Abstract
Context: There is no consensus on the preferred treatment for patients with spinal metastases. Little is known about the outcomes of surgery for this population. The objectives of this paper are to examine the outcomes of surgery among patients with spinal metastases suffering from cord compression (CC) or intractable pain (IP).
Design: Retrospective, descriptive (level 4) case series.
Setting: Rabin Medical Center, Israel.
Participants: 61 patients undergoing surgery for spinal metastasis in a tertiary care hospital. Patients were divided into two groups: those with spinal CC and those with IP only.
Interventions: Surgery due to CC or IP among patients with spinal metastases.
Outcome measures: Frankel scale to assess neurological status, ambulatory and incontinence status, which were examined before surgery, at discharge and at last follow-up. Endpoints were death or latest follow-up visit. Survival and postoperative complications were documented.
Results: There was no significant difference in Frankel score before and after surgery among patients with CC (mean score 3.5 and 3.4 respectively, P = 0.62). Complete incontinence rates significantly increased in patients with CC between preoperative and last follow-up examinations (13.6% vs. 20%, respectively, P = 0.05). Median survival of CC and IP groups was 201 and 402 days, respectively (P = 0.32). Complication rate was 41.4%.
Conclusion: In our cohort, Frankel score and walking capability of patients with CC did not change postoperatively, but continence status deteriorated over time. Surgeons should advise patients on expected surgical outcomes, especially in non-ambulatory and incontinent patients.
Keywords: Spinal metastases, Cord compression, Frankel scale, Surgical outcome, Survival, Incontinence status
Introduction
The spine is the most common site for skeletal metastasis in patients with malignancy, with up to 70% of cancer patients developing spinal metastases.1,2 The incidence of such metastases among all cancer patients is increasing due to longer life expectancy and improved medical treatment.3 Up to 10% of patients with cancer develop spinal cord compression due to spinal metastases during the course of their disease.2 Despite the fact that it is a common clinical entity, there is no consensus regarding the best treatment modality for these lesions once they become clinically significant.
Surgical intervention is usually considered for patients with signs of neurological compromise, radiological evidence for spinal instability, or intractable pain.4 Surgical treatment of metastatic spinal tumors can improve mechanical stability, relieve pain and alter neurological deterioration.5,6 Current literature does not support an effect on life expectancy for surgical intervention for the metastatic spine. Therefore, in most cases the goal of surgery is to improve patients’ quality of life (QOL).7
Only a few studies examined long-term QOL outcomes, such as pain, continence and ambulatory status, following surgery for spinal metastases.7 Reports on ambulatory status of patients with spinal metastases are inconsistent. Some studies show neurological recovery in more than 70% of patients following surgery.8 However, other studies show that the majority of patients remain in their preoperative neurological status or display a transient, short-term improvement.4,9 Existing data on continence status after spinal metastasis surgery are also inconclusive. Some studies report no to the minimal improvement of urinary continence5, whereas other studies show up to 59% recovery of urinary sphincter function.6
The purpose of this study was to evaluate the outcome of patients who underwent spinal surgery due to metastases. The primary objective was to examine the neurological outcome of these patients by means of the Frankel scale. A secondary objective was to evaluate the effect on patients’ QOL by examining ambulatory status and bowel and bladder control. We also examined patients’ survival and complication rate. Preoperative neurological status is a strong prognostic factor in patients with spinal metastases.7 Previous studies showed that patients with metastatic spinal cord compression have poorer prognosis than patients who are neurologically intact, presenting with intractable pain alone.5 Therefore, as a secondary analysis, we divided our cohort into two subgroups, i.e. patients with or without spinal cord compression, and examined the outcomes in each group separately over time.
Materials and methods
The population of this retrospective study included consecutive patients who were operated for spinal metastases between January 1, 2001 and December 31, 2010 in a tertiary care hospital. Indications for surgery were a neurologic deficit or intractable pain. We excluded patients undergoing biopsies as the only surgical intervention, patients with a life expectancy of less than six months and asymptomatic patients with spinal metastases.
Life expectancy of an oncologic patient was evaluated by a tumor board, which meets regularly at our institution to discuss the management of patients with spinal metastases and other orthopedic-oncologic patients. The board is a multi-disciplinary team comprising orthopedic surgeons trained in orthopedic oncology, senior oncologists and the patient’s treating oncologist, pathologists and musculoskeletal radiologists.
