Parathyroid cancer: Outcome analysis of 16 patients treated at the princess margaret hospital
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1 ORIGINAL ARTICLE Parathyroid cancer: Outcome analysis of 16 patients treated at the princess margaret hospital Boban M. Erovic, MD, 1 David P. Goldstein, MD, MSc, FRCS(C), 1 Dae Kim, MBChB, BDS, MSc, FRCS (Orl-HNS), PhD, 1 Ozgur Mete, MD, 2 James Brierley, MD, FRCS(C), 3 Richard Tsang, MD, FRCS(C), 3 Jeremy L. Freeman, MD, FRCS(C), 4 Sylvia L. Asa, MD, PhD, 2 Lorne Rotstein, MD, FRCS(C), 5 Jonathan C. Irish, MD, MSc, FRCS(C) 1 * 1 Departments of Otolaryngology Head and Neck Surgery/Surgical Oncology, Princess Margaret Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada, 2 Department of Laboratory Medicine and Pathobiology, Princess Margaret Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada, 3 Radiation Oncology, Princess Margaret Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada, 4 Department of Otolaryngology Head and Neck Surgery, Mount Sinai Hospital & Princess Margaret Hospital, Toronto, Ontario, Canada, 5 General Surgery/Surgical Oncology, Princess Margaret Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada. Accepted 2 November 2011 Published online 31 January 2012 in Wiley Online Library (wileyonlinelibrary.com). DOI /hed ABSTRACT: Background. The purpose of this study was to discuss the appropriate management options for parathyroid carcinomas, which is still a subject of controversy. Methods. A retrospective chart review of 16 patients with parathyroid carcinoma was undertaken to determine the clinical outcome. Results. All patients were initially treated with surgery, and 11 patients received adjuvant radiotherapy. The 5- and 10-year disease-specific survival rates were 100% and 80%, respectively; the 5- and 10-year disease-free survival rates were 69% and 43%, respectively. The 5- and 10-year locoregional control rates were 69% and 52%, respectively; the 5- and 10-year distant control rates were 89% and 74%, respectively. In this cohort, none of the clinicopathologic parameters could be defined as a predictor. Conclusion. In patients with parathyroid carcinoma, definition of prognostic factors and the role of adjuvant radiation treatment has still to be elucidated. Nevertheless, angioinvasion and positive resection margins are critical factors regarding disease-free survival in patients with parathyroid carcinomas. VC 2012 Wiley Periodicals, Inc. Head Neck 35: 35 39, 2013 KEY WORDS: parathyroid carcinoma, hyperparathyroidism, angioinvasion, disease-free survival, radiotherapy Parathyroid carcinoma is a very rare malignancy 1 and accounts for less than 1% of all cases of primary hyperparathyroidism. 2 In the absence of reliable preoperative diagnostic tests, detecting a malignant lesion at initial presentation is often difficult, and the malignant lesion is frequently misdiagnosed as parathyroid adenoma. Diagnosis is usually made on the basis of pathologic examination. Because of the very low incidence of this disease, the existing literature on this topic is mainly composed of individual case reports and case series with very small cohorts (n ¼ 1 10). 3 6 Two national database studies and 1 collective review of cases retrieved from institutions worldwide with subject numbers up to 286 patients provide an inconsistent evidence base for the best management approach for these tumors. 1,7,8 Currently, the largest single-institution study comes from the MD Anderson Cancer Center (n ¼ 27), which reported that parathyroid carcinomas are associated with a high rate of local and/or regional recurrence. In their cohort group, 11 of 26 patients developed recurrent disease after surgery. 9 En *Corresponding author: Jonathan C.Irish, Departments of Otolaryngology Head and Neck Surgery/Surgical Oncology, Princess Margaret Hospital/University Health Network, University of Toronto, Toronto, Ontario, Canada. jonathan.irish@uhn.on.ca bloc wide local resection that includes thyroidectomy and ipsilateral dissection of the adjacent tissue and lymph nodes at the time of initial surgery seems to provide the best chance of control and long-term cure. 1 Limited resection of only the enlarged parathyroid gland at the time of initial surgery for a presumed adenoma may account for the observed high recurrence rates for parathyroid carcinoma. External beam radiation has been used in an attempt to reduce the recurrence rate, but its efficacy remains controversial. 10 The purpose of this study was to assess the clinical outcomes of patients who had parathyroid cancer and had been treated at the Princess Margaret Hospital (PMH), Toronto, Ontario, Canada. PATIENTS AND METHODS Patients This study involves a retrospective medical chart review of 16 patients (6 men and 10 women) with parathyroid carcinoma treated at the PMH between 1976 and The study was performed after obtaining approval from the institutional research ethics board. The patients were identified through the PMH cancer registry. Only patients with a newly diagnosed, previously untreated parathyroid carcinoma were included in the study. Demographic, clinical, HEAD & NECK DOI /HED JANUARY
