Basal Cell Adenocarcinoma of the Major Salivary Glands: A Population-Level Study of 509 Cases
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1 The Laryngoscope VC 2015 The American Laryngological, Rhinological and Otological Society, Inc. Basal Cell Adenocarcinoma of the Major Salivary Glands: A Population-Level Study of 509 Cases Kevin Y. Zhan, MD; Eric J. Lentsch, MD Objectives/Hypothesis: We sought to better characterize patient, tumor, and long-term survival characteristics of basal cell adenocarcinoma (BCAC) of the major salivary glands with the National Cancer Database (NCDB). Study Design: Retrospective database review of the NCDB ( ). Methods: We retrospectively reviewed the NCDB for all cases of major salivary gland BCAC with histologic code 8147/ 3. Relevant demographic, tumor, and survival variables were extracted and analyzed. COX multivariate regression was performed to identify prognosticators. Results: Out of 36,224 major salivary gland cancers in the NCDB, we found 509 cases of BCAC (1.4%), 88% of which were in the parotid glands, 11.2% in the submandibular glands, and 0.8% in the sublingual glands. Age at diagnosis ranged from 18 to 92 years (average 64). No gender preference was found (50.7% male). Most tumors were 2 to 4 cm in size (47.3%). Regional (11.9%) and distant metastasis (1.8%) were uncommon. Overall survival at 5 and 10 years was 79% and 62%, respectively. Although numerous variables were found to significantly impact survival on univariate regression analysis, only age 65 (hazard ratio [HR] 2.55; 95% confidence interval [CI], ; P < 0.001) and high primary tumor (T)-stage (HR 1.85; 95% CI, ; P ) remained significant prognosticators in our multivariate model. For high T-stage disease, surgery with radiation had significantly better survival than surgery alone. Conclusion: Basal cell adenocarcinoma is a rare salivary malignancy with a good prognosis. Regional and distant metastasis were uncommon. Radiation with surgery may help for higher T-stage disease. Old age and high T-stage were significant predictors of worse survival. Key Words: Basal cell adenocarcinoma, basal cell adenoma, salivary gland cancer, parotid cancer, head and neck cancer. Level of Evidence: 4. Laryngoscope, 126: , 2016 INTRODUCTION Basal cell adenocarcinoma (BCAC) is a rare salivary gland malignancy, first classified as its own distinct entity in the World Health Organization s (WHO) second edition classification of salivary gland tumors (1991). 1 They are low-grade tumors that usually arise de novo and primarily affect the parotid glands, histologically mimicking its benign counterpart, basal cell adenoma (BCA). Its synonyms include carcinoma ex-monomorphic adenoma, basaloid salivary gland carcinoma, and malignant basal cell tumor. 2 At the time of this writing, no large population-level studies of major salivary BCAC exist, with the majority of BCAC literature being individual case reports or small case series, 1 19 the largest of which is 27 patients by Ellis and Wiskovitch (1990). 17 From the Department of Otolaryngology Head and Neck Surgery, Medical University of South Carolina (K.Y.Z., E.J.L.), Charleston, South Carolina, U.S.A. Editor s Note: This Manuscript was accepted for publication September 10, The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Kevin Y. Zhan, MD, Clinical Research Fellow, Department of Otolaryngology Head & Neck Surgery, Medical University of South Carolina, 135 Rutledge Ave, MSC 550, Charleston, SC zhank@musc.edu DOI: /lary The National Cancer Database (NCDB) is the largest cancer registry in the world, capturing 70% of all cancer diagnoses in the United States. It is a highquality, de-identified database with annual quality control checks and measures, an excellent resource for the study of rare cancers. 20 With 509 patients in our study group, we present the largest study of basal cell adenocarcinoma of the major salivary glands. We aim to describe its demographic, clinical, and prognostic features and examine its long-term survival. MATERIALS AND METHODS We conducted a retrospective review of the NCDB Participant User File from 1998 to The Medical University of South Carolina Institutional Review Board deemed this not human subjects research. We searched the database for all patients with a diagnosis of major salivary gland cancer using topological International Classification of Diseases for Oncology, Third Edition (ICD-O-3) codes C079, C080, and C081 for the parotid, submandibular, and sublingual glands, respectively. Minor salivary glands is not coded in the NCDB. Primary basal cell adenocarcinoma was identified from filtering for histologic code 8147/3, as defined in the WHO classification manual. 21 Patients who presented with metastatic disease to the salivary glands and those with tumors of questionable malignant potential were excluded in this manner. From a cohort of 36,224 salivary gland cancers, we found 509 records of BCAC. Extracted variables include the following: age at diagnosis, gender, insurance status, Charlson/Deyo score, population density,
