INTRODUCTION
As diagnostic techniques and treatment options have been improving in cancer patients, their life expectancy has been markedly extended 13) . Furthermore, the incidence and prevalence of spinal metastasis have been increasing owing to advances in neuroradiological imaging 9) . Skeletal metastasis is a frequent problem in cancer patients, and spinal metastases account for approximately 50% of bone metastases 1) . Approximately 10% of cancer patients are diagnosed with symptomatic spinal metastasis during their lifetime, and up to 50% of spinal metastasis patients require treatment due to pain or neurological deficits 2 , 12 , 30) .
Untreated spinal metastasis results in the deterioration of life quality due to severe neurological deficits and intractable pain, which can shorten life expectancy with complications. Treatment options for spinal metastasis include radiation therapy, systemic chemotherapy, bisphosphonates, radioisotopes, and surgical management. Each treatment option has advantages and disadvantages; thus individual therapy should be chosen to provide the maximum effect and minimum morbidity. In most cases of spinal metastasis, non-surgical treatment is considered first, but it is difficult to achieve rapid and direct decompression of neural structures with non-surgical treatment. Surgical management of spinal metastasis is a good treatment method for rapid decompression of neural structures and immediate stabilization of the spine. However, surgical management on spinal metastasis is still controversial 6 , 14 , 37) . General indications for surgery are spinal instability, progressive symptomatic deformities, neurological deficits, and intractable pain resistant to other treatments than surgery. As surgery often requires a significant recovery period and complications can occur, the prediction of postoperative survival time is the most critical factor in making the decision for surgery 2) . Therefore, several authors have tried to find factors related with postoperative survival time. Such efforts have been proposed by Tomita et al. 35) , Tokuhashi et al. 32 , 33) , North et al. 25) , Hirabayashi et al. 15) , Arrigo et al. 2) , and Moon et al. 24) .
We reviewed the medical records of 217 patients from 2001 to 2009 in our hospital to find out prognostic factors related to postoperative survival in spinal metastases.
MATERIALS AND METHODS
We reviewed the medical records and radiological images of 217 patients who underwent spinal metastasis operations from 2001 to 2009 at our hospital. The patients with multiple myeloma and lymphoma were excluded because they had systemic hematological disease, not a metastatic spread of a solid tumor. We followed up spinal metastasis patients until May 2011; survivors comprised 16 patients. We analyzed the prognostic factors we believed were related to postoperative survival times. They were gender, age (below 55 years old or above 56 years old groups based on a mean age of 55.5 years), primary tumor growth rate (the slow growth group involves breast cancer, prostate cancer, and thyroid cancer; moderate growth group involves bladder cancer, cervix cancer, melanoma, liposarcoma, ovarian cancer, osteosarcoma, nasopharyngeal carcinoma, renal cell carcinoma, and tongue cancer; the rapid growth group involves gastric cancer, cholangio-carcinoma, colorectal cancer, esophageal cancer, hepatocellular carcinoma, lung cancer, and masses of unknown origin), involved spinal location (cervical, thoracic, and lumbosacral spine), the timing of radiation therapy (preoperative, postoperative, and no radiation), operation type (decompressive laminectomy with or without posterior fixation, corpectomy with anterior fusion, and corpectomy with posterior fixation), preoperative systemic condition (group with Tomita score ≤5 points, group with Tomita score ≥6 points), pre- and postoperative ambulatory function (ambulatory, non-ambulatory), number of spinal metastases (single, multiple), and time to spinal metastasis from the primary cancer diagnosis (below 21 months or above 22 months, based on a mean value of 21.3 months). The occurrence of postoperative complications (complication, no complication) were also included.
