Leiomyosarcoma of the head and neck: A 17-year single institution experience and review of the National Cancer Data Base
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1 Received: 9 April 2017 Revised: 21 August 2017 Accepted: 16 November 2017 DOI: /hed ORIGINAL ARTICLE Leiomyosarcoma of the head and neck: A 17-year single institution experience and review of the National Cancer Data Base Alan D. Workman BA 1 Douglas R. Farquhar MD 2 Robert M. Brody MD 2 Arjun K. Parasher MD 2 Ryan M. Carey MD 1 Michael T. Purkey MD 2 Danish A. Nagda MD 2 John S. Brooks MD 3 Lee P. Hartner MD 4 Jason A. Brant MD 2 Jason G. Newman MD 2 1 Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pennsylvania 2 Department of Otorhinolaryngology - Head and Neck Surgery, University of Pennsylvania, Philadelphia, Pennsylvania 3 Department of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 4 Penn Oncology Hematology Associates, Philadelphia, Pennsylvania Correspondence Jason Newman, Department of Otorhinolaryngology - Head and Neck Surgery, University of Pennsylvania Medical Center, 5th Floor Ravdin Building, 3400 Spruce Street, Philadelphia, PA Jason.newman@uphs.upenn.edu Abstract Background: Leiomyosarcoma is a rare neoplasm of the head and neck. The purpose of this study was to present our single-institution case series of head and neck leiomyosarcoma and a review of cases in the National Cancer Data Base (NCDB). Methods: Patients with head and neck leiomyosarcoma at the University of Pennsylvania and in the NCDB were identified. Demographic characteristics, tumor factors, treatment paradigms, and outcomes were evaluated for prognostic significance. Results: Nine patients with head and neck leiomyosarcoma from the institution were identified; a majority had high-grade disease and cutaneous leiomyosarcoma, with a 5-year survival rate of 50%. Two hundred fifty-nine patients with leiomyosarcoma were found in the NCDB; macroscopic positive margins and high-grade disease were associated with poor prognosis (P <.01), and positive surgical margins were related to adjuvant radiation (P <.001). Conclusion: Head and neck leiomyosarcoma presents at a high grade and is preferentially treated with surgery. Several demographic and tumor-specific factors are associated with outcomes and prognosis. KEYWORDS head and neck, leiomyosarcoma, National Cancer Data Base, outcomes, treatment strategies 1 INTRODUCTION Leiomyosarcoma is a smooth muscle-derived malignant neoplasm most commonly found in the uterus and gastrointestinal tract. 1 A rare and relatively aggressive soft tissue sarcoma, it has one of the highest mortality rates of head and neck sarcomas. 2 Leiomyosarcoma accounts for 1%-4% of soft tissue sarcomas in the head and neck. 3 5 Although it most commonly presents cutaneously, 3 itcanbefoundinawidevarietyof areas, including the larynx, 6,7 scalp, and auricular region. 8 As it is the least common head and neck sarcoma, 9 diagnosis of leiomyosarcoma is often missed or delayed 10 leading to a more advanced stage of disease at the time of diagnosis. The tumor can be superficial in the cutaneous or subcutaneous layer, or can present in the deeper tissues. Cutaneous leiomyosarcoma develops from erector pili muscles of hair follicles, whereas a subcutaneous variant is derived from vascular smooth muscle in the arterial tunica media. 8 These 2 variants present with unique recurrence rates, metastatic potential, and other factors of prognostic importance. In addition to these origins, tumor development is postulated to occur from pluripotent mesenchymal cells. 11 Leiomyosarcoma can present as a primary tumor with a solitary nodule, whereas the presence of more than one nodule is suspicious for metastases from other areas of the body. 12 A number of risk factors have been associated with development 756 VC 2017 Wiley Periodicals, Inc. wileyonlinelibrary.com/journal/hed Head & Neck. 2018;40:
2 WORKMAN ET AL. 757 of leiomyosarcoma, including radiation and chemical exposure, retinoblastoma, and prior chemotherapy Once a diagnosis of leiomyosarcoma is established, surgery is overwhelmingly the preferred method of treatment. 17 Surgical margins between 2 and 5 cm have previously been recommended. 18 However, newer reports are showing that a margin closer to 1 cm, 19 or 0.5 cm if adjuvant radiation is used, 20 may hold similar prognoses to more aggressive resection while improving morbidity. For inoperable cases, radiation with or without chemotherapy is recommended, although success rates are mixed. 5,8,15,21 Compared to those of the uterus or gastrointestinal tract, leiomyosarcoma of the head and neck is more aggressive and generally has a worse prognosis. 22 Tumor size >5 cm, positive margins, high mitotic rate, high-grade, necrosis, nodularity, advanced age, and deep tumor extent are all factors that can predict a poor survival time or recurrence rate. 8,14,19 Leiomyosarcoma of the head and neck has a very high rate of regional recurrence that is not necessarily contiguous with the original tumor, even in cases of complete excision and adjuvant therapy. 23 Local recurrence is the most common cause of mortality, 15 and 5-year rates of recurrence-free survival have been reported to be as low as 32%. 17 Metastases are almost exclusively hematogenous, 24 and metastases to the cervical lymph nodes are rare 25 but documented in several cases. 13,23 Cervical lymph node dissection is generally regarded as unnecessary unless there is clinical or radiographic evidence of lymph node metastases. 26 Metastases most frequently travel to the liver, lungs, and bones. 21 Overall, 5-year survival rates vary in the literature, but generally fall between 35% and 75%. 12,24 In a subset of patients, recurrence-free survival for as long as 10 years has been reported. 15 The rarity of head and neck leiomyosarcoma contributes to the relative lack of data in the literature. Previous studies are mainly case reports from high-volume institutions, and one meta-analysis of the case reports published in However, the heterogeneity of the data in this type of metaanalysis is a reason for concern. Information from a single institution can be effective in obtaining a more homogenous dataset, and it eliminates confounding variations in patient evaluation, treatment, and outcomes. However, pooled reporting across centers can provide larger numbers of patients to elucidate important prognostic factors and to eliminate biases that may be present in single-institutional reporting. In this study, our purpose was to supplement existing reports and analyses with 9 patients with pathologically confirmed leiomyosarcoma who were treated at the University of Pennsylvania from 1998 to To provide additional insight and context, we also reviewed and analyzed all leiomyosarcoma cases in the National Cancer Data Base (NCDB). The combination of NCDB data and our retrospective cohort study offers improved characterization of leiomyosarcoma clinical management, recurrence, and survival. 2 MATERIALS AND METHODS 2.1 Patient selection and data collection After obtaining approval from the University of Pennsylvania Institutional Review Board, we performed a retrospective cohort study of all patients with head and neck leiomyosarcoma treated at either Pennsylvania Hospital or the Hospital of University of Pennsylvania over a 17-year period ( ). Patients were identified using an internal pathology database. Inpatient and outpatient medical records as well as pathology reports were accessed and reviewed. The diagnosis of each case was confirmed with an independent pathology review before publication, as the criteria for pathologic diagnosis of leiomyosarcoma have changed over the past 20 years. All patients included had primary leiomyosarcoma at presentation. All operations had a curative intent and none were palliative procedures; however, in some cases, unresectable disease was encountered during surgery. All patients lacking information on treatment or follow-up were excluded from this study. Factors examined included age, sex, ethnicity (defined as white, African-American, Hispanic, Asian, Other, or unknown), medical history of radiation (for a prior disease, and into the field in which the sarcoma originated) or chemotherapy, anatomic subsite, tumor stage, tumor grade, treatment (chemotherapy, radiotherapy, and/or surgery), treatment efficacy (resectability, negative margins, and tumor recurrence), and overall survival. A negative margin was defined as a minimum of 2 mm. Histopathological grading and staging were performed by 1 of the authors and in accordance with the seventh edition of the American Joint Committee on Cancer and International Union Against Cancer staging system for soft tissue sarcomas. 