A prediction model of survival for patients with bone metastasis from uterine corpus cancer

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1 JJCO Japanese Journal of Clinical Oncology Japanese Journal of Clinical Oncology, 2016, 46(11) doi: /jjco/hyw120 Advance Access Publication Date: 21 September 2016 Original Article Original Article A prediction model of survival for patients with bone metastasis from uterine corpus cancer Sho Takeshita 1, *, Yukiharu Todo 1, Hiroko Matsumiya 1, Kazuhira Okamoto 1, Katsushige Yamashiro 2, and Hidenori Kato 1 1 Division of Gynecologic Oncology, National Hospital Organization, Hokkaido Cancer Center, Shiroishi-ku, Sapporo, and 2 Division of Pathology, National Hospital Organization, Hokkaido Cancer Center, Shiroishi-ku, Sapporo, Japan *For reprints and all correspondence: Sho Takeshita, Division of Gynecologic Oncology, National Hospital Organization, Hokkaido Cancer Center, 4-2 Kikusui, Shiroishi-Ku, Sapporo , Japan. stakeshita@sap-cc.go.jp Received 28 April 2016; Accepted 8 August 2016 Abstract Objective: The aim of the study was to establish a predictive model of survival period after bone metastasis from endometrial cancer. Methods: A total of 28 patients with bone metastasis from uterine corpus cancer were included in the study. Data at the time of bone metastasis diagnosis, which included presence of extraskeletal metastasis, performance status, history of any previous radiation/chemotherapy and the number of bone metastases, were collected. Survival data were analyzed using Kaplan Meier methods and Cox proportional hazard models. Results: The most common site of bone metastasis was the pelvis (50.0%), followed by lumbar spine (32.1%), thoracic spine (25.0%) and rib bone (17.9%). The median survival period after bone metastasis was 25 weeks. The overall rate of survival after bone metastasis of the entire cohort was 75.0% at 13 weeks, 46.4% at 26 weeks and 42.9% at 52 weeks. Performance status of 3 4 was confirmed as an independent prognostic factor (Hazard ratio, 3.5; 95% confidence interval, ) and multiple bone metastases tended to be associated with poor prognosis (Hazard ratio, 2.4; 95% confidence interval, ). A prognostic score was calculated by adding up the number of these two factors. The 26-week survival rates after bone metastasis were 88.9% for those with a score of 0, 45.5% for those with a score of 1 and 0% for those with a score of 2 (P = ). Conclusions: This scoring system can be used to determine the optimal treatment for patients with bone metastasis from endometrial cancer. Key words: endometrial cancer, bone metastasis, prognosis, performance status Introduction Endometrial cancer is one of the most common malignancies of the female genital tract, and its incidence is increasing in industrialized nations. In the USA, the annual number of new cases increased from in 1995 (1) to in 2015 (2), and the annual number of deaths has been almost doubled from 5900 in 1995 to in Bone metastases are a frequent complication of cancer, occurring in up to 70% of patients with advanced breast or prostate cancer (3). In contrast, bone metastasis from endometrial cancer is generally uncommon and thus, there has been limited information on prognosis or prognostic factors (4 8). Median survival times for endometrial cancer patients after diagnosis of a bone metastasis have been reported to be months (4 8). For patients with bone metastasis, prediction of their remaining weeks or months might be important with regard to treatment decisions and quality of life. Katagiri et al. conducted two prospective studies based on data of their cohort of >1000 cases comprising various primary tumors The Author Published by Oxford University Press. All rights reserved. For Permissions, please journals.permissions@oup.com 973

2 974 Bone metastasis from uterine corpus cancer and proposed a scoring system to estimate the prognosis of patients with bone metastasis (9,10). They identified six significant prognostic factors: site of the primary lesion; presence of visceral or cerebral metastases; performance status (Eastern Cooperative Oncology Group status 3 or 4); any previous chemotherapy; multiple bone metastases; and abnormal laboratory data. Patients were divided into three different groups by their scoring system, which can predict distinct prognosis for each group. However, it is unclear whether these results are applicable because there were only 10 cases (1.2%) of gynecological malignancies except for cervical cancer in their study population. In their scoring system, endometrial cancer was classified in the moderate growth group, which included hormoneindependent breast cancer, hormone-independent prostate cancer, renal cell carcinoma and non-small cell lung cancer with molecularly targeted therapy. We evaluated biological aggressiveness of bone metastasis peculiar to endometrial