In the study cohort, 128 patients were male, and 89 were female. The below 55 years old group comprised 98 patients, and the above 56 years old group included 119 patients. The slow, moderate, and rapid growth tumor groups included 50, 47, and 120 patients, respectively. With regard to histology of the primary cancer, lung cancer (45 patients) was the most common. Colorectal cancer (27 patients), breast cancer (24 patients), hepatocellular carcinoma (20 patients), renal cell carcinoma (17 patients), prostate cancer (13 patients), and thyroid cancer (12 patients) followed ( Table 1 ). Regarding the spinal level of involvement, thoracic spinal metastasis (100 patients) was the most common, and lumbosacral metastasis (65 patients) and cervical metastasis (32 patients) followed. The remaining 20 patients' cancers involved the cervicothoracic spine or thoracolumbar spine simultaneously. Radiation therapy (RT) was undertaken in 53 patients preoperatively, 104 patients postoperatively and 60 patients had no radiation therapy. In no RT group, some patients received chemotherapy instead of RT and the others did not have RT due to poor systemic condition or postoperative complications.
Surgical indications in the present study were as follows : 1) life expectancy longer than 3 months, 2) axial or translational instability due to pathological fractures or tumor invasion, 3) progressed symptomatic spinal metastasis after non-surgical treatment, 4) spinal cord compression with motor weakness (below motor grade IV) or uncontrolled pain.
We classified surgery type into four groups. Decompressive laminectomy was performed in 48 patients, decompressive laminectomy with posterior fixation in 40 patients, corpectomy with anterior fusion in 74 patients, and corpectomy with posterior fixation in 55 patients.
Preoperative systemic condition was based on the Tomita scoring system which evaluates the systemic extent of cancer with primary tumor growth rate, condition of visceral metastasis, and bone metastasis 35) . The Tomita scores range from 2 to 10 points and higher score means poorer systemic status. We classified all the patients into 2 groups; unfavorable vs. favorable. The unfavorable group comprised 137 patients (≥6 points), and the favorable group comprised 80 patients (≤5 points). Pre- and postoperative ambulatory function was divided into 2 groups; ambulatory and non-ambulatory. We defined ambulatory status as Nurick grade 1 to 4. Non-ambulatory status means Nurick grade 5. The preoperative ambulatory group contained 64 patients, and the non-ambulatory group comprised 153 patients. The postoperative ambulatory group included 179 patients, and the non-ambulatory group included 38 patients. The single spinal metastasis group included 106 patients, and the multiple level involvement group included 111 patients. The number of patients who had postoperative complication was 46, and that of no complication group was 171.
The time interval from primary cancer diagnosis to spinal metastasis was divided into 2 groups. Based on a mean value of 21.3 months, the number of patients whose period was less than 21 months was 148, and the number of patients whose period was instalonger than 22 months was 69. We performed Kaplan-Meier analysis to estimate event-time distributions, made comparisons using Log-Rank statistics (Mantel-Cox with SPSS, version 14.0) and tested a Cox proportional hazards model to determine which independent factors prognosticated for postoperative survival. p -values of <0.05 were considered significant.
RESULTS
The mean age of the study cohort at the time of spine surgery was 55.5 years (range 17-83 years). The mean time interval to spinal metastasis after primary cancer diagnosis was 21.3 months (range 0-216 months). The time interval between diagnosis of primary cancer and spinal metastasis was a mean of 5.5 months (range 0-70 months) in lung cancer patients. However, the breast cancer group showed a mean 48.6 months (range 0-216 months) ( Table 1 ). The median values of overall survival times after spinal operation and spinal metastasis diagnosis were 6.0 months [95% confidence interval (CI) : 4.9-7.1 months] and 9.0 months (95% CI : 6.9-11.1 months), respectively. Thyroid cancer patients had the longest values, with 43.0 months (95% CI : 0-92.2 months) after spinal operation and 57.0 months (95% CI : 21.7-99.4 months) after spinal metastasis diagnosis. The group with the shortest durations was the colorectal cancer group, with 5.0 months (95% CI : 1.6-8.4 months) and 8.0 months (95% CI : 1.2-8.8 months) ( Table 2 ) after spinal metastasis diagnosis.