2.2 National Cancer Data Base analysis The NCDB is jointly sponsored by the American College of Surgeons and the American Cancer Society and is a clinical oncology database with data collected from >1500 Commission on Cancer accredited facilities. The NCDB, established in 1989, is a nationwide, facility-based, comprehensive clinical surveillance resource oncology dataset that includes >34 million records and represents >70% of newly diagnosed cancer cases in the United States ( programs/cancer/ncdb). The NCDB uses the International Classification of Diseases for Oncology for topography (primary site) and morphology (histology) definitions. 27 Information for tumors with location codes corresponding to
3 758 WORKMAN ET AL. TABLE 1 University of Pennsylvania patients with leiomyosarcoma Patient Sex Age Stage Grade Site Size Treatment Margins Recurrence Follow-up OS Final status 1 M 83 IIA 3 Scalp 5 cm Surg 84 mo 84 mo DOC 2 M 50 IIA 3 Parotid <5 cm Surg/XRT R2 38 mo N/A NED 3 M 79 IB 3 Scalp 5 cm Surg R1 20 mo 20 mo DOC 4 F 80 IIA 3 Nasal cavity 5 cm Surg/XRT 10 mo N/A NED 5 F 60 IIA 2 Scalp <5 cm Surg/XCRT 24 mo 24 mo DOC 6 M 58 III 3 Skull base 5 cm Surg/XCRT R1 20 mo 27 mo 27 mo DOD 7 F 43 III 3 Nasal cavity 5 cm Surg/XCRT 16 mo 61 mo N/A AWD 8 M 61 IIA 3 Skin <5 cm Surg/XCRT 2 mo 12 mo 12 mo DOD 9 F 22 IA 1 Scalp <5 cm Surg/XRT 156 mo N/A NED Abbreviations: AWD, alive with disease; DOC, died of other causes; DOD, died of disease; N/A, not applicable; NED, no evidence of disease; OS, overall survival; R1, microscopic margins; R2, macroscopic margins; Surg, surgery; XCRT, adjuvant chemoradiotherapy; XRT, adjuvant radiotherapy. subsites of the head and neck, with the histology code 8890 (leiomyosarcoma) diagnosed between 2004 and 2012, were obtained from the NCDB on March 4, Cases were not included if they were recorded as having had surgery at a distant site or if there was evidence of metastatic disease. Race was grouped as white, Black, and other. Only cases with a behavior code of 3 0 were included: Malignant neoplasms stated or presumed to be primary. Basic demographic data for all patients was reported, including age, sex, and race. Tumor and treatment factors, incorporating subsite, grade, adjuvant therapy, and surgical margins were analyzed using Cox proportional hazards modeling (single multivariable model) against the primary outcome of survival. Chisquare analysis was also used to evaluate associations between treatment modality and margin status. The majority of patients presented with stage II disease (56%), with 22% each in stages I and III. The vast majority presented with grade 3 disease (78%); there were single diagnoses of grade 1 and grade 2 in our cohort. There were 5 cases of cutaneous leiomyosarcoma; 4 of these were located on the scalp, and 1 over the angle of the mandible. Other locations were the nasal cavity, 2 the skull base, and the parotid gland. All tumors were treated surgically; 6 (67%) had resection with negative margins. Seven patients (78%) also received radiation with an average dose of 6080 centigray (cgy), and 4 (44%) received chemotherapy. The 2 patients who did not receive radiotherapy both were close to 80 years old at the time of diagnosis with multiple medical comorbidities, and both had wide surgical excisions of scalp leiomyosarcoma with negative margins. 3 RESULTS 3.1 Patient and tumor characteristics Among the 248 cases diagnosed as head and neck sarcoma at the University of Pennsylvania between 1998 and 2015, 26 (11%) were identified as leiomyosarcoma. Of these, 11 were excluded from the study due to insufficient information, and 6 were excluded after subsequent pathology review due to either a change in diagnosis or clarification of anatomic location, resulting in a final study cohort of 9 patients (Table 1). Fifty-six percent of these patients were men, and the median age at diagnosis was 61 years. Most patients were white (67%), followed by Hispanic (11%) and African American (11%) race or ethnicity. The median follow-up was 27 months with a mean of 48 months and a range of 10 to 156 months. 