cancer and verified each prognostic factor selected in the Katagiri et al. study. A prognostic scoring system particular to bone metastasis from endometrial cancer was proposed in this study. Patients and methods Patients (endometrial cancer group) In total, 926 patients were treated for uterine corpus malignancies at the National Hospital Organization, Hokkaido Cancer Center from January 1995 to December Twenty-eight (3.0%) patients with skeletal metastasis from endometrial cancer were included in the study. The medical records were reviewed, and data at the time of initial presentation, which included age, International Federation of Gynecology and Obstetrics (FIGO) stage, histological subtype and treatment, were collected. Data at the time of initial progression, namely the progression-free interval, were also investigated. In addition, data at the time of bone metastasis diagnosis, which included spread pattern, presence of extraskeletal metastasis, performance status (evaluated according to the Eastern Cooperative Oncology Group (ECOG) performance status group (11)), history of any previous radiation or chemotherapy, number of bone metastases, onset period and treatment, were collected. Finally, data regarding clinical outcome were obtained. The local institutional review board and the hospital s ethics committee approved the study protocol. Patients (cervical cancer group) To compare biological aggressiveness of bone metastasis from endometrial cancer with that from cervical cancer, patients with skeletal metastasis from cervical cancer were also included in the study. Fifty-four (5.8%) were identified among a total of 925 patients treated for cervical cancer at our institution from January 1995 to December The medical records were reviewed, and the abovementioned data were collected. Diagnosis of bone/extraskeletal metastases The presence of bone/extraskeletal metastases was determined by biopsy or imaging including bone scans, fluorodeoxyglucosepositron emission tomography, computed tomography and magnetic resonance imaging. Radiologically abnormal lesions without pathological confirmation found in patients diagnosed with other types of invasive cancer within the previous 5 years were not considered as metastatic tumors. The metastatic status of bone lesions that appeared to be in a gray zone was determined by specialists in orthopedic oncology. Survival analysis The primary outcome measure was the survival period after diagnosis of bone metastasis. Six variables were used for survival analysis and every variable had a binary classification. (i) Histological variant (endometrioid adenocarcinoma grade 1/grade 2 vs. endometrioid adenocarcinoma grade 3/non-endometrioid carcinoma); (ii) extraskeletal metastasis (no vs. yes); (iii) performance status (0 2 vs. 3 4); (iv) history of any previous radiation or chemotherapy (no vs. yes); (v) multiple bone metastases (no vs. yes); and (vi) bone metastasis-free interval (<12 months vs. 12 months). When comparing biological aggressiveness of bone metastasis from endometrial cancer with that from cervical cancer, site of the primary tumor (cervical cancer vs. endometrial cancer) was used for the analysis instead of histological variant. Progression-free interval was defined as the time from initial presentation to initial progression or death from any cause, which did not depend on the presence or absence of bone metastasis. The bone metastasis-free interval was defined as the time from initial presentation to diagnosis of bone metastasis from endometrial cancer. Survival rates were estimated using the Kaplan Meier method and compared between groups using the log-rank test. Hazard ratios (HRs) and 95% confidence intervals (CIs) were estimated using the Cox proportional hazards model. A P value of <0.05 was considered as statistically significant. All analyses were performed using R version 3.2.0: A Language and Environment for Statistical Computing (R Core Team 2015). Results Clinicopathological characteristics of the 28 patients are shown in Table 1. A total of three patients (10.7%) had FIGO (2008) stage I disease, 2 (7.1%) had stage II disease, 9 (32.1%) had stage III Table 1. Profile of the patients at the time of initial treatment (n = 28) Profile No. of patients (%) Age: median (range) 60.5 (range: 26 81) FIGO stage I 3 (10.7%) II 2 (7.1%) III 9 (32.2%) IV 14 (50.0%) Histological cell types Endometrioid grade 1 3 (10.7%) Endometrioid grade 2 6 (21.4%) Endometrioid grade 3 7 (25.0%) Non-endometrioid carcinoma 8 (28.6%) Carcinosarcoma 4 (14.3%) Initial treatment to the primary endometrial tumor Surgery alone 2 (7.1%) Surgery followed by CT 17 (60.7%) Surgery followed by HT 1 (3.6%) CT alone 4 (14.3%) CT followed by RT 1 (3.6%) CT followed by surgery 1 (3.6%) RT alone 1 (3.6%) RT followed by surgery plus CT 1 (3.6%) RT, radiotherapy; CT, chemotherapy; HT, hormonal therapy.

