Prognosis Scores of Tokuhashi and Tomita for Patients With Spinal Metastases of Renal Cancer

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1 Annals of Surgical Oncology (Ó 2006) DOI: /s Prognosis Scores of Tokuhashi and Tomita for Patients With Spinal Metastases of Renal Cancer Benjamin Ulmar, MD, 1 Ulrike Naumann, BSc, 1 Sibel Catalkaya, BSc, 1 Rainer Muche, PhD, 2 Balkan Cakir, MD, 1 Rene Schmidt, MD, 1 Heiko Reichel, MD, Professor, 1 and Klaus Huch, MD 1 1 Department of Orthopedics, University of Ulm, Oberer Eselsberg 45, D-89081, Ulm, Germany 2 Department of Biometry and Medical Documentation, University of Ulm, Schwabstrasse 13, D-89075, Ulm, Germany Background: Retrospective evaluation of the prognosis scores of Tokuhashi and Tomita for life expectancy in 37 consecutive patients with spinal metastases secondary to renal cancer who underwent surgery. The score of Tokuhashi, composed of six parameters, each rated from zero to two, has been proposed in 1990 for the prognostic assessment of patients with spinal metastases. In 2001, Tomita et al. created another prognostic score, composed of three parameters, growth behaviour of the primary tumor (slow, moderate and rapid) and the evidence of visceral and bony metastases. Methods: Thirty-seven patients, surgically treated for vertebral metastases secondary to renal cancer were studied. The scores according to Tokuhashi and Tomita were calculated for each patient. Results: Applying the Tokuhashi Score for the estimation of life expectancy of renal cancer patients with vertebral metastases was found to provide very reliable results with a statistically high significance. The analysis according to Tomita showed no correlation between predicted and real survival. The statistical analysis did not show any significance. Conclusion: For surgical decisions in renal cancer patients with spinal metastases, the prognostic score of Tokuhashi appears to be much more valuable than the Tomita score. Key Words: Prognostic scores Spinal metastasis Renal cancer Life expectancy Outcome analysis.. Since the prognosis of cancer patients has continuously improved by advances in diagnostic work-up and treatment modalities, the incidence of cancer patients with a metastatic disease has also increased. 1 Spinal metastases are a very common manifestation of bone metastasis. 2,3 Seventy-five percent of vertebral metastases originate from the five classic carcinomas: kidney, breast, prostate, lung, and thyroid gland. 4 Ten percent of all spinal metastases are produced by renal cell carcinoma. Approximately 2% of Received September 19, 2005; accepted January 20, 2006 Address correspondence and reprint requests to: Benjamin Ulmar, MD; benjamin.ulmar@uni-ulm.de Published by Springer Science+Business Media, Inc. Ó 2006 The Society of Surgical Oncology, Inc. the worldwide cancer mortality can be attributed to renal cell carcinomas. 5 Because of the bad response of this carcinoma to radiotherapy or chemotherapy, the prognosis of renal cell carcinomas with metastases is poor; survivals of 12 to 22 months are reported. 6,7 Surgical treatment in case of advanced malignant disease with metastases has to strive for the maximum palliative effect, including the reduction of pain and the maintenance or restoration of function and stability of the spine, with a minimum of operative morbidity and mortality. The individual therapy is not easy to choose, and the decision should be strongly influenced by the predicted survival. Therefore, different prognostic scores for patients with spinal metastases of different origin have been created.