3.2 Primary outcomes: Survival and recurrence The 1-year overall and disease-specific survival for patients with leiomyosarcoma at our institution was 88%, with disease-free survival at 89%. The 5-year overall survival (for the 6 of 9 patients with adequate follow-up) was 50%, with a disease-specific survival of 70% and disease-free survival of 63% (see Figure 1). The median survival for all patients in the cohort was 27 months. In addition, 33% of tumors recurred. Patient 6 (Table 1) presented with a recurrence in the orbital floor and neck, and underwent additional surgery. Patient 7 had a recurrence in the neck, and received additional chemoradiation. Patient 8 had a neck and pulmonary recurrence, and underwent palliative chemotherapy. At the time of death or end of follow-up, 3 patients had no evidence of disease (NED), 1 patient was alive with disease, 3 patients
4 WORKMAN ET AL. 759 TABLE 3 Treatment and outcomes of leiomyosarcoma in the National Cancer Data Base Variables No. of patients (%) Hazard ratio (P value) a FIGURE 1 Single institution overall survival, disease-specific survival, and disease-free survival for 9 patients with head and neck leiomyosarcoma had died of other causes, and 2 patients died of their disease. A post-hoc analysis was performed on cutaneous tumors to assess for differences in demographics or disease presentation. Although there was a trend for cutaneous tumors to present as low-stage disease (100% of cutaneous tumors TABLE 2 Patient and tumor characteristics of leiomyosarcoma in thenationalcancerdatabase Variables No. of patients (%) Total patients 259 Age, years Sex Male 197 (76) Female 62 (24) Race White 239 (92) Black 10 (4) Other 5 (2) Unknown 5 (2) Primary site Skin 152 (59) Oral cavity 24 (9) Nasopharynx 12 (5) Nasal cavity/sinuses 41 (16) Larynx/hypopharynx 15 (6) Parotid 10 (4) Thyroid 5 (2) Size, cm (55) 5 17 (7) Unknown 97 (38) Lymph nodes Examined and negative 25 (10) Examined and positive 2 (1) Not examined 228 (88) Unknown 2 (1) Age, years <54 58 (22) 1.0 (ref) (13) 2.54 (.03) (20) 1.75 (.23) > (42) 5.41 (<.001) Sex Male 197 (76) 1.0 (ref) Female 62 (24) 1.70 (.04) Treatment Radiation alone 10 (4) 1.0 (ref) Surgery alone 168 (65) 0.20 (.005) Surgery then radiation 56 (22) 0.15 (.002) Neoadjuvant radiation 4 (2) Chemotherapy 27 (10) Margins Negative 190 (73) 1.0 (ref) Positive, microscopic 11 (4) 1.32 (.58) Positive, macroscopic 1 (1) (.004) Tumor subsite Skin 155 (58) 0.59 (.06) Other 104 (42) 1.0 (ref) Grade 1 32 (13) 1.0 (ref) 2 33 (13) 1.80 (.27) 3 38 (15) 3.76 (.006) 4 19 (7) 3.09 (.05) a Cox proportional hazards modeling. Figures in boldface indicate statistical significance. were stage 1 or 2 vs 50% of other tumors; P 5.167), and to have negative margins (80% of cutaneous tumors vs 50% of other tumors), there were no significant associations due to the small sample size. 3.3 National Cancer Data Base analysis Two hundred fifty-nine patients in the NCDB were found to have leiomyosarcoma of the head and neck. Demographic and tumor-specific characteristics can be found in Table 2. At the time of diagnosis, the average patient age was 67.7 years with a male preponderance (76%), and age over 74 years was associated with increased mortality when compared with younger patients (Table 3; P <.001). Ninety-two percent of the patients were white. As expected, a majority of head and neck leiomyosarcoma was on the skin, whereas
5 760 WORKMAN ET AL. margins were significantly more likely to receive radiation treatment than those with negative margins (chi-squared, P <.001). Of note, most patients (88%) did not receive a neck dissection. Of the 27 patients who had a neck dissection performed at the time of surgery, 2 had identified nodal disease on pathologic examination. 