Topic Highlight Open Access
Copyright ©2014 Baishideng Publishing Group Inc. All rights reserved.
World J Orthop. Jul 18, 2014; 5(3): 262-271
Published online Jul 18, 2014. doi: 10.5312/wjo.v5.i3.262
Scoring system for prediction of metastatic spine tumor prognosis
Yasuaki Tokuhashi, Hiroshi Uei, Masashi Oshima, Department of Orthopaedic Surgery, Nihon University School of Medicine, Itabashi-ku, Tokyo 173-8610, Japan
Yasumitsu Ajiro, Department of Orthopaedic Surgery, Surugadai Nihon University Hospital, Chiyoda-ku, Tokyo 101-8309, Japan
Author contributions: Tokuhashi Y performed the literature review, drafted the article; Uei H and Oshima M helped in the literature review, revised the article critically for important intellectual content; Ajiro Y helped in the literature review, making tables, checked references; all finally approved for print.
Correspondence to: Yasuaki Tokuhashi, MD, Professor, Department of Orthopaedic Surgery, Nihon University School of Medicine, 30-1 Oyaguchi-kamicho, Itabashi-ku, Tokyo 173-8610 Japan. tokuhashi.yasuaki@nihon-u.ac.jp
Telephone: +81-33972-8111 Fax: +81-33972-8201
Received: December 20, 2013
Revised: March 24, 2014
Accepted: May 15, 2014
Published online: July 18, 2014

Abstract

Assessing the prognosis before treatment for metastatic spine tumor is extremely important in therapy selection. Therefore, we review some prognostic scoring systems and their outcomes. Articles with combinations of two keywords among “metastatic spine tumor” and “prognosis”, “score”, “scoring system”, “predicting”, or “life expectancy” were searched for in PubMed. As a result, 236 articles were extracted. Those referring to representative scoring systems about predicting the survival of patients with metastatic spine tumors were used. The significance and limits of these scoring systems, and the future perspectives were described. Tokuhashi score, Tomita score, Baur score, Linden score, Rades score, and Katagiri score were introduced. They are all scoring systems prepared by combining factors that affect prognosis. The primary site of cancer and visceral metastasis were common factors in all of these scoring systems. Other factors selected to influence the prognosis varied. They were useful to roughly predict the survival period, such as, “more than one year or not” or “more than six months or not”. In particular, they were utilized for decision-making about operative indications and avoidance of excessive medical treatment. Because the function depended on the survival period in the patients with metastatic spine tumor, it was also utilized in assessing functional prognosis. However, no scoring system had more than 90% consistency between the predicted and actual survival periods. Future perspectives should adopt more oncological viewpoints with adjustment of the process of treatment for metastatic spine tumor.

Key Words: Metastatic spine tumo, Prognosis evaluation system, Surgical indication, Treatment modality, Decision-making

Core tip: Some representative scoring systems for the prediction of metastatic spine tumor outcome were reviewed. Tokuhashi score, Tomita score, and others were introduced. They were useful to roughly predict the survival period, and were utilized for the purpose of decision-making about operative indications and the avoidance of excessive medical treatment. While the function in the patients was associated with the survival period, it was also useful to assess functional prognosis. However, no scoring system had more than 90% consistency between the predicted and actual survival periods. They also need a stronger oncological perspective with adjustment of the process of treatment.



INTRODUCTION

The objectives of treatment for metastatic spinal tumors are to mitigate pain and paralysis and maximize the activities of daily living (ADL) and quality of life (QOL) during the rest of life. The most important point regarding the therapeutic strategy is to predict the survival period accurately before treatment.

In the classification of the stage of cancers, the malignant tumours (TNM) classification is used for primary lesions, and approximate prediction of the survival period after detection and treatment of the primary lesion has been considered possible in most cancers. However, prediction of the survival period after the appearance of symptoms of spinal metastasis has not been satisfactory, unlike that after the detection and treatment of primary cancer.

Prediction of the survival period before treatment for spinal metastasis is extremely important for the selection of treatment. Naturally, the opinion of physicians of the department treating the primary lesion should be given priority, but their estimation of the survival period is not necessarily accurate, and the treatment should be determined by taking into consideration the estimations of orthopedists and radiologists, who are also directly involved in the treatment. For this purpose, some prognosis evaluation methods have also been developed by spine surgeons and radiologists, and scoring systems by which factors that affect the survival period are scored in an additive manner have been reported to be useful for assessing the prognosis.

Therefore, to evaluate the clinical significance and limitations in the prognostic scoring systems for metastatic spine tumors, we reviewed them and their validation studies that have been reported to date. Furthermore, it was verified which scoring system was the best. The review was conducted as follows; the literature was searched in PubMed using two-word combinations of “metastatic spine tumor” with “prognosis”, “score”, “scoring system”, “predicting”, and “life expectancy” as index terms. As a result, 236 papers were extracted. We checked their contents and describe representative scoring systems that correspond to “scoring systems for the prognosis of patients with metastatic spinal tumors” with comments on their significance and limitations. The representative prognostic scoring systems which we introduced were cited on PubMed more than at least five times. Also, as a result, it was considered the future of the prognostic scoring systems.

REPRESENTATIVE PROGNOSTIC SCORING SYSTEMS
Tokuhashi score

This system was reported by Tokuhashi et al[1-3] in 1989 as a “scoring system for the preoperative evaluation of a patient’s prognosis with a metastatic spinal tumor”. These papers have become landmark articles concerning prognostic scoring systems for patients with metastatic spinal tumors. A revised version was published in 2005[4], and the results of a prospective study in which the treatment was selected using this revised version were reported in 2009[5].

This scoring system consists of 6 items considered to affect the outcome (general condition[6], number of bone metastases other than spinal metastases, number of spinal metastases, type of the primary lesion, presence or absence of metastases to major organs, and state of paralysis). The survival periods were predicted from the total score using prognostic criteria (Tables 1 and 2). According to the original version, the estimated survival period was ≤ 3 mo when the total score was 0-5, ≤ 12 mo when the total score was ≤ 8, and ≥ 12 mo when the total score was ≥ 9. In the revised version, the staging of the primary lesion was changed from 3 (0-2) to 6 (0-5) levels, and the survival period was predicted to be ≤ 6 mo when the total score was 0-8, ≥ 6 mo when the total score was 9-11, and ≥ 1 year when the total score was ≥ 12.