2 B. ULMAR ET AL. TABLE 1. Original evaluation score for the prognosis of metastatic spine tumors by Tokuhashi et al. 8 and patient data of our study Variable Score No. Patients (%) General condition (performance status) a Poor (10% 40%) 0 14 (37.8%) Moderate (50% 70%) 1 10 (27.0%) Good (80% 100%) 2 13 (35.1%) No. extrapinal bone metastasis foci (35.1%) (10.8%) (54.1%) No. of metastases in the vertebral bodies (40.5%) (18.9%) (40.5%) Metastases to the major internal organs Unremovable 0 23 (62.2%) Removable 1 4 (10.8%) No metastases 2 10 (27.0%) Primary site of the cancer (according to Tokuhashi et al. 8 ) Lung, stomach 0 Kidney, liver, uterus, unidentified, other 1 37 (100%) Thyroid, prostate, breast, rectum 2 Spinal cord palsy Complete 0 2 (5.4%) Incomplete 1 21 (56.8%) None 2 14 (37.8%) a Performance status according to Karnofsky 23. The most popular system is the score of Tokuhashi, 8 developed in The system of Tokuhashi consists of the sum of six parameters that are used to measure the severity of the disorder: the general condition of the patient, the number of extraspinal bone metastases, the number of vertebral metastases, the number of metastases to the major internal organs, the primary site of the cancer, and spinal cord palsy. Each parameter is rated from 0 to 2. Zero signifies the worst prognosis (Table 1). Tokuhashi et al. 8 proposed a survival of 3 months or less for patients with a total score of 5 or less, a survival of 12 months or less in case of 8 points or less, and a survival of 12 months or more in patients with a total score of 9 points or more. Therefore, Tokuhashi et al. 8 recommend excisional surgery of metastases when the total score reached 9 or more and palliative treatment when the score was 5 or less. Recently, Tokuhashi modified this score by a more differentiated grouping of the primary tumor site from 0 to 5. This changes the Tokuhashi score from a 12-point to a 15-point scoring system. 9 The modified score has not been evaluated in patients yet. In 2001, Tomita et al. 10 also presented a prognostic score, which consists of 3 factors, developed on the TABLE 2. Scoring system for survival prognosis in spinal metastases developed by Tomita et al. 10 Prognostic factors Score No. patients (%) Primary tumor Slow growth (breast, thyroid, etc.) 1 Moderate growth (kidney, uterus, etc.) 2 37 (100%) Rapid growth (lung, stomach, etc.) 4 Visceral metastases None 0 10 (27.0%) Treatable 2 4 (10.8%) Untreatable 4 23 (62.2%) Bone metastases* Solitary or isolated 1 4 (10.8%) Multiple 2 33 (89.2%) *Bone metastases including spinal metastases. retrospective data of 67 surgical patients with spinal metastases of different origins: (1) grade of malignancy (slow growth, 1 point; moderate growth, 2 points; and rapid growth, 4 points), (2) visceral metastases (no metastases, 0 points; treatable metastases, 2 points; and untreatable metastases, 4 points), and (3) bone metastases (solitary or isolated, 1 point; multiple, 2 points). These three factors were added to give a prognostic score between 2 and 10. The treatment goal for each patient was set according to this score (Table 2). A score of 2 or 3 points suggested a wide or marginal excision for long-term local control, 4 or 5 points indicated marginal or intralesional excision for mid-term local control, 6 or 7 points justified palliative surgery for short-term palliation, and 8 to 10 points indicated nonoperative supportive care. The score was also tested prospectively by the authors in 61 patients with spinal metastases, and successful prediction of survival in the different prognostic groups depending on the modified surgical treatment has been reported. 10 Patients with spinal metastases and an intermediate or good prognosis seem to benefit from a more radical (excisional) removal of metastatic spine lesions Although all surgical procedures remain palliative by definition, evaluation of the prognosis is necessary to make the decision for surgical procedures (dorsoventral approach vs. isolated posterior instrumentation). Stabilization and restoration of the anterior spinal column after surgical removal of the diseased vertebra are as in acute traumatic spinal lesions with a collapse of the vertebra also recommended in patients with spinal instabilities due to metastases with a good long-term prognosis. Therefore, calculation of the survival is useful not only to improve the prognosis with a more radical surgical procedure, but also to prevent mechanical com-