Two senior spine surgeons (NO and DS) performed all interventions. Tumor origin was determined by histopathological analysis of tissue biopsies.
Data were collected from the institution’s database. To reduce possible bias, patients were identified only by their Israeli identity card (ID) numbers. The following medical and demographic information was obtained: sex, dates of birth and death, obtained from the National Civil Registration database, extent and location of spinal involvement, type and time of surgery, tumor histology and surgical complications up to one month from surgery. Results of a full neurological examination and ambulatory and continence statuses were documented during admission and at each follow-up visit.
To assess the effect of neurological status prior to surgery on outcome, we divided our study population into two subgroups: (1) patients with a neurological deficit due to compression (CC group), and (2) patients with intractable pain only (IP group). We analyzed outcomes for each subgroup separately over time. Also, outcomes were compared between the two subgroups.
We graded patients’ neurological status according to Frankel scale, as A (paralysis, no motor or sensory function), B (preserved sensation only, no motor function), C (some voluntary motor function), D (preserved functional motor function), or E (normal). Neurological scoring was performed at three-time points: before surgery, at discharge and at last follow-up visit. In Table 2, Frankel score was converted from A-E to 1–5 for statistical analysis purposes.
Table 2. Frankel score1 during the follow-up period in the two patient groups.
| Group of patients | Pre- operative | After surgery | At last visit | P-value3 for in-group differences between first and last visits | |
|---|---|---|---|---|---|
| Patients with cord compression | Median (range) | 4.0 (1.0-5.0) | 4.0 (1.0-5.0) | 3.0 (1.0-5.0) | 0.62 |
| Mean ± SD (number) | 3.5 ± 0.9 (47) | 3.6 ± 0.9 (45) | 3.4 ± 1.1 (38) | ||
| Patients without cord compression | Median (range) | 5.0 (4.0-5.0) | 5.0 (4.0-5.0) | 5.0 (3.0-5.0) | 0.02 |
| Mean ± SD (number) | 4.9 ± 0.3 (18) | 4.9 ± 0.3 (16) | 4.5 ± 0.7 (15) | ||
| P-value for comparison between the two groups2 | <0.001 | <0.000 | 0.002 |
1Frankel score is presented in numbers in this table: A = 1, B = 2, C = 3, D = 4, E = 5.
2Mann-Whitney test.
3Freedman test.
Patients from the IP group who had a radiosensitive disease were irradiated prior to surgery.
Endpoints were defined as the death of a patient, or last follow-up visit. These endpoints were used to calculate cumulative survival time. In case a patient had more than one surgery, survival was calculated from the index surgery until one of the endpoints was met. Perioperative complications occurring within a month from surgery were recorded for each patient.
The study was approved by the Institutional Review Board.
Statistical analysis
Statistical analysis was performed using the SAS9.4 software. Continuous variables were compared between groups by t-test for normally distributed variables (age) or Mann–Whitney test for ordinal categorical variables (e.g. a number of vertebrae affected by tumor). Comparisons of ordinal categorical variables over time were performed by the Row Mean Score difference test (e.g. Frankel scale), which is considered to be analogous to a non-parametric Freedman test.10 Categorical nominal variables (sex, type of cancer, part of spinal column operated, or type of surgery) were compared between the groups using Chi-Square test. Variables with a cell size of less than five were compared using Fischer’s exact test. Survival estimates and analyses were performed using Kaplan-Meier analysis and the Log-Rank test. Statistical significance was determined as p < 0.05.
Results
Demographic and clinical characteristics of the study group
During the study period, a total of 101 oncologic surgical procedures were conducted on 86 patients at our institution. Twenty-five patients were excluded from the study; thus, the study cohort consisted of 61 patients that underwent 70 surgical procedures (Table 1). Fifty-three patients underwent a single operation, seven patients had two operations, of whom two patients had one operation due to intractable pain and the other due to cord compression, and one patient was subjected to three operations. Forty-six patients were assigned to the CC group, and the IP group consisted of 17 patients (Table 1).