In univariate analysis, statistically significant factors related with longer postoperative survival were gender, primary tumor growth rate, preoperative systemic condition, and pre- and postoperative ambulatory status ( p <0.05) ( Table 3 ). In males, the median survival after surgery was 5.0 months (95% CI : 3.6-6.4 months) and 8.0 months in females (95% CI : 5.5-10.5 months). The median survival of the slow growing tumor group was 12.0 months (95% CI : 2.8-21.2 months), and those of the moderate and rapid growth groups were 6.0 and 5.0 months (95% CIs : 3.3-8.7 months and 3.9-6.1 months), respectively. Regarding preoperative systemic condition, the median survival in patients whose Tomita score was lower than 5 points was 10.0 months (95% CI : 7.1-12.9 months), and that in patients with a Tomita score higher than 6 points was 5.0 months (95% CI : 4.1-5.9 months). Preoperative ambulatory status also was a significant prognostic factor; the median survival time of the walking group was 7.0 months (95% CI : 4.8-9.2 months), and that of the non-ambulatory group was 3.0 months (95% CI : 1.6-4.4 months). Maintained ambulatory function after surgery also was a good prognostic factor. The median survival time was 8.0 months (95% CI : 6.3-9.7 months) in the ambulatory group and 1.0 month (95% CI : 0.5-1.5 months) in the non-ambulatory group. Age, involved spinal location, radiotherapy timing, operation type, number of spinal metastases, time to spinal metastasis from the primary cancer diagnosis, and the occurrence of postoperative complication had no statistical significance ( p >0.05) ( Table 3 ). We performed logistic regressive analysis of the multivariate Cox proportional hazard model with significant factors in univariate analysis ( Table 4 ) ( Fig. 1 ). It showed that preoperative systemic condition [odds ratio (OR) : 1.439, 95% CI : 1.003-2.065, p=0.048] and postoperative ambulation status (OR : 5.397, 95% CI : 3.560-8.181, p <0.001) were prognostic factors associated with longer postoperative survival.
Postoperative complications were found in 46 patients (21.2%). These included acute hematoma in 8 patients, gastrointestinal problems in 4 patients, infection in 20 patients, paraplegia in 1 patient, pulmonary complications in 11 patients, and instrument-related problems in 2 patients ( Table 5 ). The one-month mortality rate was 14.3% (31 patients). Among 46 patients with postoperative complications, 12 patients belonged to the postoperative non-ambulatory group.
DISCUSSION
As diagnostic methods and treatment options for cancer patients have improved, their survival has been extended. Therefore, spinal metastasis can be seen in cancer patients more frequently than in the past 9) . As a result, management of spinal metastasis has become an important issue. In spinal metastasis, the effectiveness of surgical treatment is still controversial 6 , 14 , 37) . Progressive and untreated spinal metastasis may lead to compression fracture of the vertebral body, vertebral column instability, pain due to the nerve root and spinal cord, and significant neurological deficits 19) . In severe cases, it may cause quadriplegia, paraplegia, and urinary incontinence and can also shorten survival with complications. Non-surgical treatment methods are suitable for patients who are ambulatory, who have minimal neurological deficits, or who have pain. However, it is difficult to expect a rapid and direct decompression of neural structures with non-surgical treatment methods. Surgery is undoubtedly the best treatment option for rapid decompression of spinal neural structures and immediate stabilization of the spine 31) . In recent studies, the effectiveness of surgical treatment has been validated 7 , 8 , 11 , 16 , 18 , 21 , 27) . These articles assert that surgery could improve quality of remaining life with maintained ambulatory function, and en bloc resection of a solitary spinal metastasis increases the survival rate. However, surgery can cause dangerous complications leading to significant morbidity and mortality. Furthermore, some complications involve prolonged recovery time and could delay adjuvant therapy. Therefore, we have to consider life expectancy after spinal metastasis surgery in the selection of surgical candidates.