3 PROGNOSIS SCORES IN SPINAL METASTASES Patient No. Sex Age (y) Karnofsky Index (%) TABLE 3. Clinical data of all study patients (n = 37) Spinal cord palsy Spinal metastases (vertebraõs) Level of Instrumentation Bone metastases Visceral metastases 1 M ic 2 L M ut 2 M no 1 L M t 3 M ic 3 T M ut 4 M ic 1 L M ut 5 M ic 2 C M n 6 M ic 1 L M t 7 F ic 1 T S n 8 M no 1 L M ut 9 M no 2 L M ut 10 F ic 2 TL M ut 11 M no 1 T M n 12 M ic 2 T M n 13 F ic 2 TL M t 14 M no 3 TL M n 15 M no 1 L M ut 16 M no 2 T S n 17 M no 1 T M n 18 M ic 3 T M ut 19 M ic 1 L S n 20 M ic 1 T M n 21 M ic 3 TL M ut 22 M ic 3 C M ut 23 M no 3 T M ut 24 M no 1 L S n 25 M no 1 L M ut 26 M no 1 T M ut 27 F ic 1 L M ut 28 M c 3 T M ut 29 M no 3 T M t 30 M ic 3 T M ut 31 M no 1 L M ut 32 M no 3 L M ut 33 M c 3 T M ut 34 M ic 3 L M ut 35 F ic 3 T M ut 36 F no 3 T M ut 37 M no 3 L M ut No, none; n, no; ic, incomplete; c, complete; m, multiple; s, solitary; t, treatable, ut, untreatable; C, cervical; T, thoracic; TL, thoracolumbar; L, lumbar. plications of an isolated dorsal instrumentation in the case of predicted long-term survival. 4,14 18 In these patients, the reconstruction of the vertebral body after vertebral removal should provide sufficient long-term stability. In times of decreasing finances, the indication for surgery especially when costly implants are used in tumor patients with a significantly reduced life expectancy should be based on proven algorithms and scores. This study was performed to evaluate the validity of the prognostic scores of Tokuhashi et al. 8 and Tomita et al. 10 and to compare the survival predicted in both scores with the definitive survival of patients with spinal metastases due to renal cell carcinoma, because the origin of the primary tumor has a substantial influence on survival Including only patients with the same type of cancer reduces the number of variable parameters in the Tokuhashi score from 6 to 5 and in the Tomita score from 3 to 2. PATIENTS AND METHODS In this retrospective study, 37 patients with spinal metastases secondary to renal cancer underwent surgery for spine fusion, reduction of pain, and/or neurological deficits between September 1984 and March 2005 (Table 3). Renal cell carcinoma could be verified in all patients by histological analysis. Before surgery, patients were examined with plain anterior-posterior and lateral radiographs of the affected spinal segment, computed tomography with sagittal reconstructions of the involved vertebra, and, in the last 15 years, magnetic resonance imaging focused on the affected spinal segment to establish the

4 B. ULMAR ET AL. extent of the osseous and spinal canal involvement. A systemic search for other metastases was performed in cooperation with urologists. This included clinical evaluation, abdominal and renal sonography, plain radiographs of the thorax to detect pulmonary metastases, and bone scans to detect other osseous metastases, especially in the spine. Computed tomographic scans of the chest, abdomen, and brain were performed in each patient with suggestive clinical findings. In addition, the preoperative Tokuhashi score 8 (Table 1) and the Tomita score 10 (Table 2) were calculated for all patients. The survival dates were censored at March 10, All findings were entered into an Excel database (Microsoft Corp., Redmond, WA) to ensure that all vertebral, bone, and visceral metastases would be listed and analyzed in the same way and to enable comparisons to be made wherever possible. The statistical unit of analysis was the patient, and statistical analysis was performed on the 37 patients available for the follow-up study. To test the prognostic value of the Tokuhashi score 8 and the Tomita score, 10 the total number of points was calculated for all patients, and the patients were divided into prognostic groups according to both scores. Both scores have been proven for retrospective use. 10,19 Statistical analysis was performed by using the log-rank test for univariate analysis. Survival curves were created by using the Kaplan-Meier life-table analysis. A P value < 0.05 (two tailed) was considered significant. RESULTS The parameters of the study patients are listed in Table 3. The mean survival of all study patients was 13.7 ± 18.9 months (range, months; median, 6.2 months). The results showed a 1-year survival rate of 13 patients (48.6%), a 2-year survival rate of 4 patients (10.8%), and a 5-year survival rate of 2 patients (5.4%). At the end of the study (March 10, 2005), 36 patients (97.3%) had died. The single patient (2.7%) who was still alive at the end of observation survived 21.7 months. For all patients, the Tokuhashi score 8 and the Tomita score 10 were calculated (Tables 1 and 2). Tokuhashi Score For the palliative group (n = 11; 29.7%), the survival was predicted according to Tokuhashi et al. 8 to be less than 3 months. The mean real survival of the group was 4.7 ± 5.8 months (range, FIG. 1. Predictive survival according to the Tokuhashi score 8 :, patients with a score of 5 or less;, patients with a score of 6 to 8; _, patients with a score of 9 or higher. months; median, 2.6 months), and in our evaluation, only six patients (54.5%) of this group survived less than 3 months. The indifferent group (patients without a palliative or excisional treatment recommendation) (n = 18; 48.6%) had a predictive survival of 12 months or less. The mean real survival was 9.5 ± 10.0 months (range, months; median, 6.2 months) in 14 patients (77.8%) of this group, and our evaluation showed a survival as predicted. The excisional group (n = 8; 21.6%) had a predicted survival of 12 months or more. In our study group, all these patients (100%) survived as predicted, and this subgroup reached a real mean survival of 35.3 ± 28.2 months (range, months; median, 20.6 months). The prognostication of survival by using the original evaluation of Tokuhashi et al. 8 was highly significant (P < ; Fig. 1). Tomita Score According to Tomita et al., 10 four patients (10.8%) reached 2 or 3 points, and their treatment goal should be long-term tumor control. For this subgroup the predicted survival was the best of all prognostic groups. However, the real mean survival was 8.7 ± 7.6 months (range, months; median, 6.4 months). Five patients (13.5%) reached 4 or 5 points with a treatment goal of mid-term tumor control. In our evaluation, the real mean survival of these patients was 23.3 ± 30.9 months (range, months; median, 17.2 months) and therefore the best survival of all prognostic groups. Five patients (13.5%) got 6 or 7 points, with a treatment goal of short-term palliation. However, the real mean survival of this group was 21.6 ± 34.6 months (range, months; median, 7.7 months). At least 23

5 PROGNOSIS SCORES IN SPINAL METASTASES FIG. 2. Predictive survival according to the Tomita score 10 :, patients with a score of 2 or 3;., patients with a score of 4 or 5; _, patients with a score of 6 or 7;, patients with a score of 8 to 10. patients (62.2%) got 8 to 10 points, resulting in the worst predicted prognosis and the suggestion of terminal care according to Tomita et al. 10 In our evaluation, the mean survival of this group was still 10.6 ± 11.1 months (range, months; median, 5.7 months). The real survival of this group was similar to that of the prognostic group, with 2 or 3 points (8.7 ± 7.6 months; range, months; median, 6.4 months). Overall, the Tomita score 10 did not show any significance for the prognosticated and real survival (P = ; Fig. 2). Significance of Single Factors of Both Scores When the single factors of both scores were analyzed, only the parameter general condition was significant for the prognosticated survival. Accordingly, neither scoring system for bone metastasis was significant to predict survival (Fig. 3). DISCUSSION This study was performed to evaluate the value of two different prognostic scores in patients with spinal metastasis due to renal cell carcinoma. The survival prognosis is important for the surgical strategy. The significant predictive value of the Tokuhashi score for survival time was reported by Riegel et al. 20 in 2002 and by Ulmar et al. 21 in To evaluate the predictive value of the Tokuhashi score 8 and of another clinical prognostic score (Tomita score 10 ) in spinal metastases of renal cell carcinomas, the actual study was performed. Survival is influenced by various isolated patientand tumor-based parameters. The prognostic scoring system of Tokuhashi et al. 8 includes six variables for the preoperative evaluation of patients with spinal metastases. In our study, the general medical condition of the patient was the only isolated parameter that significantly predicted the time of survival. This is in agreement with Chataigner and Onimus, 22 who proved that the Karnofsky Index is effective in nonneurological cases. If the Karnofsky Index 23 of patients with spinal metastases is more than 70%, the survival period will be relatively high. 24 If the general state is clearly reduced (Karnofsky index <40%), palliative treatments other than surgery should be considered for patients without neurological deficits. 22 The bone and visceral spread and the extent and number of bone metastases have been accepted as predictive factors for the patientõs survival. 