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1 Pulmonary Sclerosing Hemangioma With Lymph Node Metastases Report of 4 Cases Aya Miyagawa-Hayashino, MD; Henry D. Tazelaar, MD; Desiree J. Langel, MD; Thomas V. Colby, MD Context. Sclerosing hemangioma is an unusual pulmonary tumor. Previously, 4 patients with pulmonary sclerosing hemangioma and lymph node metastases have been described in the literature. Objective. To report 4 additional cases of metastatic sclerosing hemangioma. Design. Retrospective review of the authors consultation files and review of histologic sections of pulmonary tumors and lymph node metastases. Results. Four cases of a morphologically benign pulmonary sclerosing hemangioma with regional lymph node metastases (including hilar, peribronchial, and interlobar metastases) were identified. The patients (3 female, 1 male) had a mean age of 39 years (range, years). The tumors ranged in size (greatest dimension) from 1.5 to 4.7 cm (mean, 3.1 cm). The pulmonary tumors were typical circumscribed sclerosing hemangiomas without mitotic activity, angiolymphatic invasion, or necrosis. One tumor had focal cytologic atypia. The metastases were identified in hilar lymph nodes that were removed at operation for the lung nodule. One patient received adjuvant chemotherapy for adenocarcinoma. All of the patients are alive. No recurrences or residual disease has been detected at a mean follow-up of 4.7 years (range, years). Conclusions. On the basis of case data from the 4 patients described here and the 4 patients described previously, metastases to regional lymph nodes from pulmonary sclerosing hemangioma may occur but are rare and do not appear to affect prognosis. (Arch Pathol Lab Med. 2003;127: ) First reported by Liebow and Hubbell 1 in 1956, sclerosing hemangioma (SH) is an unusual pulmonary tumor. Histologically, SH has no known extrapulmonary counterpart. Two SH cell types are recognized: lining cells, which resemble reactive type 2 pneumocytes, and interstitial cells, which often occur in sheets. The latter are thought to be primitive pulmonary epithelial cells, 1 3 but both are regarded as neoplastic cells of pulmonary epithelial cell origin. 4 8 It is generally accepted that these tumors are benign. Four patients with histologically benign pulmonary SH and lymph node metastases have been described previously. 3,4,7,9 Four additional cases with SH and lymph node metastases are reported herein. METHODS A search of the authors consultation files yielded 4 examples of SH with lymph node involvement. In each case, surgical resection specimens, including specimens from regional and peribronchial lymph nodes, were available. All authors reviewed the histologic sections of the pulmonary tumor and the Accepted for publication September 30, From the Department of Pathology, Tenri Hospital, Nara, Japan (Dr Miyagawa-Hayashino); the Department of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, Minn (Drs Tazelaar and Langel); and the Department of Laboratory Medicine and Pathology, Mayo Clinic, Scottsdale, Ariz (Dr Colby). Reprints: Henry D. Tazelaar, MD, Department of Laboratory Medicine and Pathology, Mayo Clinic, 200 First St SW, Rochester, MN ( tazelaar.henry@mayo.edu). lymph node metastases and determined the presence or absence of cytologic atypia, foci of increased cellularity, necrosis, mitotic activity, irregular tumor borders, and angiolymphatic invasion. For each case, follow-up information was obtained from the referring pathologist and the patient s personal physician. RESULTS Clinical Characteristics The Table shows the clinical characteristics of the 4 patients with SH and lymph node metastases (also shown are the clinical characteristics of the 4 previously described patients). The patients (3 female, 1 male) had a mean age of 39 years (range, years). Two patients presented with flulike symptoms (probably unrelated to the SH), and 2 patients were asymptomatic. In each case, chest radiography revealed a solitary mass lesion in the lung (left lower lobe in 2 patients, right middle lobe in 1, and right upper lobe in 1). All patients underwent lobectomy and peribronchial and regional lymph node dissection. In all patients, lymph node lesions were detected during surgery for the pulmonary tumor. Pulmonary tumors ranged from 1.5 to 4.7 cm in greatest dimension (mean, 3.1 cm). The regional lymph nodes examined ranged from 0.5 to 1.2 cm in greatest dimension; in several nodes, focal white areas beneath the capsule were grossly identifiable. No patient has had disease recurrence as seen on chest radiographs or evidence of additional metastases at a mean follow-up of 4.7 years (range, years). One pa- Arch Pathol Lab Med Vol 127, March 2003 Pulmonary Sclerosing Hemangioma Miyagawa-Hayashino et al 321
2 322 Arch Pathol Lab Med Vol 127, March 2003 Pulmonary Sclerosing Hemangioma Miyagawa-Hayashino et al