Table 1 Tokuhashi score original (1990)[1-3].
Predictive factorScore (points)
General condition (KPS)
Poor (KPS 10%-40%)0
Moderate (KPS 50%-70%)1
Good (KPS 80%-100%)2
Number of extraspinal bone metastases foci
≥ 30
1-21
02
Number of metastases in the vertebral body
≥ 30
21
12
Metastases to the major internal organs
Unremovable0
Removable1
No metastases2
Primary site of the cancer
Lung, stomach0
Kidney, liver, uterus, others, unidentified1
Thyroid, prostate, breast, rectum2
Spinal cord palsy
Complete (Frankel A, B)0
Incomplete (Frankel C, D)1
None (Frankel E)2
Total pointsMean survival periods
0-5 ≤ 3 mo
6-8 ≤ 12 mo
9-12 ≤ 12 mo
Table 2 Revised Tokuhashi score (2005)[4].
Predictive factorScore (points)
General condition (KPS)
Poor (KPS 10%-40%)0
Moderate (KPS 50%-70%)1
Good (KPS 80%-100%)2
Number of extraspinal bone metastases foci
≥ 30
1-21
02
Number of metastases in the vertebral body
≥ 30
21
12
Metastases to the major internal organs
Unremovable0
Removable1
No metastases2
Primary site of the cancer
Lung, osteosarcoma, stomach, bladder, esophagus, pancreas0
Liver, gallbladder, unidentified1
Others2
Kidney, uterus3
Rectum4
Thyroid, prostate, breast, carcinoid tumor5
Spinal cord palsy
Complete (Frankel A, B)0
Incomplete (Frankel C, D)1
None (Frankel E)2
Total pointsMean survival periods
0-8< 6 mo
9-11≥ 6 mo
12-15≥ 12 mo

In the original version, each item was scored as 0-2, but the hazard ratio was not evaluated for the weighting of the factors. Statistically, the survival period was retrospectively shown to be correlated with the total score in 47 surgical cases[1,2]. With both the original and the revised versions, relatively broad prognostic criteria were prepared, and their clinical application was proposed.

While this scoring system was insufficient on statistical evaluation, the factors selected as affecting the survival period were relatively simple and easy to examine. In addition, it contained no factor concerning therapeutic intervention and was flexible on application. For this reason, it was applied for validation in various countries, and relatively favorable results have been reported[7-9].

Chen et al[10] reported that the revised Tokuhashi score was the most practical and provided the most accurate prognosis in 41 patients with spinal metastasis of hepatocellular carcinoma among 4 scoring systems: the revised score, Tomita score, Bauer score, and revised van der Linden score. Moreover, they suggested that the serum albumin and lactate dehydrogenase (LDH) levels are useful as prognostic factors.

Tokuhashi et al[5] also prospectively evaluated 183 patients treated according to the revised version, and reported that the prediction was in agreement with the actual survival period in 87.9% of the patients. In the revised version, the survival period was classified into 3 levels with 6 mo and 1 year, which are clinically important points, as benchmarks. According to these broad criteria, the prognoses for the moderate and favorable prognosis groups partially overlapped, but a score of 9-11 was erroneously converted to a survival period of 6 mo to 1 year in some papers[11-14], in which the agreement rate between the prognosis and actual survival period was low.

In addition, the rate of agreement between the predicted and actual survival periods differs depending on the type of primary lesion, and the usefulness of the criteria has been suggested to vary. Yamashita et al[15] (2011) reported that the predicted and actual survival periods agreed in 67 (79%) of 85 patients followed-up for 1 year or longer. In addition, they reported that the Tokuhashi score was useful regardless of the selected treatment. However, they observed that low scores were closely correlated with poor outcomes but that the outcome was more often poorer than predicted based on the score concerning the kidney, and suggested that the score allocation to the kidney was disproportionately heavy. On the other hand, Hessler et al[16] (2011) evaluated 76 patients who underwent surgery for spinal metastasis of lung cancer, and argued that the agreement rate between the survival period predicted according to the revised Tokuhashi score and the actual survival period was 67.1% and that the criteria did not reflect recent improvements in treatments for spinal metastases of cancer. They reported that some patients even with spinal metastasis of lung cancer survived for 1 year or longer and that the outcome was relatively favorable in those aged 50 years or less, those with metastasis in the lumbar spine, and those with no paralysis. Tokuhashi et al[5] basically agreed with Hessler et al[16], admitting that treatments had improved during the 13 years since the revised scoring system had been prepared and that some patients with spinal metastasis of lung cancer had survived for 2 years or longer. However, they maintained that the prognosis of patients with spinal metastasis of lung cancer is basically poor and that the precision of the score should be evaluated by including patients who tolerated only conservative treatments as well as those who underwent surgery[17].

Some papers focused on the accuracy of differentiation of good-prognosis, poor-prognosis, and intermediate groups. Quraishi et al[18] (2013) reported that 201 surgical cases could be differentiated into poor-, moderate-, and good-prognosis groups, that the agreement rate with the actual survival period was 64% or higher in each group and 66% in all patients, and that the usefulness of the score was moderate. However, in the 142 surgical cases reported by Pointillart et al[19] (2011), the agreement rate between the predicted and actual survival rates was 60% or lower with either the original or the revised version.

There have also been studies comparing the original and revised versions. Wang et al[20] (2012) considered that the revised version was particularly useful for the prognosis of patients with metastases of prostate and breast cancers and that the original version was excellent for the prognosis of patients with metastases of colon cancer. In addition, their usefulness was insufficient concerning metastases of lung or kidney cancers, and the overall accuracy was higher for the revised than the original version. However, Liang et al[21] (2013) reported that the original version was more useful than the revised version or Tomita score.

Kostuik[22] (1997) added 3 items: the radiographic appearance of the metastatic lesion, degree of kyphosis of the secondary lesion, and rate of canal compromise secondary to the metastatic lesion, to the original version and reported the usefulness of this partially modified scoring system with a full mark of 18.

Tomita score

Tomita et al[23] and Kawahara et al[24] retrospectively evaluated 67 patients including those treated conservatively and developed a new scoring system in 2001 (Table 3).

Table 3 Tomita score (2001)[23,24].
Prognostic factorsPoints
Primary tumor
Slow growth (breast, thyroid, etc.)1
Moderate growth (Kidney, uterus, etc.)2
Rapid growth (Lung, stomach, etc.)4
Visceral metastases
Treatable2
Untreatable4
Bone metastases
Solitary or isolated1
Multiple2
Total pointsPredicted prognosis
2-4> 2 yr
4-61-2 yr
6-86-12 mo
8-10< 3 mo

Since the score of each item of the original Tokuhashi scoring system lacked weighting, each factor of each item was weighted by Cox hazard analysis in the new scoring system. Paralysis, which was considered not to affect the survival period, was excluded, and the new scoring system was simplified compared with Tokuhashi’s. In addition, the expected survival period and indicated treatment were 2 years or longer and en bloc excision, respectively, when the total score was 2-4, 1-2 years and debulking when it was 4-6, 6-12 mo and palliative decompression when it was 6-8, and 3 mo or less and terminal care when it was 8-10.