3 Jpn J Clin Oncol, 2016, Vol. 46, No disease and 14 (50.0%) had stage IV disease. Sixteen (57.1%) patients had endometrioid adenocarcinoma. Treatment of the primary endometrial tumor involved surgery followed by chemotherapy, which were performed on 60.7% of patients, chemotherapy alone, which were performed on 14.3% of patients, and surgery alone, which were performed on 7.1% of patients. Clinical characteristics of the bone metastases are shown in Table 2. Twenty-four patients (85.7%) had extraskeletal metastasis at the time of diagnosis of bone metastasis. Twelve patients (42.9%) had a performance status >3. Twenty patients (71.4%) had a history of any previous radiation or chemotherapy. Fifteen patients (53.6%) had multiple bone metastases. Six cases (21.4%) of bone metastases occurred at the time of initial presentation, 10 (35.7%) occurred at the time of initial progression, and 12 (42.9%) occurred at the subsequent progression. As for treatment of the metastatic bone tumor, radiotherapy alone was done in 16 (57.1%) of cases. Best supportive care was performed in 1 (3.6%) of patients. Spinal fixation was performed in 2 (7.1%) of the patients. As shown in Fig. 1, bone metastasis to the pelvis and the vertebral column was usual. The most common site of bone metastasis was the pelvis (50.0%), followed by lumbar spine (32.1%), thoracic spine (25.0%), rib bone (17.9%) and femur (14.3%). The Kaplan Meier curve for the entire cohort is shown in Fig. 2. The median survival period after diagnosis of bone metastasis was 25 weeks (range: weeks). The overall rate of survival after diagnosis of bone metastasis of the entire cohort was 75.0% at 13 weeks, 46.4% at 26 weeks and 42.9% at 52 weeks. Table 3 shows the results of Cox regression analysis of prognostic factors in endometrial cancer patients with bone metastasis. Multivariate analysis showed that performance status of 3 4 was confirmed as independent prognostic factors (HR, 3.5; 95% CI, ), and multiple bone metastases tended to be associated with poor prognosis (HR, 2.4; 95% CI, ). A prognostic score was calculated by adding up the number of these two factors and therefore, every case was scored from 0 to 2. The rates of survival for these three subgroups were significantly different (log-rank test, P = ) (Fig. 2). The 3-month survival rates after diagnosis of bone metastasis were 100% for those with a score of 0, 72.7% for those with a score of 1 and 50.0% for those with a score of 2. The 6-month survival rates were 88.9% for those with a score of 0, 45.5% for those with a score of 1 and 0% for those with a score of 2. The 1-year survival rates were 88.9% for those with a score of 0 and 36.4% for those with a score of 1. The 2-year survival rates were 50.8% for those with a score of 0 and 27.3% for those with a score of 1. Table 4 shows the results of Cox regression analysis of prognostic factors in cervical or endometrial cancer patients with bone metastasis. Endometrial cancer was significantly associated with better survival after bone metastasis with a HR of 0.39 (95% CI = , P = 0.001) compared with cervical cancer after adjusting extraskeletal metastasis, performance status, history of any previous radiation or chemotherapy and multiple bone metastases.clinicopathological characteristics of the 54 patients in the cervical cancer group are shown in Supplementary Table S1, available in Age and Ageing online. Clinical characteristics of the bone metastases are shown in Supplementary Table S2, available in Age and Ageing online. The overall rate of survival after diagnosis of bone metastasis in the cervical cancer group was 64.2% at 13 weeks, 37.2% at 26 weeks and 15.4% at 52 weeks (Fig. 3). Endometrial cancer showed a 27.5% increase (42.9% vs. 15.4%) in the 1-year overall survival compared with cervical cancer. Table 2. Clinical characteristics of bone metastasis (n = 28) Clinical characteristics Discussion No. of patients Age at the time of bone metastasis: 60.5 years old (range: 28 84) median Extraskeletal metastasis 24 (85.7%) Performance status (ECOG) 3 or 4 12 (42.9%) Previous radiation/chemotherapy 20 (71.4%) Multiple bone metastases 15 (53.6%) Onset of bone metastasis Initial presentation 6 (21.4%) Initial progression 10 (35.7%) Second/Subsequent progression 12 (42.9%) Progression-free interval: median 6 months (range: 1 24) Bone metastasis-free interval: median 10 months (rage: 0 40) Treatment to the metastatic bone tumor CT alone 3 (10.7%) RT alone 16 (57.1%) RT plus HT 1 (3.6%) RT plus CT 4 (14.3%) RT plus surgery (spinal fixation) 2 (7.1%) Supportive care 1 (3.6%) Surgery followed by RT 1 (3.6%) ECOG, Eastern Cooperative Oncology Group. Figure 1. Distribution of sites of bone metastasis. This study showed a median survival time of 6 months after a diagnosis of bone metastasis from endometrial cancer, which was the worst among results of some earlier cohort studies (4 6), and those