2 EROVIC ET AL. and pathological data were obtained from hospital records. Only 13 of 16 cases were reviewed by the University Health Network (UHN) endocrine pathology site group (S. L. A. and O. M.). A histopathologic diagnosis of parathyroid carcinoma was made only when there was unequivocal evidence of vascular invasion as defined elsewhere, 11 invasion of adjacent structures by a parathyroid neoplasm (local gross invasion), or loss of parafibromin, retinoblastoma protein, or p27 expression, or overexpression of p53 in a parathyroid neoplasm with unusual worrisome histological features. 12 The other 3 patients primary pathology reviews were not available; however, their clinical follow-up showed locoregional and/or distant metastatic disease. The treatment approach at the PMH for patients with parathyroid carcinoma has remained uniform over the course of this study. Surgical resection is the primary treatment of choice. In cases in which there was a possibility of residual disease after treatment, further surgical resection was recommended, depending upon patient factors (ie, patient comorbidities or preferences) and the extent of the original resection. Postoperative adjuvant radiotherapy was recommended for patients with microscopic positive margins and/or nodal metastases. Statistical analysis Statistical analysis was performed using the Statistical Package for the Social Sciences software, version 15.0, for Windows (SPSS UK, Surrey, United Kingdom). Demographic and pathologic data were summarized using descriptive statistics. Outcome measures included recurrence, overall survival, and disease-free survival. The recurrence and survival rates were calculated from the date of diagnosis to the event of interest. Recurrences were classified as locoregional or distant. Survival analysis was performed using the Kaplan Meier estimate, and statistical significance was determined using the log-rank test. Statistical significance was defined as p <.05. RESULTS Demographics Thestudyincluded16patients(6menand10women). The mean and median age at the time of diagnosis was both 54 years (range, years). Preoperative imaging included a sestamibi radioisotope scan in 3 patients; neck ultrasonography and/or CT in 6 patients, and in 7 patients, reports of preoperative imaging could not be found in the charts. Clinical examination revealed that 6 patients (38%) had a palpable mass in the central neck area. None of the patients presented with a Brown tumor. At initial presentation, there was no clinical and/or radiographic evidence of regional metastases. Three patients underwent fine-needle aspiration biopsy; on analysis, the aspirates confirmed a parathyroid lesion. The mean and median intact parathyroid hormone (PTH) levels at initial presentation were pmol/l and 117 pmol/l, respectively (range, pmol/ L). The mean and median total blood calcium levels were 4.96 mmol/l and 3.94 mmol/l, respectively (range, mmol/l); 3 patients with significantly elevated calcium levels required pamidronate therapy before surgery. TABLE 1. Demographic and treatment data of 16 patients with parathyroid gland carcinoma Characteristic Value (%)* Patients 16 Sex Female 10 (63) Male 6 (37) Age Mean y 54 Median mo 54 Range y Radiotherapy Yes 11 (69) No 5 (31) Surgery Parathyroidectomy 7 (44) Parathyroidectomy þ subtotal thyroidectomy 6 (38) Total thyroidectomy 1 (6) Total thyroidectomy þ neck dissection 1 (6) Parathyroidectomy þ thymectomy þ neck dissection 1 (6) Abbreviation: OSI, overall survival index. * Values represent the number of patients (%) except as otherwise stated. Treatment All patients were managed with primary surgery, and 11 (69%) underwent postoperative radiotherapy (Table 1). The extent of surgical management was resection of the enlarged parathyroid gland in 7 patients, and only 1 of these patients had to undergo further surgery. Another 6 patients underwent parathyroidectomy with an ipsilateral thyroidectomy. Three