This scoring system is patient-centered and is often used along with Tokuhashi’s system for evaluation of the surgical indication, and its usefulness has been evaluated in many reports[25-32].

Bauer[33] (2002) reported that this scoring system successfully differentiated poor- and good-prognosis groups but pointed out that it downplayed pain and paralysis, lacked specificity for impending paralysis, and disregarded indications for many conservative treatments and palliative surgery due to an excessive emphasis on aggressive surgical treatments.

Baur scoring system

In 1995, Bauer et al[34] developed a simple scoring system by studying 153 cases of limb bone metastases and 88 cases of spinal metastases by combining 3 influential items selected by univariate analysis and Cox regression analysis of prognostic factors: the site of the primary tumor, metastatic load, and pathologic fracture (Table 4). As a result, the 1-year survival rate was predicted to be 0% when the score was 0-1 (all patients die within 6 mo), 25% when it was 2-3, and 50% when it was 4-5.

Table 4 Baur score original.
Positive prognostic factorsScore (Points)
No visceral metastases1
Absence of pathologic fracture1
solitary skeletal metastasis1
No lung cancer1
Primary tumor = breast, kidney, lymphoma, multiple myeloma1
Total score (points)1-yr survival rate (%)
0-10% (< 6 mo survival)
2-325%
4-550%

Disadvantages of this scoring system are that the judgment of pathologic fracture is difficult in the spine and that it was developed based on a multi-center collaborative study restricted to surgical cases with large variations in the surgical indications and procedures among the facilities.

However, Leithner et al[35] (2008) and Wibmer et al[36] (2011) considered that, of the 7 scoring systems including the Tokuhashi, Tomita, and Linden scoring systems, those other than the Bauer scoring system were also useful until 4 years after treatment. However, they reported that the Bauer score and modified Bauer score (Table 5), in which the item concerning the presence or absence of pathologic fracture was excluded, were superior for the prognosis after 4 or more years and differentiation between the good- and moderate-prognosis groups[35,36]. According to the modified Bauer score, the median OS and indications for treatment are 4.8 mo and no surgical indication, respectively, when the score is 0-1, 18.3 mo and palliative surgery from a posterior approach when the score is 2, and 28.4 mo and control by a combination of anterior and posterior approaches when the score is 3-4.

Table 5 Modified Baur score.
Positive prognostic factorsPoints
No visceral metastases1
No lung cancer1
Primary tumor = breast, kidney, lymphoma, multiple myeloma1
One solitary skeletal metastasis1
Total pointsMedian overall survival
0-14.8 mo
218.2 mo
3-428.4 mo
Van der Linden scoring system

In 2005, van der Linden et al[37] devised a scoring system consisting of 3 items: Karnofsky’s performance status, type of primary lesion (lung cancer, breast cancer, prostate cancer, others), and the presence or absence of visceral metastasis, by studying 342 cases of spinal metastasis (Table 6), and reported that it was effective in 73% of the patients[37].

Table 6 Linden score.
Prognostic factorsPoints
Karnofsky performance status
80-1002
50-701
20-400
Primary tumor
Breast3
Prostate2
Lung1
Other0
Visceral metastases
No1
Yes0
Total pointsMean overall survival
0-3 (n = 116)4.8 mo
4-5 (n = 164)13.1 mo
6 (n = 62)18.3 mo
Rades score

Rades et al[38] prepared a few scoring systems on the basis of data obtained from patients who underwent radiation therapy for spinal cord compression by metastatic tumors, all by Cox proportional-hazards survival analysis. The first and largest of them was derived from 1852 cases (2008, Table 7)[38], followed by one derived from a prospective study of 439 cases (2010, Table 7)[39] and a scoring system based on the type of cancer. There is also a scoring system for metastases of prostate cancer (2012, Table 8)[40], one for metastases of breast cancer (2013, Table 9)[41], and one for unknown primary lesions by Douglas et al[42] (2012, Table 10).

Table 7 Rades score.
Prognostic factorScore (points)
Type of primary tumor
Breast cancer8
Prostate cancer7
Myeloma/lymphoma9
Lung cancer3
Other tumors4
Other bone metastases at the time of RT
Yes5
No7
Visceral metastases at the time of RT
Yes2
No8
Interval from tumor diagnosis to MSCC
≤ 15 mo4
> 15 mo7
Ambulatory status before RT
Ambulatory7
Nonambulatory3
Time of developing motor deficits before RT
1-7 d3
8-14 d6
> 14 d8
Total score6-mo survival (%)
20-30 (n = 237)16
31-35 (n = 162)48
36-46 (n = 253)81
Table 8 Rades score for prostate cancer metastases.
Prognostic factorScore (points)
ECOG performance status
1-29
3-44
Ambulatory status prior to RT
Not ambulatory4
Ambulatory before RT8
Other bone metastases
No7
Yes5
Visceral metastases
No8
Yes2
Interval from cancer diagnosis to RT
≤ 15 mo5
> 15 mo7
Score groupSurvival at 6 mo (%)
20-24 (n = 58)6.5-7.4
25-34 (n = 189)44.6-45.4
35-39 (n = 189)94.7-95.8
Table 9 Rades score for breast cancer metastases.
Prognostic factorScore (points)
ECOG performance status
1-29
3-45
Ambulatory status prior to RT
Not ambulatory4
Ambulatory before RT8
Other bone metastases
No8
Yes7
Visceral metastases
No9
Yes4
Interval from tumor diagnosis to radiotherapy of MSCC
≤ 15 mo6
> 15 mo8
Time of developing motor deficits
1-7 d4
> 7 d8
Total scoreSurvival at 6 mo (%)
30-3512-14
36-4041-46
41-4574-77
46-5098-99
Table 10 Douglas score for unknown primary metastases.
Prognostic factorScore (points)
ECOG performance status
1-26
3-42
Ambulatory status prior to RT
Not ambulatory2
Ambulatory before RT4
Visceral metastases
No5
Yes0
Time of developing motor deficits
1-7 d1
> 7 d5
Score groupSurvival at 6 mo (%)
< 14 (n = 112)5-7
14-16 (n = 26)38-41
> 16 (n = 24)91-92

All are for the evaluation of conditions that are indications of radiation therapy for spinal cord compression by metastatic tumors at an advanced stage and consist of other bone metastases at the time of RT, visceral metastases at the time of RT, the interval from tumor diagnosis to metastatic spinal cord compression (MSCC), ambulatory status before RT, and time of developing motor deficits before RT, but they vary in their combination and allocation of scores depending on the cancer type. Important points regarding this scoring system are that its application is restricted to an advanced stage of spine metastases of cancer with impending paralysis, and that the prediction of the outcome for patients with some cancer types is impossible with a single pattern. In addition, the therapeutic options are restricted to radiation therapy, and the scoring systems cannot be applied to the selection of diversified treatments for spinal metastases of cancer.