4 976 Bone metastasis from uterine corpus cancer Figure 2. Kaplan Meier survival curves after diagnosis of bone metastasis in all 28 uterine corpus cancer patients included in this study (A) and in patients with prognostic scores of 0, 1 and 2 (B). The rates of survival for these three groups were significantly different (P = ). Table 3. Prognostic factors for patients with bone metastasis from primary endometrial cancer selected using Cox proportional hazards model analysis No. of patients Univariate analysis Multivariate analysis HR 95% CI P value HR 95% CI P value Histology G1/G G3/Others Extraskeletal metastasis No Yes Performance status Previous radiaion/chemotherapy No Yes Multiple bone metastases No Yes Bone metastasis-free interval >12 months <12 months HR, hazard ratio; CI, confidence interval; G1, endometrioid adenocarcinoma grade 1; G2, endometrioid adenocarcinoma grade 2; G3, endometrioid adenocarcinoma grade 3. of some literature reviews (7,8). Earlier cohort studies reported that median survival times after bone metastasis were months (4 6). Previous literature reviews reported median survival times after bone metastasis of months (7,8). Differences among results of known reports including our study might be explained by various types of selection bias. First, earlier cohort studies might have been involved in referral filter bias, which is also called healthcare access bias. While these cohort studies showed incidence rates of bone metastasis from endometrial cancer were % (4 6), the incidence rate was 3.1% in the present study. While the rates of patients without coexisting extraskeletal metastasis were % in earlier studies (4 6), it was only 14.3% in the present study. Our institution is a tertiary cancer center with a division of orthopedic oncology, radiation oncology and palliative care. Many patients with metastatic bone tumor are referred to our institution in a state that primary tumor is unknown. Many patients already treated with standard therapy are referred to our institution for the purpose of palliative treatment including radiation therapy in the latter half of their clinical course. Second, previous literature reviews might have been involved in publication biases. In general, studies with positive outcomes are more likely to be published than studies with negative outcomes (12). Just like this, case reports with successful outcome would be more likely to be published than those with unsuccessful outcome. Third, a previous review report might have been involved in length time bias in addition to publication bias. Myriokefalitaki et al. conducted a literature review of 29 cases of stage IV endometrial cancer with bone metastasis at the time of initial

5 Jpn J Clin Oncol, 2016, Vol. 46, No Table 4. Prognostic factors for patients with bone metastasis from primary cervical/endometrial cancer selected using Cox proportional hazards model analysis No. of patients Univariate analysis Multivariate analysis HR 95% CI P value HR 95% CI P value Extraskeletal metastasis No Yes Performance status < < Previous radiaion/chemotherapy No Yes Multiple bone metastases No Yes Bone metastasis-free interval >12 months <12 months Primary tumor Cervical cancer Endometrial cancer Figure 3. Kaplan Meier survival curves after diagnosis of bone metastasis in all 54 cervical cancer patients. presentation and reported a median survival time of 25.5 months, being extremely longer compared with the result of the previous studies (8). It is well known that the prognoses of asymptomatic patients who are diagnosed by cancer screening are better than those of patients who present with clinical manifestations of the tumor. Cases of diseases with long duration of progression are more easily included in surveys and may not represent cases originated in the target population (13). These cases usually have a better prognosis. Just like this, biological aggressiveness of patients with onset of bone metastasis at the time of initial presentation might be less aggressive than those with onset at the time of progression. When considering prognosis for such patients, prediction of their remaining lifespan would allow them to better plan how to live out their final days. There are some options including surgery for the treatment of bone metastasis. Life expectancy of at least 2 months is usually required before surgery is considered for metastases to the limbs (14), and of 3 6 months for metastases to the spine (15,16). According to our results, patients with a prognostic score of 0 were very good candidates for spinal surgery. This group accounted for 34.5% of the entire cohort. Despite being unexpectedly short survival time after bone metastasis, our study showed that endometrial cancer was significantly associated with better prognosis after bone metastasis compared with cervical cancer. This result concurred with Katagiri et al. classification regarding biological aggressiveness of bone