2 hospital type, region of treatment, race, surgical margin status, tumor size, type of surgery, grade, use of radiation therapy, use of chemotherapy, extraglandular spread, clinical and pathologic Tumor-Node-Metastasis stage in accordance with the American Joint Committee on Cancer classification, follow-up duration, and survival status. Population density is categorized by hometown population, with categories of metropolitan (> 250,000), urban (> 2,500), and rural (< 2,500). Academic hospitals are those that provide graduate medical programs in at least four areas. Grade was simplified into low and high. Charlson/Deyo Comorbidity scores attribute point values for 10 reported ICD-9 secondary diagnosis codes that include common but significant comorbidities such as diabetes, dementia, congestive heart failure, liver disease (different points given for degrees of severity), cerebrovascular disease, AIDS. This is truncated to 0, 1, or > 1 in the national registry, and we further simplified this into scores of 0 to 1 and > Cases were also separated by age > 65, the median age in these data. Positive occult nodal disease was defined as clinically-staged N0 (cn0) patients, who were later found to be pathologically-staged N1 (pn1). All other data fields were coded according to the NCDB database instructions. This data was then imported into version 23 of the Statistical Package for Social Sciences (IBM Corp., Armonk, NY) for further analysis. Patients missing variables were removed from pertinent analysis. Primary outcome was overall survival (OS) at 5 and 10 years (where applicable). Categorical variables are presented as frequency and percentage. Univariate and multivariate COX regression analysis were performed to adjust for confounders. A forward step-wise entry method was used with P 0.1 as exclusion criteria. Overall survival data were tabulated using the life-tables function, and pairwise comparisons between survival curves were done using the Kaplan-Meier method and log-rank testing, unless otherwise specified. A P value of < 0.05 was considered significant for all statistical tests. RESULTS We identified 509 basal cell adenocarcinomas of the major salivary glands (1.4% of all major salivary cancers), with 88.0% found in the parotid glands, 11.2% in the submandibular glands, and 0.8% in the sublingual glands. Average age at diagnosis was 64 (standard deviation 14), with a range from 18 to 92 years. Median age was 65 years. Figure 1 shows the incidence of BCAC by age; peak incidence is seen between ages 65 to 75. No gender preference was found (50.7% male). The majority of patients were Caucasian (89.9%), with 6.6% of cases in African Americans and 3.6% in other ethnicities. Most patients either had private insurance (48.0%) or Medicare/Medicaid (47.8%), with 2.9% as uninsured. A majority of patients had care at community cancer hospitals (59.5%), lived in metropolitan areas (84.1%), and had low comorbidity scores (95.7% with Charlson/Deyo scores of 0 1). Fig. 1. Incidence by age at diagnosis. [Color figure can be viewed in the online issue, which is available at Tumor and Disease Characteristics On clinical assessment, 74% of tumors were staged ct1 T2 and regional metastasis was clinically evident in 6.7% of patients. Most tumors were 2 to 4 cm in size (47.3%), with 35.8% under 2 cm. On pathologic staging, incidence of regional metastasis rose to 11.9% (8.6% N1, 3.3% N2, and no N3 disease). Occult nodal disease incidence (cn0 that are later pn1) was 5.7%. Distant metastatic disease was exceptionally rare overall (1.8%). However, incidence varied by primary site, though this analysis was limited by small sample size. By primary site, distant metastasis was found in four of 448 (0.9%) of parotid tumors, four of 57 (7%) of submandibular tumors, and one of four (25%) of sublingual tumors. Early-stage disease was more common than advancedstaged disease (67.8% vs. 32.2%), with stage I disease (43.4%) being most common. Grade information was only available in 42% of our dataset, with 48 cases (22.4% of available data, 9% of all cases) registered as high-grade. This is surprising because BCAC is traditionally understood as a low-grade malignancy. However, in Nagao et al. s review of 11 BCAC, the authors found abundant histologic evidence of necrosis, solid growth pattern, high Ki-67 index, and frequent p53 overexpression. 