Available online at www.sciencedirect.com ScienceDirect EJSO 41 (2015) 1691e1698 www.ejso.com Posterior decompression and spine stabilization for metastatic spinal cord compression in the cervical spine. A matched pair analysis M. Lei a,y.liu a, *,L.Yan b, C. Tang c, S. Liu a, **, S. Zhou d a Department of Orthopedic Surgery, Affiliated Hospital of Academy of Military Medical Sciences, No. 8, Fengtaidongda Rd, Beijing 100071, China b Department of Spine Surgery, Hong Hui Hospital, Xi an Jiaotong University College of Medicine, Xi an, China c Department of Pulmonary Neoplasms Internal Medicine, Affiliated Hospital of Academy of Military Medical Sciences, No. 8, Fengtaidongda Rd, Beijing, China d Statistics Room, Capital Medical University Affiliated Beijing Friendship Hospital, No. 95, Xuanwu District Yongan Rd, Beijing, China Accepted 27 September 2015 Available online 23 October 2015 Abstract Purpose: This study aims to compare clinical outcome of cervical spine metastasis with those of thoracic and lumbar spine metastasis after surgery for metastatic spinal cord compression (MSCC). Patients and methods: Data from nineteen patients with cervical spine metastasis were matched to thirty-eight patients with thoracic spine metastasis and thirty-eight patients with lumbar spine metastasis from a cohort of 183 patients with MSCC treated with posterior decompression and spine stabilization. Three groups were matched for eleven potential prognostic characteristics, and at least nine of eleven characteristics should match between the matched patients. Results: Deterioration of motor function was observed in 37% patients with cervical spine metastasis, 18% patients with thoracic spine metastasis, and 13% patients with lumbar spine metastasis after surgery (P ¼ 0.02). Postoperative median survival was 11.5 months for cervical spine metastasis, 10.9 months for thoracic spine metastasis, and 10.7 months for lumbar spine metastasis (P ¼ 0.64). Surgeryrelated complications occurred in 18.9% of all patients and showed no significant difference between the three groups (P ¼ 0.63). Each group experienced improvement in pain outcome when compared between pre- and post-operative pain scores (P < 0.01), while the differences had no sgnificance between the three groups (P > 0.05). Conclusions: MSCC in cervical spine is less likely to improve or maintain motor function as compared with MSCC in thoracic and lumbar spine after surgery. However, its clinical outcomes appear similar to those of thoracic and lumbar spine metastasis in terms of postoperative survival, surgery-related complication, and pain outcome. Ó 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons. org/licenses/by-nc-nd/4.0/). Keywords: Metastatic spinal cord compression; Cervical spine metastasis; Matched pair analysis; Survival prognosis; Function outcome Introduction Abbreviations: MSCC, metastatic spinal cord compression; ECOG, eastern cooperative oncology group; OR, odds ratio; CI, confidence interval; VAS, visual analog scale. * Corresponding author. Tel./fax: þ86 028 010 66947317. ** Corresponding author. Tel./fax: þ86 028 010 66947317. E-mail addresses: 632763246@qq.com (Y. Liu), lsb9126@vip.sina. com (S. Liu). Although the cervical spine metastasis is less common than the thoracic and lumbar spine metastasis, metastatic disease in the cervical spine can result in respiratory failure and neurological deficits due to the likelihood of spinal instability and metastatic spinal cord compression (MSCC). 1 MSCC occurs in 5e14% of all patients with cancer during their disease course. 2,3 The treatment goals for MSCC in the cervical spine include relieving spinal cord http://dx.doi.org/10.1016/j.ejso.2015.09.025 0748-7983/Ó 2015 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).