4 DISCUSSION FIGURE 2 Kaplan-Meier overall survival curve for patients with head and neck leiomyosarcoma in the National Cancer Data Base other sites, such as the oral cavity, nasopharynx, nasal cavity and sinuses, larynx, parotid, and thyroid, were also affected by leiomyosarcoma and are included in the analysis. The majority of tumors in the NCDB presented at <5 cm in greatest dimension. Figure 2 demonstrates overall survival of patients with leiomyosarcoma in the NCDB, and Figure 3 compares survival of patients with cutaneous leiomyosarcoma to those with noncutaneous leiomyosarcoma. Leiomyosarcoma treatment reported in the NCDB was most often surgery alone, seen in 65% of the cases. Surgery followed by radiation was utilized in close to one-quarter of patients, whereas chemotherapy was utilized in 10% of patients. Ten percent of patients received no treatment for their disease. Cox proportional hazards analysis demonstrated that patients receiving either surgery or surgery and radiation had significantly improved survival than those receiving radiation treatment alone. Most patients with known margin status after surgery had negative margins (73%). After surgery, macroscopic positive margins were also associated with decreased survival compared with patients with negative margins, and grades 3 and 4 disease were also poor prognostic factors when compared to grade 1 disease. Individuals without margin or tumor grade data were excluded from this subanalysis. Patients with positive FIGURE 3 Kaplan-Meier overall survival curves for patients with cutaneous and noncutaneous head and neck leiomyosarcoma in the National Cancer Data Base Head and neck leiomyosarcoma generally follows an aggressive course and is preferentially treated with surgery. By the time of diagnosis, most tumors have a moderate-to-high histologic grade, and infrequently respond to radiation or chemotherapy. 22 Pathologically, the tumors often present with hemorrhage or necrosis. Mitotic activity and tumor size are key to determining malignant nature. 23 Different variants of the tumor can present superficially or in a more deep-seated area. A superficial subset can be found in the cutaneous or subcutaneous layer. The 9 patients from the University of Pennsylvania were a median age of 61 years at diagnosis, and the patients with leiomyosarcoma at this institution are of similar age to those seen in prior reports, with the average age at presentation ranging from 50 to 64 years in the literature 3,17 and up to 68 years in the NCDB data. There is some controversy in the existing literature about sex predilection, with some reports showing biases toward men or women, and others, including our case series, showing a relatively equal distribution. 3,5,8,12,14 This is in stark contrast to the NCDB, which shows a definitive predilection of leiomyosarcoma for men, representing almost three-quarters of all patients recorded. Additionally, previous studies have shown that women have one-third less mortality than men with comparable disease, 28 but the data in the NCDB do not corroborate this phenomenon. The high proportion of high-grade tumors seen in our patient population (78%) is slightly greater than that seen in the Eppsteiner et al 3 meta-analysis of 578 patients with leiomyosarcoma. Tumor grade was not known in over half of the patients from the NCDB, but grade distribution was fairly evenly distributed in those patients with available data. As expected, NCDB patients with higher-grade tumors had decreased survival. Tumor location varied in our patient population and in the NCDB, but the tumors were most frequently found to be cutaneous and on the scalp. Cutaneous leiomyosarcoma is more commonly encountered on the head and neck than anywhere else in the body. 29 This superficial location is much more amenable to surgical resection than the deeper tumors of the nasal cavity or skull base. Cutaneous tumors may be a subset of leiomyosarcoma that have an improved prognosis, in accordance with literature showing that complete resection of low-grade tumors results in lower rates of recurrence, and
6 WORKMAN ET AL. 761 improved 5-year survival for cutaneous leiomyosarcoma. 3 In the NCDB, leiomyosarcoma of the skin trended toward improved prognosis (P 5.06) but this did not reach significance. The data from the NCDB is most useful in evaluating treatment patterns as well as prognostic factors associated with treatment. Most patients receive surgery as a single treatment modality, but radiation is utilized in some cases as an adjuvant or neoadjuvant therapy. The association between patients receiving adjuvant radiation and positive margin status after surgery is likely reflective of the utilization of additional treatment modalities in the absence of definitive surgical control. Chemotherapy also may play a role in the treatment of head and neck leiomyosarcoma, as some studies have demonstrated a significant decrease in local and distant recurrence with the use of systemic adjuvant chemotherapy. 