Katagiri score

Katagiri score is a scoring system prepared retrospectively by Cox proportional-hazards analysis of 350 cases of skeletal metastases (2005, Table 11)[43]. Its unique characteristics not observed in other scoring systems are that the history of chemotherapy before the crises of metastases is incorporated and bone metastases are captured as metastases of the entire skeleton rather than of the spine alone. For this reason, only 37 patients (10.6%) underwent surgery due to spinal metastases.

Table 11 Katagiri score.
Prognostic factorScore
Primary lesion
Rapid growth( Hepatocellular carcinoma, gastric carcinoma, lung carcinoma)3
Slow growth( Breast carcinoma, prostate carcinoma, multiple myeloma, malignant lymphoma, thyroid carcinoma)0
Moderate growth( Other carcinoma and sarcoma)2
Visceral or cerebral metastases2
Performance status (ECOG) 3 or 41
Previous chemotherapy1
Multiple skeletal metastases1
Total score (n = 350)6 and 12 mo survival rate (%)
0-297.9; 89.1
3-570.6; 48.8
6-831.3; 10.9

The greatest demerit of this scoring system is that it includes the history of chemotherapy, a therapeutic intervention, and that the evaluation of the degree of intervention and sensitivity for each cancer is unclear. It is likely to be affected by individual variation in attending physicians and has major problems with versatility and objectivity.

SIGNIFICANCE OF, AND PROBLEMS WITH, SCORING SYSTEMS

All scoring systems for the prognosis of patients with metastatic spinal tumors are composed of combinations of factors that affect the survival periods. Among these prognostic factors, the type of primary lesion and visceral metastases are included in all scoring systems, and other factors are arbitrarily selected. Rades et al[38-41] and Douglas et al[42] attached importance to functional factors and reported a scoring system incorporating the ambulatory ability before treatment and speed of progression of paralysis, but many scoring systems, including one by Tomita et al[23], Bauer et al[34], van der Linden et al[37] and Katagiri et al[43], totally disregarded paralysis. This wide variation is considered to have been due to differences in the patients evaluated for the preparation of the scoring systems. The patients studied by Rades et al[38] consisted entirely of those who had progressive spinal cord paralysis and underwent radiation therapy, and included a high percentage of those with a poor prognosis in whom the surgical indication could not be evaluated from the beginning. Therefore, the prognosis of patients with progressive paralysis based on this system is considerably poorer than that by other scoring systems. As suggested by Kawai et al[44] (2013), reevaluation of prognostic factors is considered necessary based on the historical background that asymptomatic metastases detected in an early stage began to be treated as new metastases.

At any rate, it is certain that such additive scoring systems combining factors considered to affect the outcome are useful for rough estimation of the survival period in terms of “6 mo or longer or less than 6 mo” and “1 year or longer or less than 1 year”. At least, they are much more reliable than the prognosis based on a single prognostic factor.

However, which of the scoring systems is the best remains unclear. There have been few validation studies concerning the prognostic accuracy of scoring systems other than Tokuhashi’s system and Tomita’s system, which succeeded it. At least, all scoring systems have limitations, and there is no system by which the agreement rate between the predicted and actual survival periods is 90% or higher.

Scoring systems are practically used most frequently for the evaluation of surgical indications[25-32,45-53]. Some scoring systems were prepared to avoid selecting excessive treatments for patients with a poor prognosis[54-56]. Rades et al[56] (2013) examined risk factors for dying within two months after radiotherapy. As a result, for those with 24 points or more, 96.0% died within two months after radiotherapy, and the specificity was 99.8% (Table 12)[56]. Scoring systems are often important for preventing the unnecessary widening of surgical indications in particular. As cost-effectiveness has recently begun to be demanded in medical care, evaluation in this regard has also become necessary.

Table 12 Rades risk score for death within 2 mo after radiotherapy.
CharacteristicScore( points)
ECOG performance status
20
3-44
Tumor type
Breast cancer1
Prostate cancer2
Myeloma/lymphoma1
Lung cancer3
Other3
Further bone metastases
No1
Yes3
Visceral metastases
No1
Yes4
Interval from cancer diagnosis to MSCC
≤ 15 mo3
> 15 mo1
Ambulatory status prior to RT
Not ambulatory4
Ambulatory before RT1
Time of developing motor deficits
1-7 d4
> 7 d1

Moreover, because of the nature of the disease, the functional prognosis depends on the survival period. Therefore, scoring systems have also begun to be used for assessing the functional prognosis. Tang et al[57] (2007) used the Tokuhashi score to determine the indications of rehabilitation by admission on the basis of its correlation with the functional independence measure (FIM). In addition, Yamashita et al[58] (2008) and Putz et al[59] (2008) reported that the Tokuhashi score can also be used for the prediction of functional recovery due to its correlation with neurological recovery. Rades et al[60,61] also reported that the ambulatory ability after treatment can be predicted using factors related to the survival period of prognostic scoring systems.

Under these circumstances, scoring systems have begun to be applied clinically as outcome measures[62,63], but no scoring system is satisfactory regarding the validity, reliability, or responsiveness.

On the other hand, there is criticism against limiting treatment alternatives based on simple numerical indices of such scoring systems[64-66]. Gasbarrini et al[64,65] attached importance to the evaluation of individual patients in consideration of the sensitivity, particularly to adjuvant therapies, and proposed a treatment algorithm emphasizing the multidisciplinary selection of treatments including scoring systems. Paton et al[67] also proposed a therapeutic strategy taking the location level (L), mechanical instability (M), neurology (N), oncology (O), patient fitness, prognosis, and prior therapy (P) into consideration.

FUTURE SCORING SYSTEMS

Scoring systems for the prognosis of patients with metastatic spinal tumors have been prepared by frontline orthopedists and radiologists from clinical viewpoints. Many of these scoring systems were proposed when sufficient systematic treatments were not performed for metastatic spinal tumors and have been used as simple and excellent tools[68]. However, as metastatic tumors have also begun to be treated aggressively, the scoring systems have become unfit for the actual situation with the diversification of treatments. Therefore, challenges for future scoring systems need some discussion.