1692 M. Lei et al. / EJSO 41 (2015) 1691e1698 compression, providing spinal stability, improving pain outcome, maintaining function and maximizing the quality of remaining life. Since the 1980s, the improvements in surgical techniques and advent of spinal implants have allowed better removal of the tumor with immediate spinal cord decompression, along with the possibility of stabilizing and reconstructing the spine during the operation. Decompressive surgery and spine stabilization is widely and effectively used in patients with MSCC with a tolerable rate of complications. 4e7 Furthermore, it is associated with improved neurological function, pain outcome, and, likely, overall survival. 8 Metastatic disease in the cervical spine is always regarded to be a poorer prognosis than in the thoracic and lumbar spine metastasis. 1,9,10 However, relatively few articles is published about surgery in metastasis to the cervical spine, let alone report systematically comparing the clinical outcome and surgical results of the cervical spine metastasis with those of the thoracic and lumbar spine metastasis after posterior decompression and spine stabilization for MSCC. Therefore, we performed a matched pair analysis following strict matching criteria and choosing eleven potential prognostic characteristics in 95 patients with MSCC. This design was considered to provide the highest level of evidence apart from a randomized trial. Postoperative motor function, survival, surgery-related complication, and pain outcome were compared between the cervical spine metastasis group and the thoracic and lumbar spine metastasis groups. Patients and methods Patients Nineteen patients with MSCC in the cervical spine operated with decompression and stabilization were retrospectively analyzed at the Affiliated Hospital of Academy of Military Medical Sciences, Beijing, between May 2005 and May 2015. Each patient with the cervical spine metastasis was matched with two patients with the thoracic spine metastasis and two patients with the lumbar spine metastasis (1:2:2) from a cohort of 183 patients with MSCC treated with posterior decompression and spine stabilization. Therefore, 95 patients with MSCC were included in this study. The patients were matched for eleven potential prognostic characteristics: age (57 vs. >57 years, median age: 57 years), sex (female vs. male), type of primary tumor (breast cancer vs. thyroid cancer vs. lung cancer vs. others), preoperative ambulatory status (ambulatory vs. not ambulatory), extraspinal bone metastasis (no vs. yes), Eastern Cooperative Oncology Group (ECOG) performance status (1e2 vs. 3e4), number of involved vertebrae (1e2 vs. 3), visceral metastasis (no vs. yes), interval from cancer diagnosis to surgery (2 years vs. >2 years, median time: 2 years), time developing motor deficit (2 vs. >2 weeks), and targeted therapy (no vs. yes). At least nine of these factors should match between the five matched patients. The Medical Research Ethics Board of the Affiliated Hospital of Academy of Military Medical Sciences approved this retrospective study and required neither patient approval nor informed consent for review of patients images and medical records. The data were retrospective in nature and anonymized by the Medical Research Ethics Board of the Affiliated Hospital of Academy of Military Medical Sciences. Surgical indications The indication for surgery was neurological deficit due to spinal cord compression which had been confirmed by spinal magnetic resonance imaging, and a life expectancy at least three months. The diagnosis of cancer or bone metastasis was confirmed histologically. All patients were operated with posterior decompression and spine stabilization. Local radiotherapy, systemic chemotherapy, and targeted therapy were performed after the wound healed, about 3e4 weeks after the surgery. Evaluation indexes Motor function was evaluated before operation, and up to 6 months after operation with a 5-point scale 11 : 0: normal strength, 1: ambulatory without aid, 2: ambulatory with aid, 3: not ambulatory, 4: paraplegia. Improvement or deterioration of motor function was defined as a change of at least one point. In addition to the comparison of motor function between the three groups, postoperative survival, surgery-related complication, and pain outcome were compared. The postoperative survival was defined as the time between the date of surgery and death or the latest follow-up. Seven patients were still alive by the end of the study period, with a median follow-up of 10 months (2e33 months) in those patients. The time developing motor deficits meant the time between deterioration of motor function to disability or surgery which was developed from Rades study. 