Table 1. Patients’ demographics and characteristics.
| Patients with cord compression (46 patients, 52 surgeries) | Patients without cord compression (17 patients, 18 surgeries) | Total (61 patients, 70 surgeries)¹ | P-value | |
|---|---|---|---|---|
| Age at surgery, years | ||||
| Mean ± SD | 59.0 ± 14.5 | 60.7 ± 9.0 | 59.4 ± 13.3 | 0.57 |
| Median (range) | 60.5 (27.0–87.0) | 58.5 (48.0–79.0) | 60 (27.0–87.0) | |
| Male sex, % (number of patients) | 40.9 (18/44) | 52.9 (9/17)1 | 44.3 (27/61) | 0.4 |
| Type of cancer, % (number of patients) | ||||
| Breast | 26.9 (14) | 16.7 (3) | 24.3 (17) | 0.35 |
| Prostate | 11.5 (6) | 5.6 (1) | 10.0 (7) | |
| Lung | 11.5 (6) | 22.2 (4) | 14.3 (10) | |
| Colorectal | 7.7 (4) | 0 | 5.7 (4) | |
| Kidney | 3.9 (2) | 16.7 (3) | 7.1 (5) | |
| Thyroid | 7.7 (4) | 5.6 (1) | 7.1 (5) | |
| Others | 30.8 (16) | 33.3 (6) | 31.4 (22) | |
| Number of vertebrae affected by tumor, % (number of patients) | ||||
| 1 | 44.2 (23) | 66.7 (12) | 50.0 (35) | 0.08 |
| 2 | 34.6 (18) | 27.8 (5) | 32.9 (23) | |
| 3 | 9.6 (5) | 0 | 7.1 (5) | |
| 4 | 9.6 (5) | 5.6 (1) | 8.6 (6) | |
| 5 | 1.9 (1) | 0 | 1.4 (1) | |
| Part of spinal column operated, % (number of patients) | ||||
| Cervical | 9.6 (5) | 22.2 (4) | 12.9 (9) | <0.001 |
| Thoracic | 80.8 (42) | 33.3 (6) | 68.6 (47) | |
| Lumbar | 9.6 (5) | 44.4 (8) | 18.6 (13) | |
| Type of surgery, % (number of patients) | ||||
| ASF | 38.5 (20) | 22.2 (4) | 34.3 (24) | 0.01 |
| PSF | 15.4 (8) | 38.9 (7) | 21.4 (15) | |
| ASF + PSF | 0 | 11.1 (2) | 2.9 (2) | |
| No fusion, laminectomy only | 46.2 (24) | 27.8 (5) | 41.4 (29) | |
1Eight patients underwent two surgeries and one patient was operated three times during the study period.
Abbreviations: ASF, anterior spinal fusion; PSF, posterior spinal fusion.
There was no statistically significant difference between the two groups in the distribution of cancer types (P = 0.35). The most common primary tumor among all patients was breast cancer (24.3%). Most patients (82.9% of procedures) had metastases involving 1–2 vertebrae. The most frequent site of metastases was the thoracic spine (68.6% of all surgeries). There was a statistically significant difference in the distribution of spinal metastases between the two groups (P < 0.001). In the IP group, 44.4% of metastases were located in the lumbar spine and 33.3% were in the thoracic spine, whereas in the CC group, 9.6% were in the lumbar spine and 80.8% were in the thoracic spine (Table 1).
Most patients were submitted to laminectomy only or to corpectomy with anterior fusion. Forty-four patients (84.7%) in the CC group underwent one of these procedures. In the IP group, there was more diversity in the types of surgery (Table 1). The mean follow-up period was 230 days.
Neurological status
In the CC group, there was no marked difference in the Frankel score between the first and last examinations, as about half of the patients had a score of A-C at both baseline and last follow-up visit. However, 10 patients improved temporarily after the procedure (to D-E) (Table 2). The IP group had a median Frankel score of E prior to surgery. This score did not change throughout follow-up, but two patients regressed to a score of C at their last follow-up (Table 2).
QOL outcomes: walking ability and incontinence
Walking ability, which was initially significantly superior in the IP group, deteriorated between discharge and last follow-up in both groups. However, the deterioration was statistically significant only in the IP group (P = 0.05; Table 3). In the CC group, there were significantly more patients with complete incontinence at last follow-up than prior to surgery (P = 0.05; Table 3).