First, oncological viewpoints, which conventional scoring systems lacked, should be incorporated with progress in cancer treatments. They include: (1) consideration of the stage and level of the disease; (2) evaluation according to the nature of the primary cancer; (3) introduction of serum levels of prognostic markers; and (4) multidisciplinary approaches, among others.

Regarding the disease stage, metastatic spinal tumors varying from those in the asymptomatic period, those in the period of progression of spinal paralysis, to those in the terminal period must be handled due to the improvement in the metastasis-detection power, but they cannot be evaluated uniformly with a single scoring system. At least, the disease stage should be specified, and scoring systems should be prepared and used accordingly. In addition, little attention has been paid to the level of involvement, and the lack of an appropriate scoring system for the cervical spine, which is infrequently affected, has been suggested as a problem to be addressed in the future[69].

Concerning evaluation according to the nature of the primary cancer, Chen et al[10] and Morgen et al[51] (2013) reported that, in some cancer types, the prognosis of patients with spinal metastases was significantly improved during a period of 5 years due to rapid improvements in the treatment, and stressed that the improvements in the prognosis should be reflected in scoring systems. The necessity of scoring systems for different types of cancer has been discussed for some time[70-72], and the development of those for different cancer types is expected to be promoted by the accumulation of cases and systematization of treatments. In this process, it is possible to incorporate specific markers of particular types of cancer as prognostic factors. Crnalic et al[73] reported a specialized scoring system for prostate cancer metastases including prostate-specific antigen (Table 13).

Table 13 Crnalic score for prostate cancer metastases.
Prognostic factorScore (points)
Hormone status
Hormone native2
Hormone refractory0
KPS (%)
80-1002
≤ 700
Visceral metastasis
Absent1
Present0
PSA (ng/mL)
Hormone native1
Hormone refractory
< 2001
≥ 2000
Total pointsMedian overall survival
0-13 mo
2-416 mo
5-661.7 mo

Finally, attention to multidisciplinary approaches is necessary instead of preparing scoring systems on the basis of the results of, or for the selection of, a single treatment. Gregory et al[74] proposed that prognostic scoring systems should be changed by introducing anti-vascular endothelial growth factor. The introducti ion of such new treatments may exert favorable effects on other conventional treatments[75]. Therefore, the importance of considering multidisciplinary treatments must be stressed.