23 We performed a subgroup analysis and found that high-grade tumors were more often staged T3 to T4 (50% vs. 23.9% low grade; P ), more likely to receive surgery with radiation (60.4% vs. 35.2%; P < 0.001), and presented more with extraglandular spread (38.9% vs. 18.3%; P ). Of note, high grade had no significant impact on survival compared to low-grade tumors (P ). Moreover, no significant differences were seen in chi-squared analysis when comparing gender, type of treating hospital, or margin status by grade. All BCAC in our dataset were included for all analyses. Treatment and Overall Survival and Regression Analysis Surgery alone was the most common treatment modality (45.1%), followed by surgery with radiation (39.4%) and no therapy (6.9%). Surgical margins were frequently positive (35.9%), and extraglandular spread was seen in 22% of cases. Overall survival by significant clinical and pathologic variables is shown in Table I. Five- and 10-year survival were 79% and 62%, respectively. We found that 1087
3 TABLE I. Overall Survival by Numerous Variables. Variable N 5-Year OS 10-Year OS P Value Variable N 5-Year OS 10-Year OS P Value Overall 79% 62% Distant Metastasis <.001 Hospital Type No % 63% Community % 58% Yes 7 29% Academic % 70% Stage Insurance Type <.001 I II % 69% Private 84 86% 76% III IV % 52% Medicare/Medicaid 69 70% 47% Positive Margins Age <.001 No % 68% < % 79% Yes % 53% % 47% Treatment in T3 T4 Disease Tumor Size Surgery 45 53% 38% < 2 cm (A) % 72% A&B Surgery 1 radiation 61 75% 60% 2 4 cm (B) % 58% A&C > 4 cm (C) 76 67% 53% B&C T-Stage <.001 T1 T % 69% T3 T % 49% OS 5 overall survival; T 5 tumor. worse survival was significant associated with older age, community hospitals (vs. academic), Medicaid/Medicare insurance (vs. private), high T-stage, distant metastasis, advanced stage, and positive margins. Kaplan-Meier survival plots by important prognosticators are shown in Figures 2A D. No significant survival differences were seen when comparing by primary site (all pairwise comparisons P > 0.142), gender (P ), ethnicity (all pairwise comparisons P > 0.20), regional metastasis (P ), extraglandular spread (P ), and treatment (comparing surgery vs. surgery with radiation overall; P ). However for high T-stages (T3 T4), surgery with radiation showed a significant survival benefit (P ) (Fig. 2D). COX regression data are summarized in Table II. In our multivariate model, only high T-stage and old age remained significant, independent negative prognosticators, with age 65 having the worst hazard ratio (HR) of 2.55 (P < 0.001). DISCUSSION Basal cell adenocarcinoma is histologically similar to its benign counterpart, basal cell adenoma, and differentiation can be especially challenging with small biopsy specimens. 23 Both contain similar cell populations and morphologic categorizations. 17 Cytologic differentiation is virtually impossible, making fine-needle aspiration biopsy inadequate for this task. 24 Invasive activity is the hallmark of BCAC, and various staining methods may be helpful for differentiation. Differential diagnosis of BCAC includes basal cell adenoma, adenoid cystic carcinoma, basaloid squamous carcinoma, and cutaneous basal cell carcinoma with deep invasion. 25 Of note, 1088 BCAC arising from pleomorphic adenomas have also been reported. 24 The presence of 48 cases of high-grade BCAC (9% of all cases) certainly suggests the possibility that a more aggressive histologic and clinical variant may exist. Given the lack of a formal grading system for BCAC, these cases may be reflect the more aggressive features of BCAC reported by Nagao et al. (solid growth, p53 staining, high Ki-67 index). 