Table 3. QOL outcomes in both patient groups during the follow-up period.
| QOL outcomes | Time point | Continence level1 | Patients with cord compression (CC group) | Patients without cord compression (IP group) | P-value for comparisons between groups | P-value2 for in-group differences between first and last visits | |
|---|---|---|---|---|---|---|---|
| CC group | IP group | ||||||
| Capable of walking, % (number) | Pre- operative | 56.5 (26/46) | 100.0 (18/18) | <0.001 | 0.08 | 0.05 | |
| At discharge | 61.4 (27/44) | 100.0 (16/16) | 0.003 | ||||
| At last visit | 46.0 (17/37) | 80.0 (12/15) | 0.03 | ||||
| Continence, % (number) | Pre- operative | Full | 68.2 (30/44) | 100.0 (18/18) | 0.03 | 0.05 | 0.32 |
| Partial | 18.2 (8/44) | 0 | |||||
| None | 13.6 (6/44) | 0 | |||||
| At discharge | Full | 71.1 (27/38) | 93.8 (15/16) | 0.17 | |||
| Partial | 18.4 (7/38) | 6.3 (1/16) | |||||
| None | 10.5 (4/38) | 0 | |||||
| At last visit | Full | 67.0 (20/30) | 92.3 (12/13) | 0.16 | |||
| Partial | 13.3 (4/30) | 7.7 (1/13) | |||||
| None | 20.0 (6/30) | 0 | |||||
¹“Partial” continence level is defined as urinary incontinence only.
²Freedman test.
Survival
At the end of the study period, only seven out of 61 patients were alive. Mean survival time was 291 days in the CC group days and 281 days in the IP group. Median survival time was 201 days (6.7 months) in the CC group and 402 days (13.4 months) in the IP group. The difference in median survival time was not statistically significant (P = 0.32; Fig. 1).
Figure 1.
Survival of patients with and without cord compression after surgery.
When considering cancer types, median survival time was 194 days among patients with lung cancer and 439 days among patients with breast cancer; yet, the difference was not statistically significant (P = 0.42; Fig. 2).
Figure 2.
Survival of patients according to cancer type.
Complications
Complications occurred in 41.4% of cases. Perioperative death rate was 7%. The most common complication was surgical wound infection (10%). In 5.7% of surgeries, blood transfusions were required due to post-operative hemorrhage.
Discussion
In our cohort of patients with spinal metastases, breast cancer was the most common tumor type, similar to what was previously described in the literature.2 The most common site for metastases was the thoracic spine, which is also in line with the literature.11 In the IP group, the most frequent site of spinal metastases was the lumbar spine. The thoracic spine is more stable and less mobile than the lumbar spine, mainly due to the surrounding rib cage. Pain would be more pronounced where there is more movement. Also, the lumbar spine has a wider canal diameter than the thoracic spine. Therefore, metastases in this region would cause pain more commonly than they would cause cord compression. This can explain why the patients of the IP subgroup presented with pain rather than a neurological deficit as their chief complaint. To our knowledge, no other study reported the location of spinal metastases among patients without cord compression.
41.4% of our patients underwent laminectomy only, most of them in the CC group, and 58.6% underwent decompression and fusion, mostly in the IP group. This difference can be explained by the distinct surgical goals. Surgery in the CC group was performed primarily to achieve decompression, whereas in the IP group, fusion was the main goal. Witham et al. observed better functional outcomes after posterior decompression combined with stabilization, as compared to laminectomy alone, with the same mortality rates.12 Nevertheless, one should take into account the poor general status and low expected survival of the patients, which did not always allow for extensive and prolonged surgery. Therefore, at our institution we consider laminectomy alone as a salvage operation for certain complex patients with a neurological deficit due to spinal metastases, who cannot withstand longer surgeries or have low expected survival.
Patients with metastatic spinal cord compression (MSCC) pose a dilemma to medical teams. Younger patients with a mild deficit (Frankel D or E) who have a good prognosis are favorable candidates for surgery. Unfortunately, the situation is different when the patient is older, with an unpredictable prognosis and significant neurological deficit. Our results show that Frankel score of some patients with CC improved transiently following surgery. In recent years, there has been evidence on the improved outcomes after corpectomy and stabilization in comparison to other methods of treatment of patients with CC.12 However, in our cohort, this treatment did not alter significantly Frankel scores of patients with CC at the last follow-up visit, relative to baseline levels. Other studies also found unchanged or re-deteriorated Frankel scores at long-term follow-up after surgery in the majority of cases.4,9 The setback was mainly due to disease progression after surgery. Unfavorable outcomes in our cohort might also be accounted for by the inclusion of patients in poor general health. Moreover, improvement could be hampered by the long and extensive surgical procedure, which might have been too aggressive for these frail patients.
Patients in the IP group had some decrease in Frankel score between the perioperative period and last visit. This observation may be explained by the fact the final encounter with the patient was often at the last admission at the end of their lives, when general deterioration occurred.