3 tient (patient 4), whose SH was initially diagnosed as adenocarcinoma, received chemotherapy after her lung operation. Histologic Analysis The pulmonary tumors displayed a mixture of sclerotic, solid, and papillary patterns. Two tumors also displayed a hemorrhagic pattern. All tumors had smooth, circumscribed borders and lacked necrosis, foci of increased cellularity, mitotic activity, or angiolymphatic invasion. Three tumors showed bland cytology throughout. The tumor from patient 3 had a focus of surface cells with moderate cytologic atypia characterized by nuclear enlargement, hyperchromatism, coarse chromatin, and the presence of eosinophilic nucleoli (Figure 1); however, because these features were very focal, they were not thought sufficient to warrant a histologic diagnosis of malignancy. In no case was there evidence of angiolymphatic invasion or direct extension into lymph nodes. Metastasis to 3 of 6 hilar lymph nodes occurred in 1 patient. Metastasis to 1 lymph node occurred in the other 3 patients. All metastases showed bland cytology. Perinodal soft tissue extension of tumor was identified in patient 2 (Figure 2). As compared with the primary tumors, the lymph node metastases displayed some variation in the proportions of tumor growth patterns (Table). Although a solid pattern was predominant in 1 patient s primary tumor, a solid pattern was present or predominant in the lymph node metastases in all 4 patients (Figure 3). COMMENT Many authors have speculated on the histogenesis of SH. 5,8,10 19 Now, however, it is generally accepted that SH differentiates from respiratory epithelium. 4,6,9 Both the cuboidal surface cells and the pale round cells are positive for thyroid transcription factor-1 and epithelial membrane antigen and are negative for neuroendocrine markers. The cuboidal surface cells also stain positively for pancytokeratin and surfactant proteins, which provides additional evidence of the epithelial nature of this tumor. 4,9 Although it has been debated whether both cell types are neoplastic, 1,2,5,7,8,10,13 16 Nihoetal 6 recently demonstrated that the surface cells and the round cells in 5 cases of SH were similarly clonal. The fact that the metastatic lesions in the lymph nodes of the patients described in this article consisted of papillary proliferations of round cells covered by surface cells also suggests that both cell types are neo- Figure 1. Patient 3. Sclerosing hemangioma. a, Lung tumor with cytologic atypia characterized by nucleomegaly and the presence of prominent nucleoli (hematoxylin-eosin, original magnification 200). b and c, Metastasis in hilar lymph node consisted of solid sheets of cells without atypia but with perinodal extension (hematoxylin-eosin, original magnifications 50 [b], 100 [c]). Figure 2. Patient 2. Sclerosing hemangioma. a, Lung tumor was composed of sclerotic, solid, and papillary patterns (hematoxylin-eosin, original magnification 25). b and c, Lymph node metastasis with similar features (hematoxylin-eosin, original magnifications 25 [b], 200 [c]). Figure 3. Patient 4. Sclerosing hemangioma. a, Pulmonary tumor had sclerotic, papillary, and solid patterns (hematoxylin-eosin, original magnification 25). Metastatic focus in hilar lymph node consisted of both sclerotic (b) and solid (c) patterns (hematoxylin-eosin, original magnifications 50 [b], 200 [c]). Arch Pathol Lab Med Vol 127, March 2003 Pulmonary Sclerosing Hemangioma Miyagawa-Hayashino et al 323
4 Clinical Characteristics of 8 Patients With Metastasizing Pulmonary Sclerosing Hemangiomas* Patient No. Source, y Age, y/sex Symptoms Site Tumor Size, cm Devouassoux-Shisheboran et al, Tanaka et al, Chan and Chan, Spencer and Nambu, /F 45/F 45/M 56/F 18/F 22/M 48/M / Flulike Flulike... * indicates not available; RML, right middle lobe; RUL, right upper lobe;, left lower lobe; RLL, right lower lobe; H, hemorrhagic; SC, sclerotic pattern; P, papillary pattern; and, solid pattern. Greatest dimension. RML RUL RLL RLL plastic (or at least capable of metastasis). Finally, the neoplastic nature of SH was recognized by the World Health Organization in its 1999 histologic classification of lung tumors 20 ; in the 1981 World Health Organization classification of lung tumors, SH was classified as a tumorlike lesion. 21 Before the publication of this article, descriptions of 4 patients with metastasizing SH had been published (case data included in Table). Among the patients for whom the information is known, there were 2 men and 1 woman; their mean age was 29.3 years (range, years). Lobectomy showed that the tumor location was the right lower lobe in 2 patients and the left lower lobe in 1 patient. Tumor size ranged from 3.5 to 8 cm in diameter. The tumor measuring 8 cm in diameter was in a 48-year-old patient and had first been discovered on a chest radiograph 31 years before surgery. 4 In1of the 4 previously described patients, metastatic deposits were identified in 2 of 5 peribronchial lymph nodes. 