patients underwent more extensive surgery that included parathyroidectomy together with total thyroidectomy, with or without paratracheal node dissection and/or thymectomy. Four-gland exploration was done in 6 patients, ipsilateral neck exploration in 3 patients, and in 7 patients, no further parathyroid gland exploration was performed. Histopathological analysis The histopathological parameters provided in this study are from 13 cases that were reviewed and diagnosed as parathyroid carcinoma by the UHN endocrine pathologists. The mean and median diameters of the parathyroid specimens were 33 mm and 28 mm, respectively (range, mm). The mean volume was 22 cm 3 and the was median 8 cm 3. Capsular invasion was observed in 69% of the specimens (n ¼ 9), and invasion into the adjacent soft tissue was observed in 46% of the specimens (n ¼ 6; Table 2). Positive resection margins were observed in 8 surgical specimens (62%). Unequivocal evidence of vascular invasion was observed in 85% of the tumors (n ¼ 11); the other 2 tumors were diagnosed as parathyroid carcinoma based on the loss of Rb, p27, and parafibromin. No lymph node metastases were observed in the 2 patients that elective central compartment node dissection was performed. Outcomes The mean and median follow-up of the cohort of patients was 88 and 79 months, respectively (range, 36 HEAD & NECK DOI /HED JANUARY 2013
3 CLINICAL OUTCOMES OF PATIENTS WITH PARATHYROID CARCINOMA TABLE 2. Histopathological data of 13 patients with parathyroid gland carcinoma. Value (%) Specimens n ¼ 13 Size, mm Mean 33 Median 28 Range Volume, cm 3 Mean 22 Median 8 Range Capsule invasion Positive 9 (69) Negative 0 (0) N/A 4 (31) Vascular invasion Positive 11 (85) Negative 2 (15) Margins Positive 8 (62) Negative 0 (0) N/A 5 (38) Invasion to adjacent tissue Positive 6 (46) Negative 3 (23) N/A 4 (31) Abbreviation: N/A, not available months). The PTH levels returned to normal in 3 patients after surgery, and in 5 patients, persistent hyperparathyroidism was observed. Data regarding the postoperative PTH levels of the remaining 8 patients were not available in the archives. The calcium levels returned to normal in 13 patients immediately after surgery. From the remaining patients, the calcium levels of 1 patient returned to normal within 1 year after surgery; data regarding the postoperative calcium levels were not available for 2 patients. At the last follow-up, 13 patients (81%) were alive without disease, 2 patients (13%) were alive with disease and 1 patient (6%) died due to uncontrolled hypercalcemia. Overall, 7 patients (44%) developed recurrent disease. Locoregional recurrence was observed in 5 patients, and, in 2 of those patients, distant metastases occurred after 48 and 78 months. The mean time to recurrence was 61 months, and the median time to recurrence was 46 months (range, months). The 5- and 10-year locoregional control rates were 69% and 52%, respectively, and the 5- and 10-year distant control rates were 89% and 74%, respectively. Separate from the 5 patients with evident locoregional or distant recurrent disease, 1 patient exhibited elevated PTH levels after 76 months and the second after 152 months, neither of which had clinical or radiographic evidence of recurrence despite the rise in PTH levels. The 5- and 10-year disease-specific survival rates were 100% and 80%, respectively; the 5- and 10-year diseasefree survival rates were 69% and 43%, respectively. The mean and median survival times after disease recurrence were 66 and 64 months, respectively (range, months). Univariate analysis did not reveal any clinicopathologic predictors (Table 2) of disease-specific survival and disease-free survival. In this study cohort, angioinvasion was observed by the UHN endocrine pathology site group in 11 of 13 parathyroid carcinomas (85%). Four patients with locoregional recurrence presented with angioinvasion and subsequently 1 of them developed distant metastases within 5 years. In contrast, none of the 2 patients without vascular invasion developed recurrent disease within the follow-up period. Three of 4 angioinvasive and locally recurrent cases revealed involvement of the resection margins. Of the 5 patients with positive surgical margins, all underwent postoperative radiotherapy and 3 of them subsequently developed recurrent disease. In contrast, 1 patient who had positive margins and did not receive radiation therapy stayed disease-free during the follow-up period. Two patients who had negative but close margins did not receive radiation treatment; these