The Frankel scale may be a limited tool for assessment of neurological status. In some patients, the motor improvement observed after surgery did not change the score. Therefore, we also evaluated QOL outcomes, namely walking ability and incontinence. Ambulatory status in the CC group did not improve significantly after surgery. Moreover, a deterioration of ambulatory status was seen at the last follow-up. Similarly, Patchell et al. showed that regained walking ability is preserved for approximately two months after surgery.13 In the IP group, we detected a statistically significant deterioration in walking ability at last follow-up. Combined with a reduction in the Frankel score in this group, this may indicate general health deterioration and disease progression in these patients.
The most common autonomic finding in patients with MSCC is bladder dysfunction, which also correlates with motor dysfunction.11 Surgery is aimed at stopping autonomic dysfunction; yet, in our study, sphincter control in the CC group significantly deteriorated from post-operative discharge to last follow-up. Our findings confirm those of a previous study, which found that most patients with MSCC suffering from urinary incontinence did not improve after surgery.5 However, another study showed fully recovered urinary control in up to 59% of patients with MSCC following surgery.14 In the latter study, patients were followed for one year or until death, with a median survival of five months. This is a short follow-up period, during which urinary continence can remain unchanged. Recurrent spinal metastases may lead to neurological deterioration within a year from surgery in approximately 70% of patients.15 This might account for the deterioration in the ambulatory and incontinence status of the CC group in our study.
Our results show no significant improvement in Frankel score or QOL outcomes in the CC group after surgery and during the follow-up period. Other studies demonstrate some improvement in these parameters following surgery.14 However, there is a selection bias associated with retrospective studies. In our study, patients with CC seemed to be in a more deteriorated preoperative neurological condition compared to other reports. 32% of the patients in our study were non-ambulatory prior to surgery, whereas in other studies the reported rates were 14%–24% patients.5,14 Preoperative neurological status is a strong prognostic factor in patients with MSCC.7,15 Therefore, worse preoperative neurological status may account for some of the differences between our results and previously published outcomes.
Regarding survival, patients in the IP group lived longer than patients with CC, but the difference was not statistically significant, most probably due to the small cohorts. Yet, our results are in concordance with other publications, which found a correlation between advanced neurological deterioration prior to surgery and poor survival.5,14
The significance of the primary tumor type as a prognostic factor among patients with spinal metastases is well established.7,14 In line with other papers, we found differences in survival among patients with different cancer types.16 The differences were not statistically significant, again most likely due to the small sample size. Based on survival data from our study, it is reasonable to conclude that MSCC patients with cancer types of more favorable prognosis, such as breast or prostate, could benefit from surgery more than patients with more aggressive tumors such as lung cancer.
Surgical morbidity and the postoperative 30-day mortality rates for our patients were 41.4% and 7%, respectively. Other studies have reported surgical complications in 11%–48% of patients.17,18 Mortality rates up to 30 days after surgery ranged between 3% and 30%.19,20 Wound dehiscence was the most common complication in our series (10%), with a similar rate noted in the literature.4,20 We found no other report presenting hemorrhage as a complication in patients with spinal metastases.4,17–21 Therefore, we cannot comment on this issue, which might have increased the complication rate in our study.
There are several limitations to our study. First, this is a retrospective study and, as such, it has an inherent selection bias. For example, as previously discussed, our cohort consisted of more non-ambulatory patients than previous cohorts in the literature.5,14 This could influence the results of our statistical analyses of the CC subgroup and comparisons between the two subgroups. Another limitation is the relatively small cohort in the IP subgroup, which could prevent statistical significance in different comparisons. One such example is survival analysis, which did not show statistically significant differences between the IP and CC groups. Another limitation is the different time points at which walking ability and continence status were examined. As this is a retrospective study, we only had data from preoperative, immediate postoperative and last follow-up visits. Latest follow-up could often represent an admission of a patient in general deterioration before he or she passed away. This may explain the deterioration in walking ability and Frankel score in the IP group and in continence status among CC patients at last follow-up.
In conclusion, neurological deterioration in patients operated due to symptomatic spinal metastases, as indicated by walking ability and continence status, was halted in our study shortly after surgery. However, this effect was not preserved during longer follow-up periods and patients, both with and without cord compression, experienced a decline in walking ability and continence status. Surgeons should advise patients on expected surgical outcomes, especially in non-ambulatory and incontinent patients.
Conflicts of interest
No potential conflict of interest was reported by the authors.
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