9 In another patient, small metastatic foci were identified in 2 regional lymph nodes. 4 In the remaining 2 patients, small metastatic foci were identified in 1 hilar lymph node each. 3,7 In 3 patients, the lymph node metastases had a solid pattern of round cells 3,4,9 ; in 1 patient, the lymph node metastasis had sheets of round cells with focal papillary areas similar to those of the pulmonary tumor. 7 One of the 4 patients was alive with no evidence of residual, recurrent, or metastatic disease after 27 months follow-up. No follow-up information was available for the other 3 patients. It is difficult to estimate the incidence of lymph node metastases from SHs. In our experience, lymph node sampling in cases of SH is limited because it is a benign tumor. The 4 patients we describe represent an extremely biased sample. theless, during the period that these cases were collected ( ), we evaluated approximately 100 to 200 cases of SH. Therefore, a rough estimate is that 2% to 4% metastasize. Although the number of reported cases with pulmonary SH and lymph node metastases is small, a solid pattern appears to be the growth pattern most commonly identified in lymph nodes. If the nature of the primary tumor is not known, diagnostic difficulty and erroneous therapy could result, as happened with 1 of our patients. The differential diagnosis would include metastatic carcinoma (pulmonary or extrapulmonary, eg, of the breast), other metastasis (eg, melanoma), metastatic mesothelioma, and benign reactive mesothelial cells. Immunohistochemical studies in such cases could lead to further confusion because thyroid transcription factor-1 reactivity may suggest a carcinoma of pulmonary origin. 4,9 Particularly in nonsmokers or young patients, examination of the pulmonary lesion may be essential for proper classification of a metastatic lesion. The primary tumor from 1 patient in the current series had a moderate degree of cytologic atypia focally. In our opinion, this feature was insufficient to warrant a diagnosis of malignancy. Criteria for malignancy in SHs have not been established. We suggest that, at a minimum, such tumors have more widespread cytologic atypia, some degree of mitotic activity, and possibly necrosis. The significance of regional lymph node involvement in patients with metastasizing SH is not clear. The tumors in both the lungs and the lymph nodes of the patients described here were histologically benign. Also, the histologic appearance of primary tumors in patients with no metastasis is indistinguishable from that of primary tumors in patients with metastasis. In the 5 patients for whom follow-up information was available, the prognosis did not appear to be affected by the presence of regional lymph node metastases. In the current series, all 4 patients were alive without evidence of disease at a mean follow-up of 4.7 years after surgery. Although 1 patient had focal cytologic atypia in the primary pulmonary tumor, he was alive and well without recurrence 2.5 years after surgery. Another patient also had perinodal extension, but is alive without recurrence after 4 years of follow-up. Although they may result in morbidity and even mortality, similar metastases from uterine leiomyomas, 22,23 mixed tumors of salivary gland, 24,25 giant cell tumors of the bone, 26 chondroblastomas, 27 thymomas, 28 meningiomas, 29 and nevus cells 30 have generally not been considered malignant. This study suggests that metastasizing SH does not portend a poor prognosis; therefore, we still consider SHs to be benign tumors. However, longer follow-up analysis of a larger group of patients is needed. The authors thank the following physicians, who provided information and material on their patients: Howard B. Goldstein, MD; Kenneth Steinglass, MD; Anna Mathew, MD; Mossimo Brisigotti, MD; Larry W. Cartmell, MD; Kathleen Sunshine, MD; and William Travis, MD. 324 Arch Pathol Lab Med Vol 127, March 2003 Pulmonary Sclerosing Hemangioma Miyagawa-Hayashino et al
5 No., Location, and Size (cm ) of Lymph Nodes With Metastases 1 regional, hilar, peribronchial, interlobar, pulmonary artery, peribronchial, 1 hilar, regional, 1 hilar, Follow-up, y Extended Lung H SC P SC P H SC P H P SC H, SC, P, Growth Pattern Lymph Node, P H SC P H SC, P References 1. Liebow AA, Hubbell DS. Sclerosing hemangioma (histiocytoma, xanthoma) of the lung. Cancer. 1956;9: Katzenstein AL, Gmelich JT, Carrington CB. Sclerosing hemangioma of the lung: a clinicopathologic study of 51 cases. Am J Surg Pathol. 1980;4: Spencer H, Nambu S. Sclerosing haemangiomas of the lung. Histopathology. 1986;10: Chan AC, Chan JK. Pulmonary sclerosing hemangioma consistently expresses thyroid transcription factor-1 (TTF-1): a new clue to its histogenesis. Am J Surg Pathol. 2000;24: Nagata N, Dairaku M, Sueishi K, Tanaka K. Sclerosing hemangioma of the lung: an epithelial tumor composed of immunohistochemically heterogenous cells. 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