30 Additionally, the NCDB data shows that most surgeons do not perform an elective neck dissection for leiomyosarcoma, and this seems to be appropriate in the setting of a low incidence of lymph node metastasis (ie, only 2 of 27 patients in the NCDB who underwent neck dissections had positive nodes). Overall, 1-year survival in our cohort was 88%, and 5- year survival was 50%. These rates are slightly lower than those published in a meta-analysis, in which 5-year survival rates were close to 57%. 3 This difference is likely due to a higher proportion of high-grade tumors in our cohort. Nonetheless, both studies illustrate the poor prognosis of this disease. As with other types of head and neck tumors, a multidisciplinary approach may optimize patient management and survival. 29 Overall, leiomyosarcoma is associated with a high mortality, and age may be a risk factor for a poor prognosis. Surgery is the preferred treatment, with radiation utilized more frequently when negative margins cannot be obtained. There are several other demographic and tumor-specific factors identified in our case series and in the NCDB that are associated with patient outcomes and prognosis. ORCID Alan D. Workman BA REFERENCES [1] McLeod AJ, Zornoza J, Shirkhoda A. Leiomyosarcoma: computed tomographic findings. Radiology. 1984;152: [2] Mattavelli D, Miceli R, Radaelli S, et al. Head and neck soft tissue sarcomas: prognostic factors and outcome in a series of patients treated at a single institution. Ann Oncol. 2013;24: [3] Eppsteiner RW, DeYoung BR, Milhem MM, Pagedar NA. Leiomyosarcoma of the head and neck: a population-based analysis. 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Metastatic leiomyosarcoma of the palate. J Oral Maxillofac Surg. 1990;48: [12] Snowden RT, Osborn FD, Wong FS, Sebelik ME. Superficial leiomyosarcoma of the head and neck: case report and review of the literature. Ear Nose Throat J. 2001;80: [13] Papoian V, Yarlagadda BB, Devaiah AK. Multifocal, recurrent sinonasal leiomyosarcoma: case report and review of literature. Am J Otolaryngol. 2014;35: [14] Pop M, Botar Jid C, Hotoleanu C, Vasilescu D, Sfrangeu S. Superficial leiomyosarcoma of the scalp: a case report. Med Ultrason. 2011;13: [15] Ulrich CT, Feiz-Erfan I, Spetzler RF, et al. Sinonasal leiomyosarcoma: review of literature and case report. Laryngoscope. 2005;115: [16] Fitzpatrick SG, Woodworth BA, Monteiro C, Makary R. Nasal sinus leiomyosarcoma in a patient with history of non-hereditary unilateral treated retinoblastoma. Head Neck Pathol. 2011;5: [17] Akcam T, Oysul K, Birkent H, Gerek M, Yetiser S. 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7 762 WORKMAN ET AL. [24] Kudo M, Suzaki H. Leiomyosarcoma arising in the nasal cavity. Grand Rounds. 2012;13:4-11. [25] Izumi K, Maeda T, Cheng J, Saku T. Primary leiomyosarcoma of the maxilla with regional lymph node metastasis. Report of a case and review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 1995;80: [26] Mindell RS, Calcaterra TC, Ward PH. Leiomyosarcoma of the head and neck: a review of the literature and report of two cases. Laryngoscope. 1975;85: [27] World Health Organization. International Classification of Diseases for Oncology, 3rd Edition (ICD-O-3) who.int/classifications/icd/adaptations/oncology/en/. Accessed June 1, [28] Wu AW, Suh JD, Metson R, Wang MB. Prognostic factors in sinonasal sarcomas: analysis of the surveillance, epidemiology and end result database. Laryngoscope. 2012;122: [29] Annest NM, Grekin SJ, Stone MS, Messingham MJ. Cutaneous leiomyosarcoma: a tumor of the head and neck. Dermatol Surg. 2007;33: [30] Pervaiz N, Colterjohn N, Farrokhyar F, Tozer R, Figueredo A, Ghert M. A systematic meta-analysis of randomized controlled trials of adjuvant chemotherapy for localized resectable softtissue sarcoma. Cancer. 2008;113: How to cite this article: Workman AD, Farquhar DR, Brody RM, et al. Leiomyosarcoma of the head and neck: A 17-year single institution experience and review of the National Cancer Data Base. Head & Neck. 2018;40:
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