12 Pain outcome was preoperatively and 6-month postoperatively assessed with visual analog scale (VAS), which has a score scale of 1e10. Statistical analysis Both univariate and multivariate analysis of the motor function outcome were performed with the ordered-logit model, as the data for function outcome are ordinal (better ¼ 1, no change ¼ 2, worse ¼ 3). The univariate analysis of survival prognosis was calculated with the
M. Lei et al. / EJSO 41 (2015) 1691e1698 1693 KaplaneMeier method and log-rank test, as well as simple Cox regression model. All prognostic factors were also evaluated in a multivariate analysis performed with the multiple Cox regression model (stepwise selection of variables) for survival prognosis. In order to account for the matched-pair design, a stratified model has been used. Surgery-related complication was compared with Chisquare test between three groups. Regarding pain outcome, paired t test was used to analyze differences between preand post-operative pain scores in each group; Dunnett s t test was used to compare the pain scores of the cervical spine group and those of the thoracic spine and lumbar spine groups. A P value of 0.05 or less was considered statistically significant. Statistical analysis was performed using SAS 9.2 software. Results Patient characteristics Of the total series of 95 patients, 19 patients with the cervical spine metastasis were matched with 38 patients with the thoracic spine metastasis and 38 patients with the lumbar spine metastasis. The patients were operated with posterior decompression and spine stabilization due to MSCC (Fig. 1). Patient characteristics related to the three groups were summarized in Table 1. It demonstrated that pair-matching was successful, as the distribution of these variables was similar in the three groups. In the series of 19 patients in the cervical spine metastasis group, 8 were females and 11 were males. Median age was 57 years (range 29e69 years). The distribution of primary tumors was as follows: breast cancer 4, thyroid cancer 3, lung cancer 8, and others 4. Functional outcome According to the univariate analysis, improvement of motor function (Table 2) was correlated with non-cervical spine metastasis (P ¼ 0.02), favorable tumor type (P ¼ 0.04), ambulatory status before surgery (P < 0.01), better ECOG performance status (P < 0.01), absence of visceral metastasis (P < 0.01), longer interval between tumor diagnosis and surgery (P < 0.01), slower development of motor deficits (P < 0.01), and administration of targeted therapy (P < 0.01). In the multivariate analysis of motor function, metastatic location (OR ¼ 1.93; 95% CI, 1.12e3.33; P ¼ 0.02), preoperative ambulatory status (OR ¼ 2.80; 95% CI, 1.17e6.71; P ¼ 0.02), and time developing motor deficit (OR ¼ 5.75; 95% CI, 2.22e14.89; P < 0.01) were significant, whereas other variables were excluded by Cox model. In detail, deterioration of motor function occurred in 37% of patient in cervical spine group, 18% of patient in thoracic spine group, and 13% of patient in lumbar spine group (Table 2). Cervical spine metastasis seems significantly associated with poor motor function as compared with thoracic and lumbar spine metastasis. Figure 1. A 51-year-old woman who was unable to sit due to metastatic spinal cord compression (MSCC) resulted from lung cancer. A. Preoperative radiographs presented vertebral collapse due to MSCC at C6 and C7. B. Preoperative MRI showed pathologic collapse of C6 and C7. C. Following laminectomy at C5eC7, and pedicle screw fixation was conducted to spine stabilization. Postoperative motor function was improved from 3 to 2 point. She died at postoperative 5 months and spine stability was maintained throughout the survival period.