patients did not develop recurrent disease. Five patients with recurrent disease underwent salvage therapy that included either only surgery (n ¼ 1) or surgery and radiotherapy (n ¼ 2). Two patients who had elevated PTH levels were watched by close follow-up. DISCUSSION The choice of an optimal treatment plan for any malignancy relies upon reliable diagnosis before treatment and involves a multimodality therapy plan that is based upon prognostic factors and includes options for the regional and systemic treatment of more aggressive and advanced disease. The clinical diagnosis and management of parathyroid carcinomas remains difficult because of the rarity and lack of diagnostic tools. Hundahl et al 1 and Lee et al 7 published epidemiologic and outcome data on 224 and 286 patients derived from national databases. Despite the large numbers, these studies are limited by the lack of detailed clinicopathologic data, with a focus mainly on survival. Moreover, national database studies do not report on the site of recurrence, control rates, and diseasefree survival. 1,7 The largest observational study was reported by Sandelin et al, 8 who performed a multiinstitutional retrospective review of 95 patients with parathyroid carcinoma. In the current literature, the majority of scientific publications on parathyroid carcinomas include case reports or small case series. 3 6 While the current study is also a case series of 16 patients, it also includes a detailed analysis of 1 of the larger cohorts of patients with parathyroid carcinoma reported in the literature treated in a uniform manner by a single tertiary care institution. Preoperative or intraoperative determination of parathyroid carcinoma is paramount in ensuring adequate resection with clear margins. Based on the current literature, a parathyroid carcinoma should be suspected whenever patients have severely elevated calcium levels, a palpable neck mass, or renal and skeletal disorders. Those clinical factors are representing significant clinical predictors for malignancy. 10,13 Patients with parathyroid carcinomas have up to 30% to 60% incidences of severe hypercalcemia (total serum calcium level >3.5 mmol/l). 3,6 Because of limited preoperative data, including data on imaging and biochemical tests, it was not possible in the current HEAD & NECK DOI /HED JANUARY
4 EROVIC ET AL. study to evaluate the previously reported predictors of parathyroid carcinoma in patients presenting with primary hyperparathyroidism. Of the 16 patients included in our study, 6 patients had a palpable neck mass before surgery, which raised the possibility of a parathyroid carcinoma. However, without ultrasonographic examination, it is very difficult to determine if patients are presenting with a concurrent thyroid neoplasm. Another challenging aspect of parathyroid carcinoma is its histopathologic examination. Diagnosis should not be based on single features like broad fibrous bands, increased mitotic activity, nuclear atypia, and pleomorphism. 12 The most reliable features for the diagnosis of parathyroid carcinoma include invasion into the surrounding tissues (local gross invasion), unequivocal vascular invasion, 11 and known distant metastasis. In this cohort, we found that patients without vascular invasion (15%) did not develop recurrence, whereas all patients with vascular invasion developed recurrent disease. We recognize that our study included a very small number of patients; nevertheless, vascular invasion seems to be an accurate predictor of worse clinical outcome compared to patients without vascular invasion. The most reliable protein profile is loss of retinoblastoma protein and parafibromin. 14,15 When immunohistochemistry was performed in our cohort, all specimens showed this protein expression profile, making the diagnosis of a parathyroid carcinoma more reliable. Parathyroid carcinomas are considered to be indolent malignancies that are associated with a good prognosis; however, recurrences occur, and in several cases, they often develop many years after initial treatment. Our data reveal similar tumor behavior in these patients, with 5- and 10-year overall survival rates of 100% and 80%, respectively, but 5- and 10-year disease-free survival rates of 69% and 43%, respectively. Despite the high survival rate, recurrences were commonly observed, with an overall recurrence rate of 44% over an extended period (range, months). Currently, there is also a limited amount of literature on clinicopathologic predictors of outcome in patients with parathyroid carcinoma. We assessed numerous potential clinical and pathologic parameters, and, similar to the previous studies, all of the factors failed to predict patient outcomes. In our study, the presence of vascular invasion and the status of surgical margins seem to be the most important features correlating with clinical outcome in patients with parathyroid carcinoma. The extent of initial surgery has previously been shown to be predictive of disease-free survival. 