Footnotes

P- Reviewers: Liu HM, Verlaan JJ S- Editor: Ji FF L- Editor: A E- Editor: Lu YJ

References
1.  Tokuhashi Y, Kawano H, Ohsaka S, Matsuzaki H, Toriyama S. [A scoring system for preoperative evaluation of the prognosis of metastatic spine tumor (a preliminary report)]. Nihon Seikeigeka Gakkai Zasshi. 1989;63:482-489.  [PubMed]  [DOI]  [Cited in This Article: ]
2.  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.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 531]  [Cited by in F6Publishing: 435]  [Article Influence: 12.8]  [Reference Citation Analysis (0)]
3.  Tokuhashi Y, Matsuzaki H, Kawano H, Sano S. [The indication of operative procedure for a metastatic spine tumor: a scoring system for the preoperative evaluation of the prognosis]. Nihon Seikeigeka Gakkai Zasshi. 1994;68:379-389.  [PubMed]  [DOI]  [Cited in This Article: ]
4.  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.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 796]  [Cited by in F6Publishing: 766]  [Article Influence: 40.3]  [Reference Citation Analysis (0)]
5.  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.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 143]  [Cited by in F6Publishing: 138]  [Article Influence: 9.2]  [Reference Citation Analysis (0)]
6.  Karnofsky DA. Clinical evaluation of anticancer drugs: Cancer chemotherapy. Gann Monograph. 1967;2:223-231.  [PubMed]  [DOI]  [Cited in This Article: ]
7.  Enkaua EA, Doursounian L, Chatellier G, Mabesoone F, Aimard T, Sallant G. Vertebral metastases, a critical appreciation of the preoperative prognostic Tokuhashi score in a series of 71 cases. Spine. 1997;22:2293-2298.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 126]  [Cited by in F6Publishing: 132]  [Article Influence: 4.9]  [Reference Citation Analysis (0)]
8.  Riegel T, Schilling T, Sitter H, Benes L, Wilke A, Gross MW, Bertalanffy H. [Analysis of factors affecting the prognosis of vertebral metastases]. Zentralbl Neurochir. 2002;63:2-6.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 16]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
9.  Ulmar B, Richter M, Cakir B, Muche R, Puhl W, Huch K. The Tokuhashi score: significant predictive value for the life expectancy of patients with breast cancer with spinal metastases. Spine (Phila Pa 1976). 2005;30:2222-2226.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 59]  [Cited by in F6Publishing: 59]  [Article Influence: 3.1]  [Reference Citation Analysis (0)]
10.  Chen H, Xiao J, Yang X, Zhang F, Yuan W. Preoperative scoring systems and prognostic factors for patients with spinal metastases from hepatocellular carcinoma. Spine (Phila Pa 1976). 2010;35:E1339-E1346.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 36]  [Cited by in F6Publishing: 36]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
11.  Majeed H, Kumar S, Bommireddy R, Klezl Z, Calthorpe D. Accuracy of prognostic scores in decision making and predicting outcomes in metastatic spine disease. Ann R Coll Surg Engl. 2012;94:28-33.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
12.  Hernandez-Fernandez A, Vélez R, Lersundi-Artamendi A, Pellisé F. External validity of the Tokuhashi score in patients with vertebral metastasis. J Cancer Res Clin Oncol. 2012;138:1493-1500.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 19]  [Cited by in F6Publishing: 18]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
13.  Padalkar P, Tow B. Predictors of survival in surgically treated patients of spinal metastasis. Indian J Orthop. 2011;45:307-313.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 32]  [Cited by in F6Publishing: 33]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
14.  Tabouret E, Cauvin C, Fuentes S, Esterni B, Adetchessi T, Salem N, Madroszyk A, Gonçalves A, Casalonga F, Gravis G. Reassessment of scoring systems and prognostic factors for metastatic spinal cord compression. Spine J. 2013;Oct 9; Epub ahead of print.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 54]  [Cited by in F6Publishing: 65]  [Article Influence: 7.2]  [Reference Citation Analysis (0)]
15.  Yamashita T, Siemionow KB, Mroz T, Podichetty V, Lieberman IH. A prospective analysis of prognostic factors in patients with spinal metastases: Use of the revised Tokuhashi score. Spine. 2011;36:910-917.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 57]  [Cited by in F6Publishing: 54]  [Article Influence: 4.2]  [Reference Citation Analysis (0)]
16.  Hessler C, Vettorazzi E, Madert J, Bokemeyer C, Panse J. Actual and predicted survival time of patients with spinal metastases of lung cancer: evaluation of the robustness of the Tokuhashi score. Spine (Phila Pa 1976). 2011;36:983-989.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 56]  [Cited by in F6Publishing: 57]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
17.  Tokuhashi Y, Oshima M, Uei H. Letter to editor. Spine. 2012;37:429.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 3]  [Article Influence: 0.3]  [Reference Citation Analysis (0)]
18.  Quraishi NA, Manoharan SR, Arealis G, Khurana A, Elsayed S, Edwards KL, Boszczyk BM. Accuracy of the revised Tokuhashi score in predicting survival in patients with metastatic spinal cord compression (MSCC). Eur Spine J. 2013;22 Suppl 1:S21-S26.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 68]  [Cited by in F6Publishing: 71]  [Article Influence: 6.5]  [Reference Citation Analysis (0)]
19.  Pointillart V, Vital JM, Salmi R, Diallo A, Quan GM. Survival prognostic factors and clinical outcomes in patients with spinal metastases. J Cancer Res Clin Oncol. 2011;137:849-856.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
20.  Wang M, Bünger CE, Li H, Wu C, Høy K, Niedermann B, Helmig P, Wang Y, Jensen AB, Schättiger K. Predictive value of Tokuhashi scoring systems in spinal metastases, focusing on various primary tumor groups: evaluation of 448 patients in the Aarhus spinal metastases database. Spine (Phila Pa 1976). 2012;37:573-582.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 46]  [Cited by in F6Publishing: 45]  [Article Influence: 3.8]  [Reference Citation Analysis (0)]
21.  Liang T, Wan Y, Zou X, Peng X, Liu S. Is surgery for spine metastasis reasonable in patients older than 60 years? Clin Orthop Relat Res. 2013;471:628-639.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 34]  [Cited by in F6Publishing: 34]  [Article Influence: 3.1]  [Reference Citation Analysis (0)]
22.  Kostuik JP The development of a preoperative scoring assessment system of metastatic spine disease. Proceeding of The 12th Annual Meeting of North American Spine Society;. 1997;Oct 22-25; New York.  [PubMed]  [DOI]  [Cited in This Article: ]
23.  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.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 973]  [Cited by in F6Publishing: 900]  [Article Influence: 39.1]  [Reference Citation Analysis (0)]
24.  Kawahara N, Tomita K, Murakami H, Demura S. Total en bloc spondylectomy for spinal tumors: surgical techniques and related basic background. Orthop Clin North Am. 2009;40:47-63, vi.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 102]  [Cited by in F6Publishing: 104]  [Article Influence: 6.9]  [Reference Citation Analysis (0)]
25.  Zairi F, Arikat A, Allaoui M, Marinho P, Assaker R. Minimally invasive decompression and stabilization for the management of thoracolumbar spine metastasis. J Neurosurg Spine. 2012;17:19-23.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 61]  [Cited by in F6Publishing: 62]  [Article Influence: 5.2]  [Reference Citation Analysis (0)]
26.  Walter J, Reichart R, Waschke A, Kalff R, Ewald C. Palliative considerations in the surgical treatment of spinal metastases: evaluation of posterolateral decompression combined with posterior instrumentation. J Cancer Res Clin Oncol. 2012;138:301-310.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 22]  [Article Influence: 1.7]  [Reference Citation Analysis (0)]