1694 M. Lei et al. / EJSO 41 (2015) 1691e1698 Table 1 Comparison of the distribution of the potential prognostic characteristics in the three groups. Characteristics No. Cervical spine Thoracic spine Lumbar spine No. % No. % No. % Age 57 years 50 10 53 21 55 19 50 >57 years 45 9 47 17 45 19 50 Sex Female 40 8 42 16 42 16 42 Male 55 11 58 22 58 22 58 Type of primary tumor Breast cancer 20 4 21 8 21 8 21 Thyroid cancer 15 3 16 6 16 6 16 Lung cancer 40 8 42 16 42 16 42 Others 20 4 21 8 21 8 21 Preoperative ambulatory status Ambulatory 53 11 58 20 53 22 58 Not ambulatory 42 8 42 18 47 16 42 Extraspinal bone metastasis No 23 5 26 9 24 9 24 Yes 72 14 74 29 76 29 76 ECOG performance status 1e2 58 12 63 22 58 24 63 3e4 37 7 37 16 42 14 37 No. of involved vertebrae 1e2 36 7 37 14 37 15 39 3 59 12 63 24 63 23 61 Visceral metastasis No 59 12 63 23 61 24 63 Yes 36 7 37 15 39 14 37 Interval from cancer diagnosis to surgery 2 years 45 9 47 17 45 19 50 >2 years 50 10 53 21 55 19 50 Time developing motor deficit 2 weeks 36 7 37 15 39 14 37 >2 weeks 59 12 63 23 61 24 63 Targeted therapy No 55 11 58 22 58 22 58 Yes 40 8 42 16 42 16 42 ECOG indicates Eastern Cooperative Oncology Group. Overall survival In the entire cohort of 95 patients, the overall median survival time was 10.9 months (95% CI, 9.3e11.9 months), and the 6-month and 12-month survival rates were 76.6% and 39.2%, respectively. According to the univariate analysis, postoperative survival (Table 3) was associated with type of primary tumor (P < 0.01), preoperative ambulatory status (P < 0.01), ECOG performance status (P < 0.01), visceral metastasis (P < 0.01), interval from cancer diagnosis to surgery (P < 0.01), time developing motor deficit (P < 0.01), and targeted therapy (P < 0.01). Metastatic location in spine regions was not significantly associated with postoperative survival (P ¼ 0.40). In the multivariate analysis, postoperative survival was significantly associated with type of primary tumor (RR ¼ 1.86; 95% CI, 1.45e2.38; P < 0.01), preoperative ambulatory status (RR ¼ 1.91; 95% CI, 1.17e3.13; P ¼ 0.01), visceral metastasis (RR ¼ 2.07; 95% CI, 1.25e3.42; P < 0.01), and targeted therapy (RR ¼ 1.77; 95% CI, 1.03e3.03; P ¼ 0.04), whereas ECOG performance status, interval from cancer diagnosis to surgery, and time developing motor deficit lost significance. Surgery-related complication and pain outcome Surgery-related complications occurred in 18 patients (18.9%, Table 4): 5 patients (26.3%) were observed in cervical spine group, 7 patients (18.4%) were found in thoracic spine group, and 6 patients (15.8%) were detected in lumbar spine group (P ¼ 0.63). The rate of complication was relatively high in cervical spine group, but it showed no significant difference between the three groups (P ¼ 0.63). Each group experienced improvement in their pain outcome when compare between pre- and post-operative
M. Lei et al. / EJSO 41 (2015) 1691e1698 1695 Table 2 Univariate and multivariate analysis of the impact of potential prognostic characteristics on motor function. Characteristics No. Better No change Worse Univariable analysis Multivariable analysis (%) (%) (%) OR (95% CI) P OR (95% CI) P Metastatic location Cervical spine 19 21 42 37 Thoracic spine 38 29 53 18 Lumbar spine 38 42 45 13 1.82 (1.08e3.06) 0.02 1.93 (1.12e3.33) 0.02 Age 57 years 50 34 58 8 >57 years 45 31 36 33 2.03 (0.94e4.38) 0.07 Not included Sex Female 40 30 60 10 Male 55 35 38 27 1.32 (0.61e2.84) 0.48 Not included Type of primary tumor Breast cancer 20 35 50 15 Thyroid cancer 15 47 40 13 Lung cancer 40 33 57 10 Others 20 20 30 50 1.47 (1.01e2.14) 0.04 Not included Preoperative ambulatory status Ambulatory 53 43 47 10 Not ambulatory 42 19 48 33 3.81 (1.68e8.64) <0.01 2.80 (1.17e6.71) 0.02 Extraspinal bone metastasis No 23 35 48 17 Yes 72 32 47 21 1.18 (0.49e2.84) 0.72 Not included ECOG performance status 1e2 58 41 52 7 3e4 37 18 41 41 4.94 (2.09e11.67) <0.01 Not included No. of involved vertebrae 1e2 36 33 45 22 3 59 32 49 19 0.95 (0.44e2.06) 0.89 Not included Visceral metastasis No 59 39 51 10 Yes 36 22 42 36 3.21 (1.41e7.28) <0.01 Not included Interval from cancer diagnosis to surgery 2 years 45 20 44 36 >2 years 50 44 50 6 2.65 (1.21e5.82) 0.02 Not included Time developing motor deficit 2 weeks 36 14 44 42 >2 weeks 59 44 49 7 6.84 (2.76e16.94) <0.01 5.75 (2.22e14.89) <0.01 Targeted therapy No 55 16 60 24 Yes 40 55 30 15 4.11 (1.80e9.40) <0.01 Not included ECOG indicates Eastern Cooperative Oncology Group; OR, odds ratio; CI, confidence