1,7,16 The results of several studies provide evidence indicating that initial en bloc resection of the tumor and adjacent soft tissues, which involves procedures like ipsilateral thyroid lobectomy, thymectomy, and central neck dissection, provides the best outcomes for disease-free survival. Our data also showed that most patients (86%) who developed recurrent disease had only undergone a simple parathyroidectomy, whereas all the patients who had been more aggressively treated (wide local resection or en bloc resection) by primary surgical resection remained disease free. Given the rarity of parathyroid carcinomas and the inability to distinguish preoperatively parathyroid carcinoma from adenoma, most parathyroid masses are managed initially by simple parathyroidectomy. Wide local resection to obtain clear margins and central compartment neck dissection in high-risk patients are usually secondary procedures performed after the diagnosis is made on the basis of pathological results or when infiltrating tumor behavior is observed intraoperatively. At our institution, we perform en bloc resection of the parathyroid gland, including hemithyroidectomy and paratracheal node resection on the ipsilateral side if the diagnosis of parathyroid carcinoma is highly suspected. The reported effectiveness of postoperative radiotherapy in reducing disease recurrence in high-risk patients, including patients with microscopic positive or close margins, is variable, and its role remains controversial in this regard. 7,17 To date, only a very small number of such patients have been treated with radiotherapy, even within the largest study series; of these patients, many were being treated for recurrent disease. 4,9 Our study includes the largest series with respect to the use of adjuvant radiotherapy in treating parathyroid carcinomas, where 69% (11 patients) of the study cohort was given radiation therapy after surgery. Of these 11 patients, 7 developed recurrence. Because of the very small number of patients in this and other series and a selection bias toward patients who had more advanced disease that were receiving radiation therapy, the benefits of this treatment cannot be determined. However, the finding that 3 of the 4 patients who had positive margins and underwent radiation therapy developed recurrence highlights the importance of wide resection and, therefore, the knowledge of the status of resection margins. This finding also emphasizes the fact that postoperative radiation should not be used as the sole salvage therapy after incomplete surgical resection. In summary, parathyroid neoplasms should be evaluated by experienced endocrine pathologists, because vascular invasion and the status of the resection margins are critical factors in determining the prognosis of patients with parathyroid carcinomas. Given the high survival rates of patients with parathyroid carcinoma, adequate resection (either at the time of initial surgery if the diagnosis is suspected or as a revision procedure) is paramount in disease control. The role of postoperative radiotherapy in the case of parathyroid carcinomas still remains to be elucidated and validated in multiple-institution collaborative studies that involve an adequate number of patients. REFERENCES 1. Hundahl SA, Fleming ID, Fremgen AM, Menck HR. Two hundred eightysix cases of parathyroid carcinoma treated in the U.S. between : a National Cancer Data Base Report. The American College of Surgeons Commission on Cancer and the American Cancer Society. Cancer 1999;86: Ruda JM, Hollenbeak CS, Stack BC Jr. A systematic review of the diagnosis and treatment of primary hyperparathyroidism from 1995 to Otolaryngol Head Neck Surg 2005;132: Schoretsanitis G, Daskalakis M, Melissas J, Tsiftsis DD. Parathyroid carcinoma: clinical presentation and management. Am J Otolaryngol 2009; 30: Chow E, Tsang RW, Brierley JD, Filice S. Parathyroid carcinoma the Princess Margaret Hospital experience. Int J Radiat Oncol Biol Phys 1998;41: Messerer CL, Bugis SP, Baliski C, Wiseman SM. 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