spine J. 2020;14(4):513525.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2

    Kumar N, Patel R, Tan JH, et al. Symptomatic construct failure after metastatic spine tumor surgery. Asian Spine J. 2021;15(4):481490.

  • 3

    Walsh GL, Gokaslan ZL, McCutcheon IE, et al. Anterior approaches to the thoracic spine in patients with cancer: indications and results. Ann Thorac Surg. 1997;64(6):16111618.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4

    Bakar D, Tanenbaum JE, Phan K, et al. Decompression surgery for spinal metastases: a systematic review. Neurosurg Focus. 2016;41(2):E2.

  • 5

    Versteeg AL, Hes J, van der Velden JM, et al. Sparing the surgical area with stereotactic body radiotherapy for combined treatment of spinal metastases: a treatment planning study. Acta Oncol. 2019;58(2):251256.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6

    Khan M, Garg R, Gui C, et al. Neuroimaging and stereotactic body radiation therapy (SBRT) for spine metastasis. Top Magn Reson Imaging. 2019;28(2):8596.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7

    Spratt DE, Beeler WH, de Moraes FY, et al. An integrated multidisciplinary algorithm for the management of spinal metastases: an International Spine Oncology Consortium report. Lancet Oncol. 2017;18(12):e720e730.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8

    Laufer I, Zuckerman SL, Bird JE, et al. Predicting neurologic recovery after surgery in patients with deficits secondary to MESCC: systematic review. Spine (Phila Pa 1976). 2016;41(suppl 20):S224-S230.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Chaichana KL, Woodworth GF, Sciubba DM, et al. Predictors of ambulatory function after decompressive surgery for metastatic epidural spinal cord compression. Neurosurgery. 2008;62(3):683692.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10

    Finkelstein JA, Zaveri G, Wai E, Vidmar M, Kreder H, Chow E. A population-based study of surgery for spinal metastases. Survival rates and complications. J Bone Joint Surg Br. 2003;85(7):10451050.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11

    Park SJ, Lee CS, Chung SS. Surgical results of metastatic spinal cord compression (MSCC) from non-small cell lung cancer (NSCLC): analysis of functional outcome, survival time, and complication. Spine J. 2016;16(3):322328.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12

    Kumar N, Patel R, Tan BWL, et al. Asymptomatic construct failure after metastatic spine tumor surgery: a new entity or a continuum with symptomatic failure? Asian Spine J. 2021;15(5):636649.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Hinojosa-Gonzalez DE, Roblesgil-Medrano A, Villarreal-Espinosa JB, et al. Minimally invasive versus open surgery for spinal metastasis: a systematic review and meta-analysis. Asian Spine J. 2022;16(4):583597.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Quraishi NA, Arealis G, Salem KM, Purushothamdas S, Edwards KL, Boszczyk BM. The surgical management of metastatic spinal tumors based on an Epidural Spinal Cord Compression (ESCC) scale. Spine J. 2015;15(8):17381743.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15

    Chen YJ, Chang GC, Chen HT, et al. Surgical results of metastatic spinal cord compression secondary to non-small cell lung cancer. Spine (Phila Pa 1976). 2007;32(15):E413E418.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16

    Kim CH, Chung CK, Jahng TA, Kim HJ. Resumption of ambulatory status after surgery for nonambulatory patients with epidural spinal metastasis. Spine J. 2011;11(11):10151023.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17

    Itshayek E, Candanedo C, Fraifeld S, et al. Ambulation and survival following surgery in elderly patients with metastatic epidural spinal cord compression. Spine J. 2018;18(7):12111221.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18

    Foster JA, Salinas GD, Mansell D, Williamson JC, Casebeer LL. How does older age influence oncologists’ cancer management? Oncologist. 2010;15(6):584592.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19

    Chi JH, Gokaslan Z, McCormick P, Tibbs PA, Kryscio RJ, Patchell RA. Selecting treatment for patients with malignant epidural spinal cord compression-does age matter? Results from a randomized clinical trial. Spine (Phila Pa 1976). 2009;34(5):431435.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20

    Bilsky MH, Laufer I, Fourney DR, et al. Reliability analysis of the epidural spinal cord compression scale. J Neurosurg Spine. 2010;13(3):324328.

  • 21

    Marino RJ, Leff M, Cardenas DD, et al. Trends in rates of ASIA Impairment Scale conversion in traumatic complete spinal cord injury. Neurotrauma Rep. 2020;1(1):192200.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Wänman J, Jernberg J, Gustafsson P, et al. Predictive value of the Spinal Instability Neoplastic Score for survival and ambulatory function after surgery for metastatic spinal cord compression in 110 patients with prostate cancer. Spine (Phila Pa 1976). 2021;46(8):550558.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23

    Chong S, Shin SH, Yoo H, et al. Single-stage posterior decompression and stabilization for metastasis of the thoracic spine: prognostic factors for functional outcome and patients’ survival. Spine J. 2012;12(12):10831092.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24

    Versteeg AL, Elkaim LM, Sahgal A, et al. Steroids in the management of preoperative neurological deficits in metastatic spine disease: results from the EPOSO study. Neurospine. 2022;19(1):4350.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25

    Kumar A, Weber MH, Gokaslan Z, et al. Metastatic spinal cord compression and steroid treatment: a systematic review. Clin Spine Surg. 2017;30(4):156163.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26

    Ronen J, Goldin D, Itzkovich M, et al. Outcomes in patients admitted for rehabilitation with spinal cord or cauda equina lesions following degenerative spinal stenosis. Disabil Rehabil. 2005;27(15):884889.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27

    Cotton BA, Pryor JP, Chinwalla I, Wiebe DJ, Reilly PM, Schwab CW. Respiratory complications and mortality risk associated with thoracic spine injury. J Trauma. 2005;59(6):14001409.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28

    Colman MW, Hornicek FJ, Schwab JH. Spinal cord blood supply and its surgical implications. J Am Acad Orthop Surg. 2015;23(10):581591.

  • 29

    Bassett G, Johnson C, Stanley P. Comparison of preoperative selective spinal angiography and somatosensory-evoked potential monitoring with temporary occlusion of segmental vessels during anterior spinal surgery. Spine (Phila Pa 1976). 1996;21(17):19962000.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30

    Dommisse GF. The blood supply of the spinal cord. A critical vascular zone in spinal surgery. J Bone Joint Surg Br. 1974;56(2):225235.

  • 31

    Park JH, Jeon SR. Pre- and postoperative lower extremity motor power and ambulatory status of patients with spinal cord compression due to a metastatic spinal tumor. Spine (Phila Pa 1976). 2013;38(13):E798E802.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32

    Hessler C, Burkhardt T, Raimund F, et al. Dynamics of neurological deficit after surgical decompression of symptomatic vertebral metastases. Spine (Phila Pa 1976). 2009;34(6):566571.

    • Crossref
    • Search Google Scholar
    • Export Citation

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