4,8,19,25 28 Du rr et al. 25,26 accordingly reported a significantly better survival rate for renal cancer and breast cancer patients with solitary bone metastases, in contrast to patients with multiple bone metastases or additional visceral spread. However, our data did not show any significance for the isolated evaluation of metastatic spread (Fig. 3). Variable survival rates have been reported by several authors, depending on the primary site of the tumor. 22,29 35 Tatsui et al. 33 evaluated the 1-year survival of 425 patients with spinal metastases of different origins after detection by bone scan. They reported a 1-year survival rate of 83.3% for patients with prostatic cancer, of 77.7% for patients with breast cancer, of 51.2% for patients with renal cancer (our patients showed a 1-year survival rate of 46.6%), of 44.6% for patients with uterine cancer, of 21.7% for patients with lung cancer, and of 0% for those with gastric cancer. Therefore, Tokuhashi et al. 8 and Tomita et al. 10 included the site of tumor as one major prognostic factor influencing survival. Paraplegia is another controversially discussed prognostic factor in patients with spinal metastases. The rapidity of the onset of muscular weakness has been reported as having a considerable bearing on the ultimate prognosis. 36 Spiegel et al. 37 and Enkaoua et al. 19 reported that neurological deficits are not significantly associated with the length of survival in melanoma patients or in patients with thyroid cancer, renal cancer, and metastasis of unknown origin. Patients with paraplegia seem to die sooner because of progression of their cancer, but not as a result of the paraplegia itself. Tomita et al. 10 did not accept the neurological state as a prognostic factor for their system of survival prognostication in spinal metas-

6 B. ULMAR ET AL. Spinal cord palsy (p=0.5850) Primary side of cancer Visceral metastases (p=0.5644) Vertebral metastases (p=0.2134) Extraspinal metastases (p=0.4625) General condition (p<0.0001) Primary tumor Visceral metastases s (p=0.5644) Bone metastases (p=0.5830) Number of patients FIG. 3. a Evaluation of the isolated parameter according to Tokuhashi et al. 8 for the study patients, including the isolated significance of each parameter., patients with a score of 0;, patients with a score of 1 scoring points;, patients with a score of 2. b Evaluation of the isolated parameter according to Tomita et al. 10 for the study patients, including the isolated significance of each parameter., patients with a score of 0;, patients with a score of 1;, patients with a score of 2,, patients with a score of 4. tases. Accordingly, our study did not show any significant predictive value of spinal cord palsy in patients with renal cancer (Tables 2 and 3). Enkaoua et al. 19 studied 28 patients with vertebral metastases from renal cancer. Twenty-seven of these patients died, and one patient was alive at the time of the last follow-up examination. Those patients, who died had had a mean length of survival of 13 months (range, 1 45 months) and a median survival of 9 months. The mean survival rate was very close to that found in our study (mean survival, 13.7, months; range: months). The median survival of our study patients was shorter (6 months) (Table 4). TABLE 4. Comparison of our study results and survival data with the results of Enkaoua et al. 19 Variable Actual data Enkaoua et al. 19 No. dead/total 36/37 27/28 age ± SD 61.4 ± 10.3 years 57.6 ± 11.7 years Sex (M/F) 31/6 20/8 Tokuhashi score 6.1 ± 2.3 points 8.1 ± 2.4 points points ± SD Neurological deficits 23/37 9/28 Mean survival (mo) Median survival ± SD 6 9 (ms) Range (mo) CONCLUSION In our study, patients with spinal metastasis secondary to renal cell carcinoma survived as estimated by the Tokuhashi score. 8 For the palliative group, the mean survival was 4.7 ± 5.8 months and was, therefore, slightly longer than predicted by Tokuhashi (<3 months). For the indifferent group, the mean survival was 9.5 ± 10.0 months and was, therefore, as predicted by the Tokuhashi score ( 12 months). The excisional group had a mean survival of 35.3 ± 28.2 months, as predicted by the Tokuhashi score ( 12 months). The precision of survival prediction increased with the prognosis. Accordingly, the predicted survival was reached by all patients of the best-prognosis group. The Tomita score 10 showed no significance for the prognosticated and real survival (P = ). The mean survival of the best-prognosticated group (longterm control group), for example, was the worst of the entire study group (8.7 ± 7.6 months). We therefore recommend the Tokuhashi score 8 to estimate the prognosis in renal cancer with spinal metastases.

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