Several studies have attempted to investigate prognostic factors for survival outcome after spinal metastasis surgery 2 , 15 , 24 , 25 , 32 , 33 , 35) . Popular scoring systems for the evaluation of preoperative systemic condition were suggested by Tomita and Tokuhashi. The Tomita scoring system is scored by primary tumor growth rate, condition of visceral metastasis, and bone metastasis 35) . In this report, these factors had statistical significance and different weight. It also suggested treatment strategies for spinal metastasis ranging from wide or marginal excision to supportive care according to Tomita's score and the treatment goal. Tokuhashi et al. 32 , 33) suggested another scoring system and subsequently issued a revised system. Six factors, such as general condition, extra-spinal metastasis, number of vertebral body metastases, grade of major internal organ metastasis, primary cancer type, and level of palsy comprise their scoring system. The factors which comprise the Tomita scoring system are also included in the Tokuhashi scoring system. However, several differences are present between the two scoring systems. Tomita emphasized the grade of primary tumor growth rate and visceral metastasis; however, Tokuhashi placed more weight on the primary tumor growth rate. Colorectal cancer belongs to the rapid tumor growth group in Tomita's classification, but it is included in the good prognosis group in Tokuhashi's classification. North et al. 25) also analyzed prognostic factors related with postoperative survival time. They evaluated multiple factors, such as tumor type, gender, age, preoperative ambulatory grade, continence, radiotherapy, type of surgery, and number of compressed spinal levels, etc. In their study, statistically significant prognostic factors for reduced survival were surgical intervention extending over two or more spinal segments, recurrent or persistent disease after primary radiotherapy involving the operative site, diagnosis other than breast cancer, and a cervical spinal procedure. Hirabayashi et al. 15) identified anatomic sites of primary cancer and postoperative ambulation were associated with longer survival after palliative spinal surgery. Arrigo et al. 2) confirmed that primary tumor type, radio-sensitivity of the tumor and preoperative ambulatory status were significant predictors of survival. Moon et al. 24) found significant factors related with survival were preoperative Eastern Cooperative Oncology Group performance status and Tomita score.
However, most of these studies had a small sample design (less than 100 patients) except for the studies by Arrigo and Moon et al. In our study cohort of 217 patients, the median survival time after spinal operation was 6.0 months. This value is shorter than that of other published reports, which ranged from 7 to 14 months 7 , 10 , 15 , 20 , 25 , 34 , 36) . In the present study, patients with Tomita scores from 8 to 10 comprised 25.3% (55 patients), and 55.3% (120 patients) belonged to the rapid growth tumor group. Patients with poor general condition and rapid growth tumors were associated with short postoperative survival.
In multivariate analysis, preoperative systemic condition and postoperative ambulation status were significant factors. Between these two factors, postoperative ambulatory function was the more powerful prognostic factor ( p <0.001) 4 , 11 , 15) . For this reason, if some patients have a chance to recover their ambulatory function, more aggressive surgical management is recommended. In recent studies on spinal metastasis treatment, it is known that direct decompressive surgery with postoperative radiotherapy is superior to treatment with radiotherapy alone in terms of post-treatment survival 18 , 27) . According to the results with regard to postoperative ambulation, the surgery with or without postoperative radiotherapy group (84%) had better results compared with the radiotherapy only group (57-64%). Furthermore, the chance to regain ambulatory function was higher in the surgery with or without postoperative radiotherapy group (54-62%) compared with the radiotherapy only group (19-26%) 18 , 27) .
In the present study, 115 preoperative non-ambulatory patients (75.2%) regained ambulatory function after surgery. Factors related to postoperative ambulatory function were investigated in some reports 18 , 27) . North et al. 25) found risk factors related with the loss of postoperative ambulation, including loss of preoperative ambulatory ability, recurrent or persistent disease after primary radiotherapy of the operative site, a procedure other than corpectomy, and tumor type other than breast cancer 18 , 27) . Patchell et al. 27) reported surgery and the pretreatment Frankel score to be associated with longer ambulatory time 18) .