interval. pain scores (P < 0.01), while the differences were 4.47 1.71, 5.42 2.12, and 4.79 2.38, respectively (P > 0.05, Table 4). Discussion Metastatic spinal cord compression (MSCC) is a severe complication of malignant tumors that occurs in 5e14% of patients with cancer and can cause intractable pain, disability, and incontinence, negatively impacting the patient s quality of remaining life. Notably, MSCC in the cervical spine can leads to respiratory failure and quadriplegia, severely threatening the patient s life. Timely decompression and proper spine stabilization for cervical spinal metastasis was found to be effective in terms of neurological recovery and immediate pain control. 1,6 Generally, metastatic disease in the cervical spine is always regarded to be a poorer prognosis than in the thoracic and lumbar spine metastasis. 1,9,10 In fact, there was no report systematically comparing the clinical outcome and surgical results of the cervical spine metastasis with those of the thoracic and lumbar spine metastasis after surgery for MSCC. Therefore, we performed a matched pair analysis following strict matching criteria and choosing eleven potential prognostic characteristics in a series of 95 patients with MSCC. This design was considered to provide the highest level of evidence apart from a randomized trial. Unfortunately, because our study is based on retrospective data, a hidden selection bias cannot be excluded. In the present study, postoperative motor function was significantly associated with metastatic location in spine, preoperative ambulatory status, and time developing
1696 M. Lei et al. / EJSO 41 (2015) 1691e1698 Table 3 Univariate and multivariate analysis of the impact of potential prognostic characteristics on overall survival. Characteristics No. KaplaneMeier Simple Cox regression Multiple Cox regression MOS P HR (95% CI) P HR (95% CI) P Metastatic location Cervical spine 19 11.5 Thoracic spine 38 10.9 Lumbar spine 38 10.7 0.64 0.89 (0.67e1.18) 0.40 Not included Age 57 years 50 10.3 >57 years 45 11.4 0.66 0.91 (0.59e1.39) 0.66 Not included Sex Female 40 10.9 Male 55 11.4 0.63 0.90 (0.59e1.39) 0.63 Not included Type of primary tumor Breast cancer 20 14.3 Thyroid cancer 15 27.8 Lung cancer 40 10.3 Others 20 6.4 <0.01 2.11 (1.62e2.75) <0.01 1.86 (1.45e2.38) <0.01 Preoperative ambulatory status Ambulatory 53 13.5 Not ambulatory 42 9.3 <0.01 2.69 (1.68e4.33) <0.01 1.91 (1.17e3.13) 0.01 Extraspinal bone metastasis No 23 11.0 Yes 72 10.6 0.91 1.03 (0.62e1.73) 0.91 Not included ECOG performance status 1e2 58 13.3 3e4 37 7.7 <0.01 2.85 (1.77e4.61) <0.01 Not included No. of involved vertebrae 1e2 36 11.2 3 59 10.7 0.42 1.19 (0.77e1.85) 0.43 Not included Visceral metastasis No 59 11.8 Yes 36 7.0 <0.01 2.19 (1.40e3.42) <0.01 2.07 (1.25e3.42) <0.01 Interval from cancer diagnosis to surgery 2 years 45 9.3 >2 years 50 13.3 <0.01 2.38 (1.50e3.78) <0.01 Not included Time developing motor deficit 2 weeks 36 9.0 >2 weeks 59 11.8 <0.01 2.11 (1.34e3.33) <0.01 Not included Targeted therapy No 55 7.7 Yes 40 13.9 <0.01 3.33 (2.08e5.32) <0.01 1.77 (1.03e3.03) 0.04 MOS indicates median overall survival; HR, hazard rate; CI, confidence interval; ECOG, Eastern Cooperative Oncology Group. motor deficit before surgery. Deterioration of motor function occurred in 37% of patient in the cervical spine group, 18% of patient in the thoracic spine group, and 13% of patient in the lumbar spine group. It demonstrated that MSCC in the cervical spine was associated with deterioratedmotorfunctionwhencomparedwithmsccinthe thoracic and lumbar spine after surgery. It might be explained by patients with relatively high-grade spinal cord Table 4 Comparison of the surgery-related complications and VAS in the three groups. Metastatic location No. No. of complication VAS No Yes P a Pre Post Differences P b Cervical spine 19 14 5 7.32 1.53 2.84 1.21 4.47 1.71 <0.01 Thoracic spine 38 31 7 7.61 2.09 2.18 1.16 5.42 2.12 <0.01 Lumbar spine 38 32 6 0.63 7.42 1.87 2.63 1.55 4.79 2.38 <0.01 P c e e e e >0.05 >0.05 >0.05 e VAS indicates visual analog scale; Pre, preoperation; Post, Postoperation. a Chi-square test. b Paired t test, comparing between pre- and post-operative pain scores in each group. c Dunnett s t test, thoracic spine and lumbar spine groups compared with cervical spine group.