27.  Zhang D, Xu W, Liu T, Yin H, Yang X, Wu Z, Xiao J. Surgery and prognostic factors of patients with epidural spinal cord compression caused by hepatocellular carcinoma metastases: retrospective study of 36 patients in a single center. Spine (Phila Pa 1976). 2013;38:E1090-E1095.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 31]  [Cited by in F6Publishing: 29]  [Article Influence: 2.6]  [Reference Citation Analysis (0)]
28.  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.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 55]  [Cited by in F6Publishing: 56]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
29.  Omeis I, Bekelis K, Gregory A, McGirt M, Sciubba D, Bydon A, Wolinsky JP, Gokaslan Z, Witham T. The use of expandable cages in patients undergoing multilevel corpectomies for metastatic tumors in the cervical spine. Orthopedics. 2010;33:87-92.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 14]  [Cited by in F6Publishing: 16]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
30.  Sundaresan N, Rothman A, Manhart K, Kelliher K. Surgery for solitary metastases of the spine: rationale and results of treatment. Spine (Phila Pa 1976). 2002;27:1802-1806.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 190]  [Cited by in F6Publishing: 164]  [Article Influence: 7.5]  [Reference Citation Analysis (0)]
31.  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;34:431-435.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 72]  [Cited by in F6Publishing: 62]  [Article Influence: 4.1]  [Reference Citation Analysis (0)]
32.  Hu Y, Xia Q, Ji J, Miao J. One-stage combined posterior and anterior approaches for excising thoracolumbar and lumbar tumors: surgical and oncological outcomes. Spine (Phila Pa 1976). 2010;35:590-595.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 28]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
33.  Bauer H, Tomita K, Kawahara N, Abdel-Wanis ME, Murakami H. Surgical strategy for spinal metastases. Spine (Phila Pa 1976). 2002;27:1124-1126.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 36]  [Cited by in F6Publishing: 42]  [Article Influence: 1.9]  [Reference Citation Analysis (0)]
34.  Bauer HC, Wedin R. Survival after surgery for spinal and extremity metastases. Prognostication in 241 patients. Acta Orthop Scand. 1995;66:143-146.  [PubMed]  [DOI]  [Cited in This Article: ]
35.  Leithner A, Radl R, Gruber G, Hochegger M, Leithner K, Welkerling H, Rehak P, Windhager R. Predictive value of seven preoperative prognostic scoring systems for spinal metastases. Eur Spine J. 2008;17:1488-1495.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 201]  [Cited by in F6Publishing: 213]  [Article Influence: 13.3]  [Reference Citation Analysis (0)]
36.  Wibmer C, Leithner A, Hofmann G, Clar H, Kapitan M, Berghold A, Windhager R. Survival analysis of 254 patients after manifestation of spinal metastases: evaluation of seven preoperative scoring systems. Spine (Phila Pa 1976). 2011;36:1977-1986.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 118]  [Cited by in F6Publishing: 122]  [Article Influence: 9.4]  [Reference Citation Analysis (0)]
37.  van der Linden YM, Dijkstra SP, Vonk EJ, Marijnen CA, Leer JW. Prediction of survival in patients with metastases in the spinal column: results based on a randomized trial of radiotherapy. Cancer. 2005;103:320-328.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 269]  [Cited by in F6Publishing: 275]  [Article Influence: 14.5]  [Reference Citation Analysis (0)]
38.  Rades D, Dunst J, Schild SE. The first score predicting overall survival in patients with metastatic spinal cord compression. Cancer. 2008;112:157-161.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 103]  [Cited by in F6Publishing: 105]  [Article Influence: 6.6]  [Reference Citation Analysis (0)]
39.  Rades D, Douglas S, Veninga T, Stalpers LJ, Hoskin PJ, Bajrovic A, Adamietz IA, Basic H, Dunst J, Schild SE. Validation and simplification of a score predicting survival in patients irradiated for metastatic spinal cord compression. Cancer. 2010;116:3670-3673.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 57]  [Cited by in F6Publishing: 59]  [Article Influence: 4.2]  [Reference Citation Analysis (0)]
40.  Rades D, Douglas S, Veninga T, Bajrovic A, Stalpers LJ, Hoskin PJ, Rudat V, Schild SE. A survival score for patients with metastatic spinal cord compression from prostate cancer. Strahlenther Onkol. 2012;188:802-806.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 19]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
41.  Rades D, Douglas S, Schild SE. A validated survival score for breast cancer patients with metastatic spinal cord compression. Strahlenther Onkol. 2013;189:41-46.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 17]  [Cited by in F6Publishing: 20]  [Article Influence: 1.7]  [Reference Citation Analysis (0)]
42.  Douglas S, Schild SE, Rades D. Metastatic spinal cord compression in patients with cancer of unknown primary. Estimating the survival prognosis with a validated score. Strahlenther Onkol. 2012;188:1048-1051.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 17]  [Article Influence: 1.4]  [Reference Citation Analysis (0)]
43.  Katagiri H, Takahashi M, Wakai K, Sugiura H, Kataoka T, Nakanishi K. Prognostic factors and a scoring system for patients with skeletal metastasis. J Bone Joint Surg Br. 2005;87:698-703.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 180]  [Cited by in F6Publishing: 186]  [Article Influence: 9.8]  [Reference Citation Analysis (0)]
44.  Kawai T, Aota Y, Yamashita T, Ono M, Mroz TE, Liberman IH, Saito T. Analysis of survival prognostic factors in patients with newly detected metastatic spinal tumors. J Spine Res. 2013;4:136-142.  [PubMed]  [DOI]  [Cited in This Article: ]
45.  Rompe JD, Hopf CG, Eysel P. Outcome after palliative posterior surgery for metastatic disease of the spine--evaluation of 106 consecutive patients after decompression and stabilisation with the Cotrel-Dubousset instrumentation. Arch Orthop Trauma Surg. 1999;119:394-400.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 44]  [Cited by in F6Publishing: 44]  [Article Influence: 1.8]  [Reference Citation Analysis (0)]
46.  Chataigner H, Onimus M. Surgery in spinal metastasis without spinal cord compression: indications and strategy related to the risk of recurrence. Eur Spine J. 2000;9:523-527.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 54]  [Cited by in F6Publishing: 47]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
47.  Ernstberger T, Kögel M, König F, Schultz W. Expandable vertebral body replacement in patients with thoracolumbar spine tumors. Arch Orthop Trauma Surg. 2005;125:660-669.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 28]  [Cited by in F6Publishing: 27]  [Article Influence: 1.4]  [Reference Citation Analysis (0)]
48.  Melcher I, Disch AC, Khodadadyan-Klostermann C, Tohtz S, Smolny M, Stöckle U, Haas NP, Schaser KD. Primary malignant bone tumors and solitary metastases of the thoracolumbar spine: results by management with total en bloc spondylectomy. Eur Spine J. 2007;16:1193-1202.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 80]  [Cited by in F6Publishing: 78]  [Article Influence: 4.6]  [Reference Citation Analysis (0)]
49.  Abel R, Keil M, Schläger E, Akbar M. Posterior decompression and stabilization for metastatic compression of the thoracic spinal cord: is this procedure still state of the art? Spinal Cord. 2008;46:595-602.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 8]  [Cited by in F6Publishing: 8]  [Article Influence: 0.5]  [Reference Citation Analysis (1)]
50.  Biermann JS, Holt GE, Lewis VO, Schwartz HS, Yaszemski MJ. Metastatic bone disease: diagnosis, evaluation, and treatment. Instr Course Lect. 2010;59:593-606.  [PubMed]  [DOI]  [Cited in This Article: ]
51.  Morgen SS, Lund-Andersen C, Larsen CF, Engelholm SA, Dahl B. Prognosis in patients with symptomatic metastatic spinal cord compression: survival in different cancer diagnosis in a cohort of 2321 patients. Spine (Phila Pa 1976). 2013;38:1362-1367.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 63]  [Cited by in F6Publishing: 60]  [Article Influence: 5.5]  [Reference Citation Analysis (1)]