Gender, which was not significant in other reports, was a significant factor for postoperative survival in univariate analysis 2 , 15 , 25) . The reason may be the difference in the composition of primary cancer histologies between male and female patients. The proportion of the rapid growth tumor group was higher in male patients (65.6%, 84/128 patients) than in the female (43.8%, 36/89 patients). In multivariate analysis, gender proved to be statistically insignificant.
Primary cancer histology can affect postoperative survival in spinal metastasis because it determines the aggressiveness of spinal metastasis and response to treatment 3 , 15) . Thyroid cancer, prostate cancer, and breast cancer are included in the slow growing tumor groups 2 , 15 , 25 , 32 , 33 , 35) . Median survival times of spinal metastasis according to tumor histology were reported as 2.9-4.7 months in lung cancer, 4.1-6.9 months in colorectal cancer, 21.0-27.1 months in breast cancer, and 6.2 months in hepatocellular carcinoma, in previous articles 2 , 5 , 17 , 26 , 29) . In the present study, postoperative survival was different according to the primary tumor growth rate, but statistical significance was not found.
Regarding the spinal level of involvement, the median survival after surgery of the cervical spinal metastasis group was 4.0 months. The median survival times of the thoracic spinal metastasis and lumbosacral metastasis groups were 6.0 and 8.0 months, respectively. In general, metastases to the cervical spine are known as having worse prognoses than thoracic and lumbosacral metastases because many anatomical structures like the esophagus, trachea, vessels, and nerves are located around the cervical spine and frequently injured intraoperatively 22 , 23 , 28) . However, the involved spinal location had no statistical significance in our series.
The median survival time after surgery of the postoperative RT group (7.0 months) was shown to be longer than the no RT or preoperative RT groups (5.0 months, respectively). The patients in the preoperative RT group were in a more progressed state at the time of surgery than the patients in the postoperative RT group because the surgically removed metastasis had been already irradiated as an initial treatment.
CONCLUSION
As diagnostic tools and treatment methods have improved, the number of spinal metastasis patients has increased. The management of spinal metastasis patients is a very difficult problem. Predicting postoperative life expectancy is an important factor for selecting the appropriate treatment method. In the present study cohort of 217 patients, the overall median survival was 6.0 months following the spine metastasis operation. Preoperative systemic condition and postoperative ambulatory status were statistically significant for postoperative survival time.
1 Aebi M Spinal metastasis in the elderly Eur Spine J 2003 12 Suppl 2 S202 S213 14505120 10.1007/s00586-003-0609-9 PMC3591831
2 Arrigo RT Kalanithi P Cheng I Alamin T Carragee EJ Mindea SA Predictors of survival after surgical treatment of spinal metastasis Neurosurgery 2011 68 674 681 discussion 681 21311295 10.1227/NEU.0b013e318207780c
3 Bilsky MH Lis E Raizer J Lee H Boland P The diagnosis and treatment of metastatic spinal tumor Oncologist 1999 4 459 469 10631690
4 Black P Spinal metastasis : current status and recommended guidelines for management Neurosurgery 1979 5 726 746 392332 10.1227/00006123-197912000-00016