M. Lei et al. / EJSO 41 (2015) 1691e1698 1697 compression and the complicated anatomy in the cervical region. Neurological deficit was recognized as a prognostic factor for postoperative motor function by Cho et al. 1 Rades et al. 13 concluded that ambulatory status was positively associated with motor function outcome in a cohort of 1304 patient with MSCC, but patients included in their study were treated with radiation alone. Notably, the data that postoperative ambulatory status was strongly related to preoperative ambulatory status had been shown in Parks study. 14 In our series, type of primary tumor, preoperative ambulatory status, visceral metastasis, and targeted therapy had significant impact on postoperative survival, whereas ECOG performance status was excluded by Cox model. Type of primary tumor, preoperative ambulatory status, and visceral metastasis are known as predictors for postoperative survival. 1,15,16 ECOG performance status was also included as a prognostic factor in the studies of the patients treated with radiotherapy alone, 17 while it was excluded in those of surgically treated patients, 18 because patients with very poor performance status cannot bear surgery who were excluded in the studies. Recently, several studies have reported improvement in the treatment of solid tumors. Achievements in molecular targeted treatment and antivascular endothelial growth factor therapies have increased the survival of patients experiencing tumors like breast, renal, and lung cancer during the past 10 years, 19e22 globally. 23 Expectedly, targeted therapy was included as a significant prognostic factor for survival in our study. Surgery-related complications occurred in 18.9% of all patients, and five patients (26.3%) were observed in the cervical spine group. 10e30% of patients was reported in other studies. 1,24,25 In the cervical spine metastasis group, operation site infection was observed in two cases, which was successfully treated by continuous irrigation. One patient showed epidural hematoma and required surgical removal. Cerebrospinal fluid leakage was found in one case and required percutaneous lumbar drainage. Pneumonia occurred in one case and was controlled by antibiotics. Preoperative baths for patients, spinal navigation at the cervicothoracic junction, and early mobilization can minimize postoperative complications. 4 Each group experienced improvement in their pain outcome when compare between pre- and 6-month post-operative pain scores, and the differences showed no significance between the three groups. In conclusion, posterior decompression and spine stabilization for MSCC in the cervical spine was found to be effective. Unfortunately, MSCC in the cervical spine is less likely to improve or maintain motor function as compared with MSCC in the thoracic and lumbar spine after posterior decompression and spine stabilization. Its clinical outcomes appear similar to those of the thoracic and lumbar spine metastasis in terms of postoperative survival, surgery-related complication, and pain outcome. A new randomized trial is justified. Conflict of interest statement None. Acknowledgments The work is supported by Application Study of Capital Clinical Characteristics of China (NO. Z131107002213052). References 1. Cho W, Chang UK. Neurological and survival outcomes after surgical management of subaxial cervical spine metastases. Spine 2012;37: E969 77. 2. Nelson KA, Walsh D, Abdullah O, et al. Common complications of advanced cancer. Semin Oncol 2000;27:34 44. 3. Byrne TN. 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