52.  Kim HJ, Buchowski JM, Moussallem CD, Rose PS. Modern techniques in the treatment of patients with metastatic spine disease. Instr Course Lect. 2013;62:375-382.  [PubMed]  [DOI]  [Cited in This Article: ]
53.  Druschel C, Disch AC, Melcher I, Luzzati A, Haas NP, Schaser KD. [Multisegmental en bloc spondylectomy. Indications, staging and surgical technique]. Oper Orthop Traumatol. 2012;24:272-283.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 5]  [Article Influence: 0.4]  [Reference Citation Analysis (0)]
54.  Tancioni F, Navarria P, Lorenzetti MA, Pedrazzoli P, Masci G, Mancosu P, Alloisio M, Morenghi E, Santoro A, Rodriguez y Baena R. Multimodal approach to the management of metastatic epidural spinal cord compression (MESCC) due to solid tumors. Int J Radiat Oncol Biol Phys. 2010;78:1467-1473.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 21]  [Cited by in F6Publishing: 18]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
55.  Tancioni F, Navarria P, Pessina F, Attuati L, Mancosu P, Alloisio M, Scorsetti M, Santoro A, Baena RR. Assessment of prognostic factors in patients with metastatic epidural spinal cord compression (MESCC) from solid tumor after surgery plus radiotherapy: a single institution experience. Eur Spine J. 2012;21 Suppl 1:S146-S148.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 31]  [Cited by in F6Publishing: 29]  [Article Influence: 2.4]  [Reference Citation Analysis (0)]
56.  Rades D, Hueppe M, Schild SE. A score to identify patients with metastatic spinal cord compression who may be candidates for best supportive care. Cancer. 2013;119:897-903.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 46]  [Cited by in F6Publishing: 48]  [Article Influence: 4.0]  [Reference Citation Analysis (0)]
57.  Tang V, Harvey D, Park Dorsay J, Jiang S, Rathbone MP. Prognostic indicators in metastatic spinal cord compression: using functional independence measure and Tokuhashi scale to optimize rehabilitation planning. Spinal Cord. 2007;45:671-677.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 50]  [Cited by in F6Publishing: 52]  [Article Influence: 3.1]  [Reference Citation Analysis (0)]
58.  Yamashita T, Aota Y, Kushida K, Murayama H, Hiruma T, Takeyama M, Iwamura Y, Saito T. Changes in physical function after palliative surgery for metastatic spinal tumor: association of the revised Tokuhashi score with neurologic recovery. Spine (Phila Pa 1976). 2008;33:2341-2346.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 20]  [Cited by in F6Publishing: 18]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
59.  Putz C, Wiedenhöfer B, Gerner HJ, Fürstenberg CH. Tokuhashi prognosis score: an important tool in prediction of the neurological outcome in metastatic spinal cord compression: a retrospective clinical study. Spine (Phila Pa 1976). 2008;33:2669-2674.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 29]  [Cited by in F6Publishing: 29]  [Article Influence: 1.8]  [Reference Citation Analysis (0)]
60.  Rades D, Rudat V, Veninga T, Stalpers LJ, Basic H, Karstens JH, Hoskin PJ, Schild SE. A score predicting posttreatment ambulatory status in patients irradiated for metastatic spinal cord compression. Int J Radiat Oncol Biol Phys. 2008;72:905-908.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 60]  [Cited by in F6Publishing: 38]  [Article Influence: 2.4]  [Reference Citation Analysis (0)]
61.  Rades D, Douglas S, Huttenlocher S, Rudat V, Veninga T, Stalpers LJ, Basic H, Karstens JH, Hoskin PJ, Adamietz IA. Validation of a score predicting post-treatment ambulatory status after radiotherapy for metastatic spinal cord compression. Int J Radiat Oncol Biol Phys. 2011;79:1503-1506.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 33]  [Cited by in F6Publishing: 23]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
62.  North RB, LaRocca VR, Schwartz J, North CA, Zahurak M, Davis RF, McAfee PC. Surgical management of spinal metastases: analysis of prognostic factors during a 10-year experience. J Neurosurg Spine. 2005;2:564-573.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 92]  [Cited by in F6Publishing: 97]  [Article Influence: 5.1]  [Reference Citation Analysis (0)]
63.  Quraishi NA, Manoharan SR, Arealis G, Boszczyk BM. Thirty days mortality rate in the surgical treatment of patients with metastatic spinal cord compression. Spine J. 2013;7:193.  [PubMed]  [DOI]  [Cited in This Article: ]
64.  Gasbarrini A, Cappuccio M, Mirabile L, Bandiera S, Terzi S, Barbanti Bròdano G, Boriani S. Spinal metastases: treatment evaluation algorithm. Eur Rev Med Pharmacol Sci. 2004;8:265-274.  [PubMed]  [DOI]  [Cited in This Article: ]
65.  Gasbarrini A, Li H, Cappuccio M, Mirabile L, Paderni S, Terzi S, Boriani S. Efficacy evaluation of a new treatment algorithm for spinal metastases. Spine. 2010;35:1466-1470.  [PubMed]  [DOI]  [Cited in This Article: ]
66.  Sun YQ, Cai YB, Rong GW. [Comparison of evaluating system for patients with spinal metastases]. Zhonghua Waike Zazhi. 2003;41:570-574.  [PubMed]  [DOI]  [Cited in This Article: ]
67.  Paton GR, Frangou E, Fourney DR. Contemporary treatment strategy for spinal metastasis: the “LMNOP” system. Can J Neurol Sci. 2011;38:396-403.  [PubMed]  [DOI]  [Cited in This Article: ]
68.  Tokuhashi Y, Ajiro Y, Oshima M. Algorithms and planning in metastatic spine tumors. Orthop Clin North Am. 2009;40:37-46, v-vi.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 12]  [Cited by in F6Publishing: 12]  [Article Influence: 0.8]  [Reference Citation Analysis (0)]
69.  Cho W, Chang UK. Neurological and survival outcomes after surgical management of subaxial cervical spine metastases. Spine (Phila Pa 1976). 2012;37:E969-E977.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 36]  [Cited by in F6Publishing: 34]  [Article Influence: 2.8]  [Reference Citation Analysis (0)]
70.  Ogihara S, Seichi A, Hozumi T, Oka H, Ieki R, Nakamura K, Kondoh T. Prognostic factors for patients with spinal metastases from lung cancer. Spine (Phila Pa 1976). 2006;31:1585-1590.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 51]  [Cited by in F6Publishing: 49]  [Article Influence: 2.7]  [Reference Citation Analysis (0)]
71.  Shehadi JA, Sciubba DM, Suk I, Suki D, Maldaun MV, McCutcheon IE, Nader R, Theriault R, Rhines LD, Gokaslan ZL. Surgical treatment strategies and outcome in patients with breast cancer metastatic to the spine: a review of 87 patients. Eur Spine J. 2007;16:1179-1192.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 67]  [Cited by in F6Publishing: 71]  [Article Influence: 4.2]  [Reference Citation Analysis (0)]
72.  Williams BJ, Fox BD, Sciubba DM, Suki D, Tu SM, Kuban D, Gokaslan ZL, Rhines LD, Rao G. Surgical management of prostate cancer metastatic to the spine. J Neurosurg Spine. 2009;10:414-422.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 2]  [Reference Citation Analysis (0)]
73.  Crnalic S, Löfvenberg R, Bergh A, Widmark A, Hildingsson C. Predicting survival for surgery of metastatic spinal cord compression in prostate cancer: a new score. Spine (Phila Pa 1976). 2012;37:2168-2176.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 40]  [Cited by in F6Publishing: 39]  [Article Influence: 3.3]  [Reference Citation Analysis (0)]
74.  Gregory TM, Coriat R, Mir O. Prognostic scoring systems for spinal metastases in the era of anti-VEGF therapies. Spine. 2013;38:965-966.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 22]  [Article Influence: 2.0]  [Reference Citation Analysis (0)]
75.  Chong S, Shin SH, Yoo H, Lee SH, Kim KJ, Jahng TA, Gwak HS. Single-stage posterior decompression and stabilization for metastasis of the thoracic spine: prognostic factors for functional outcome and patients’ survival. Spine J. 2012;12:1083-1092.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 55]  [Cited by in F6Publishing: 61]  [Article Influence: 5.1]  [Reference Citation Analysis (0)]