5 Brown PD Stafford SL Schild SE Martenson JA Schiff D Metastatic spinal cord compression in patients with colorectal cancer J Neurooncol 1999 44 175 180 10619502 10.1023/a:1006312306713
6 Byrne TN Spinal cord compression from epidural metastases N Engl J Med 1992 327 614 619 1296600 10.1056/NEJM199208273270907
7 Chaichana KL Pendleton C Sciubba DM Wolinsky JP Gokaslan ZL Outcome following decompressive surgery for different histological types of metastatic tumors causing epidural spinal cord compression. Clinical article J Neurosurg Spine 2009 11 56 63 19569942 10.3171/2009.1.SPINE08657
8 Chaichana KL Woodworth GF Sciubba DM McGirt MJ Witham TJ Bydon A Predictors of ambulatory function after decompressive surgery for metastatic epidural spinal cord compression Neurosurgery 2008 62 683 692 discussion 683-692 18425015 10.1227/01.neu.0000317317.33365.15
9 Cho DC Sung JK Palliative surgery for metastatic thoracic and lumbar tumors using posterolateral transpedicular approach with posterior instrumentation Surg Neurol 2009 71 424 433 18586305 10.1016/j.surneu.2008.02.049
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 1045 1050 14516044 10.1302/0301-620x.85b7.14201
11 Gerszten PC Welch WC Current surgical management of metastatic spinal disease Oncology (Williston Park) 2000 14 1013 1024 discussion 1024, 1029-1030 10929589
12 Harel R Angelov L Spine metastases : current treatments and future directions Eur J Cancer 2010 46 2696 2707 20627705 10.1016/j.ejca.2010.04.025
13 Hayat MJ Howlader N Reichman ME Edwards BK Cancer statistics, trends, and multiple primary cancer analyses from the Surveillance, Epidemiology, and End Results (SEER) Program Oncologist 2007 12 20 37 17227898 10.1634/theoncologist.12-1-20
14 Heidecke V Rainov NG Burkert W Results and outcome of neurosurgical treatment for extradural metastases in the cervical spine Acta Neurochir (Wien) 2003 145 873 880 discussion 880-881 14577009 10.1007/s00701-003-0107-1
15 Hirabayashi H Ebara S Kinoshita T Yuzawa Y Nakamura I Takahashi J Clinical outcome and survival after palliative surgery for spinal metastases : palliative surgery in spinal metastases Cancer 2003 97 476 484 12518372 10.1002/cncr.11039
16 Ibrahim A Crockard A Antonietti P Boriani S Bünger C Gasbarrini A Does spinal surgery improve the quality of life for those with extradural (spinal) osseous metastases? An international multicenter prospective observational study of 223 patients. Invited submission from the Joint Section Meeting on Disorders of the Spine and Peripheral Nerves, March 2007 J Neurosurg Spine 2008 8 271 278 18312079 10.3171/SPI/2008/8/3/271
17 Kim SU Kim do Y Park JY Ahn SH Nah HJ Chon CY Hepatocellular carcinoma presenting with bone metastasis : clinical characteristics and prognostic factors J Cancer Res Clin Oncol 2008 134 1377 1384 18483745 10.1007/s00432-008-0410-6 PMC12161720
18 Klimo P Jr Thompson CJ Kestle JR Schmidt MH A meta-analysis of surgery versus conventional radiotherapy for the treatment of metastatic spinal epidural disease Neuro Oncol 2005 7 64 76 15701283 10.1215/S1152851704000262 PMC1871618
19 Lee IW Ha YS Lee SW Jo TH Baik MW Yoon SH Clinical analysis of 27 cases of metastatic spine tumors J Korean Neurosurg Soc 1988 17 63 72
20 Leithner A Radl R Gruber G Hochegger M Leithner K Welkerling H Predictive value of seven preoperative prognostic scoring systems for spinal metastases Eur Spine J 2008 17 1488 1495 18787846 10.1007/s00586-008-0763-1 PMC2583181
21 Liljenqvist U Lerner T Halm H Buerger H Gosheger G Winkelmann W En bloc spondylectomy in malignant tumors of the spine Eur Spine J 2008 17 600 609 18214553 10.1007/s00586-008-0599-8 PMC2295282