23 In our series, these patients presented with higher T-stages, and were treated more often with surgery with radiation versus surgery alone. However, we were unable to find a significant survival difference when comparing by grade. Without the ability to verify the histopathology in our study design, this is certainly a limitation in our analysis. Clinically, most patients with BCAC report a slowly enlarging, nontender mass. Symptom duration may range from 3 weeks to 7 years prior to diagnosis, with average of 1.8 years in Ellis and Wiskovitch s series. 1,17 In their series of 29 patients, only three cases (10%) presented with pain or tenderness, and two patients experienced rapid swelling (6.8%). Additionally, 10% to 15% of BCAC cases are associated with other cutaneous lesions such as eccrine cylindromas and trichoepitheliomas; thus, dermatologic examination is warranted. We found regional (11.8%) and distant metastases to be uncommon (1.9%). Aside from incidence of distant metastasis, we did not find any significant differences in demographic or disease characteristics by primary site. When present, distant spread to the lungs, 17 scalp, 19 manubrium, 24 and even hand 8 have been reported. Basal cell adenocarcinoma frequently recurs (16.7% 50%), 1,23,24 with time to recurrence varying from 6 months to 2 years. Notably, one report described a patient who recurred four times. Nagao et al. reported five
4 Fig. 2. Kaplan-Meier survival plot by primary site (A), old age (B), T-stage (C), and treatment modality in high T-stages (D). T 5 tumor. [Color figure can be viewed in the online issue, which is available at recurrences in their series of 11 BCACs, despite tumorfree surgical margins in all cases. Four out of five occurred after total gland removal (either total parotidectomy or submandibular gland excision), with three having also received adjuvant radiation. 23 Although the NCDB lacks disease-free data, our high incidence of positive surgical margins may be a contributing factor to recurrence. Based on Nagao s small case series, BCACs seem to recur despite adequate surgical resection and even radiation therapy. TABLE II. COX Regression Analysis. Univariate HR (95% CI) P Value Multivariate HR (95% CI) P Value Community hospital 1.47 ( ) High T-Stage (T3 T4) 1.85 ( ) Medicare/Medicaid 2.41 ( ) <.001 Age ( ) <.001 Age ( ) <.001 High T-Stage (T3 T4) 2.27 ( ) <.001 Distant metastasis 6.74 ( ) <.001 Advanced stage (III IV) 1.88 ( ) Positive margins 1.47 ( ) CI 5 confidence interval; HR 5 hazard ratio; T 5 primary tumor. 1089
5 No consensus exists regarding treatment, with some reports recommending local excision and others suggesting total parotidectomy for even benign basal cell adenomas (membranous type) out of concern for recurrence. 26 In our analysis, we did find a significant survival benefit with adding radiation therapy to surgery for high T-stage tumors (T3 T4). We found that OS is good, even 10 years out (62%). Despite numerous prognosticators in univariate analysis, high T-stage (HR 1.85; 95% confidence interval (CI), ) and age > 66 (HR 2.55; 95% CI, ) are the only two significant predictors of worse survival. Moreover, their HRs were modest giving credence to the good prognosis of this disease. CONCLUSION Basal cell adenocarcinoma is a rare major salivary gland malignancy with a good overall prognosis. Both regional and distant metastases were uncommon, and disease characteristics did not significantly differ by primary site. Radiation added to surgery may help for higher T-stage tumors. We found old age and high T-stage to be significant independent predictors of worse survival. Acknowledgments The data used in the study are derived from a de-identified NCDB file. The American College of Surgeons and the Commission on Cancer have not verified and are not responsible for the analytic or statistical methodology employed, or the conclusions drawn from these data by the investigator. BIBLIOGRAPHY 1. Muller S, Barnes L. Basal cell adenocarcinoma of the salivary glands. Report of seven cases and review of the literature. Cancer 1996;78: Quddus MR, Henley JD, Affify AM, Dardick I, Gnepp DR. Basal cell adenocarcinoma of the salivary gland: an ultrastructural and immunohistochemical study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1999;87: Tse GM, To EW, Yuen EH, Chen M. Basal cell adenocarcinoma of the salivary gland: report of a case with morphology on fine needle aspiration cytology. Acta Cytol 2001;45: Ozgun A, Tuncel T, Emirzeoglu L, Haholu A. 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