metastasis from endometrial cancer. In their system, while cervical cancer was classified in the rapid growth group, endometrial cancer was classified in the moderate growth group (10). Indeed in our study, while only two patients (3.7%) survived >2 years in the cervical cancer group, seven patients (25.0%) did in the endometrial cancer group. While no one survived >4 years in the cervical cancer group, four patients (14.3%) did in the endometrial cancer group. Among prognostic factors selected in the Katagiri et al. studies, presence of extraskeletal metastases and a history of previous chemotherapy were not confirmed as prognostic factors in the present study. This result might be explained by the following two reasons. First, the number of patients included in the study might have been too small to confirm these variables as prognostic factors. Second, these two variables might be prognostic factors for a rapid growth group but not be ones for slow/moderate growth groups. Third, the different treatments undertaken for the bone metastases at the time of diagnosis might have influenced the significance of these variables on prognosis. It is highly possible that these variables and treatment at the time of diagnosis for bone metastasis are confounding factors each other. Indeed, some endometrial cancers are hormonally dependent and their prognosis would be influenced by treatment-related factors. Our study has some limitations. First, the number of patients included in the study was too small to power statistically conclusive results. Second, there was no consistent follow-up policy for diagnosing metastatic bone tumors and no consistent treatment policy for metastatic bone tumors in our institution. These issues

6 978 Bone metastasis from uterine corpus cancer are caused by the fact that ours was a retrospective, observational study conducted at a single institution. However, our study had other strong points; insufficiency fractures or compression fractures were appropriately excluded from our study by the orthopedic oncologists. Additionally, many of our patients were treated at or referred to our institution for the purpose of palliative treatment in the latter half of their clinical course. Consequently, greater than half of the deceased patients passed away at our institution not at hospices. These additional factors lend support to the validity of our study. In conclusion, performance status and multiple bone metastases might be independent prognostic factors for patients with bone metastasis from endometrial cancer. Our scoring system based on these two factors can be used to determine the optimal treatment for patients with bone metastasis from endometrial cancer. Supplementary data Supplementary data are available at Conflict of interest statement None declared. References 1. Wingo PA, Tong T, Bolden S. Cancer statistics, CA Cancer J Clin 1995;45: Siegel R, Miller KD, Jemal A. Cancer statistics, CA Cancer J Clin 2015;65: Coleman RE, Rubens RD. The clinical course of bone metastases from breast cancer. Br J Cancer 1987;55: Kehoe SM, Zivanovic O, Ferguson SE, Barakat RR, Soslow RA. Clinicopathologic features of bone metastases and outcomes in patients with primary endometrial cancer. Gynecol Oncol 2010;117: Uccella S, Morris JM, Bakkum-Gamez JN, Keeney GL, Podratz KC, Mariani A. Bone metastases in endometrial cancer: report on 19 patients and review of the medical literature. Gynecol Oncol 2013;130: Yoon A, Choi CH, Kim TH, et al. Bone metastasis in primary endometrial carcinoma: features, outcomes, and predictors. Int J Gynecol Cancer 2014;24: Albareda J, Herrera M, Lopez Salva A, Garcia Donas J, Gonzalez R. Sacral metastasis in a patient with endometrial cancer: case report and review of the literature. Gynecol Oncol 2008;111: Myriokefalitaki E, D Costa D, Smith M, Ahmed AS. Primary bone metastasis as initial presentation of endometrial cancer (stage IVb). Arch Gynecol Obstet 2013;288: 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: Katagiri H, Okada R, Takagi T, et al. New prognostic factors and scoring system for patients with skeletal metastasis. Cancer Med 2014;3: Oken MM, Creech RH, Tormey DC, et al. Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 1982;5: Dickersin K. The existence of publication bias and risk factors for its occurrence. JAMA 1990;263: Simon R. Length biased sampling in etiologic studies. Am J Epidemiol 1980;111: Harrington KD. Orthopaedic management of extremity and pelvic lesions. Clin Orthop Relat Res 1995;312: Harrington KD, Sim FH, Enis JE, Johnston JO, Diok HM, Gristina AG. Methylmethacrylate as an adjunct in internal fixation of pathological fractures. Experience with three hundred and seventy-five cases. J Bone Joint Surg Am 1976;58: Cybulski GR, Von Roenn KA, D Angelo CM, DeWald RL. Luque rod stabilization for metastatic disease of the spine. Surg Neurol 1987;28:

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