22 Liu JK Rosenberg WS Schmidt MH Titanium cage-assisted polymethylmethacrylate reconstruction for cervical spinal metastasis : technical note Neurosurgery 2005 56 E207 discussion E207 15799818 10.1227/01.neu.0000144494.12738.81
23 Mazel C Balabaud L Bennis S Hansen S Cervical and thoracic spine tumor management : surgical indications, techniques, and outcomes Orthop Clin North Am 2009 40 75 92 vi-vii 19064057 10.1016/j.ocl.2008.09.008
24 Moon KY Chung CK Jahng TA Kim HJ Kim CH Postoperative survival and ambulatory outcome in metastatic spinal tumors : prognostic factor analysis J Korean Neurosurg Soc 2011 50 216 223 22102952 10.3340/jkns.2011.50.3.216 PMC3218181
25 North RB LaRocca VR Schwartz J North CA Zahurak M Davis RF Surgical management of spinal metastases : analysis of prognostic factors during a 10-year experience J Neurosurg Spine 2005 2 564 573 15945430 10.3171/spi.2005.2.5.0564
26 Ogihara S Seichi A Hozumi T Oka H Ieki R Nakamura K Prognostic factors for patients with spinal metastases from lung cancer Spine (Phila Pa 1976) 2006 31 1585 1590 16778693 10.1097/01.brs.0000222146.91398.c9
27 Patchell RA Tibbs PA Regine WF Payne R Saris S Kryscio RJ Direct decompressive surgical resection in the treatment of spinal cord compression caused by metastatic cancer : a randomised trial Lancet 2005 366 643 648 16112300 10.1016/S0140-6736(05)66954-1
28 Riegel T Schilling T Sitter H Benes L Wilke A Gross MW [Analysis of factors affecting the prognosis of vertebral metastases] Zentralbl Neurochir 2002 63 2 6 12098076 10.1055/s-2002-31578
29 Sciubba DM Gokaslan ZL Suk I Suki D Maldaun MV McCutcheon IE Positive and negative prognostic variables for patients undergoing spine surgery for metastatic breast disease Eur Spine J 2007 16 1659 1667 17486376 10.1007/s00586-007-0380-4 PMC2078314
30 Sciubba DM Petteys RJ Dekutoski MB Fisher CG Fehlings MG Ondra SL Diagnosis and management of metastatic spine disease J Neurosurg Spine 2010 13 94 108 20594024 10.3171/2010.3.SPINE09202
31 Steinmetz MP Mekhail A Benzel EC Management of metastatic tumors of the spine : strategies and operative indications Neurosurg Focus 2001 11 e2 16463994 10.3171/foc.2001.11.6.3
32 Tokuhashi Y Ajiro Y Umezawa N Outcome of treatment for spinal metastases using scoring system for preoperative evaluation of prognosis Spine (Phila Pa 1976) 2009 34 69 73 19127163 10.1097/BRS.0b013e3181913f19
33 Tokuhashi Y Matsuzaki H Oda H Oshima M Ryu J A revised scoring system for preoperative evaluation of metastatic spine tumor prognosis Spine (Phila Pa 1976) 2005 30 2186 2191 16205345 10.1097/01.brs.0000180401.06919.a5
34 Tokuhashi Y Matsuzaki H Toriyama S Kawano H Ohsaka S Scoring system for the preoperative evaluation of metastatic spine tumor prognosis Spine (Phila Pa 1976) 1990 15 1110 1113 1702559 10.1097/00007632-199011010-00005
35 Tomita K Kawahara N Kobayashi T Yoshida A Murakami H Akamaru T Surgical strategy for spinal metastases Spine (Phila Pa 1976) 2001 26 298 306 11224867 10.1097/00007632-200102010-00016
36 Ulmar B Huch K Naumann U Catalkaya S Cakir B Gerstner S Evaluation of the Tokuhashi prognosis score and its modifications in 217 patients with vertebral metastases Eur J Surg Oncol 2007 33 914 919 17210240 10.1016/j.ejso.2006.11.018
37 Young RF Post EM King GA Treatment of spinal epidural metastases. Randomized prospective comparison of laminectomy and radiotherapy J Neurosurg 1980 53 741 748 7441333 10.3171/jns.1980.53.6.0741