Immunohistochemical Study of Some Rare Vascular Tumors
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1 Journal of the Egyptian Nat. Cancer Inst., Vol. 16, No. 2, June: , 2004 MONA EL-SAYED, M.D. and MOHAMMAD RAMADAN, PH.D. The Department of Pathology, Faculty of Medicine, Zagazig University. ABSTRACT Purpose: Kaposiform-hemangioendothelioma (KHE) is a rare vascular tumor, developing predominantly in infants and children. Despite its benign histology, this tumor frequently behaves aggressively, causing significant morbidity and mortality. The striking resemblance of its spindle cell proliferation to that seen in Kaposi sarcoma (KS) led to the designation of KHE for this rare lesion. This work examined the histopathologic features of KHE and KS and assessed the value of some vascular immunohistochemical markers such as CD34, CD31 and factor VIII associated antigen in routine diagnosis and differential diagnosis of these vascular tumors. Material and Methods: Three cases of KHE and twenty cases of KS were included in this study. All specimens are fixed in formalin, embedded in paraffin wax and stained with hematoxylin & eosin and reticulin stains. The antibodies to CD34, CD31 and factor VIII associated antigen were applied using the streptavidin biotin technique. Results: Immunohistochemically, all elements within the lesions were labeled with anti-cd34 antibody. Labeling of spindle cells was less consistent with anti-cd31, while the antibody to factor VIII associated antigen labeled only the well-formed capillaries. Conclusion: KHE and KS are tumors of endothelial cell origin. Immuno-staining for CD34, and to a lesser extent, CD31, are more reliable for labeling KHE and KS than the traditional endothelial cell marker, factor VIII associated antigen. These markers can be used for diagnosis in routinely processed tissue of KS and KHE. Key Words: Kaposiform hemangioendothelioma (KHE) - Kaposi sarcoma (KS) - Immunohistochemistry - CD34 - CD31 - F. VIII associated antigen. INTRODUCTION Kaposiform-hemangioendothelioma (KHE) is a rare locally aggressive vascular tumor of the skin, deep soft tissue, and bone found mostly in children, and is characterized by infiltrating nodules, sheets of spindle cells, and an unmistakable resemblance to Kaposi sarcoma [1]. Motiz Kaposi originally described Kaposi sarcoma (KS) in 1872 as an idiopathic multiple pigmented sarcoma of the skin. Four distinct variants of KS are recognized: The chronic, also called classic or European KS; the lymphadenopathic or African type; the iatrogenic type; and AIDS-associated KS [2-6]. Immunohistochemistry has been used extensively in the study of vascular tumors: first, to confirm their endothelial cell origin, and second, to aid diagnosis in routine histopathology [7]. Monoclonal antibodies directed against CD34 and CD31 have prompted interest in the study of vascular tumors. While they are not endothelial cell specific, they are widely expressed in vascular endothelium, particularly in pathological conditions [7]. CD34 is a cell surface protein encoded by the CD34 gene on chromosome 1q32. It is expressed by human hematopoietic cells of both the myeloid and lymphoid series, as well as endothelial cells. It may have a role in regulating early events in blood cell differentiation, or it may function as an adhesion molecule in both endothelial cells and hematopoietic progenitor cells [8]. CD31 is a 130-KD transmembrane glycoprotein. It is expressed on platelets, monocytes, granulocytes, B-cells, a subset of leukocytes and endothelial cells [9]. Factor VIII associated antigen is a large multimeric protein that is synthesized by endothelial cells. It can also be found in platelets and megakaryocytes. It has become a reasonably good marker of endothelial differentiation [9]. 123
2 124 In addition to studying the clinico-pathologic features of KHE and KS, our study also assessed the value of some immunohistochemical markers as CD34, CD31 and F VIII associated antigen in routine diagnosis and differential diagnosis of these vascular tumors. MATERIAL AND METHODS Three cases of KHE and twenty cases of KS were retrieved from the consultation files of one of the authors and the archives of the Department of Pathology, Faculty of Medicine, Zagazig University. For conventional light microscopy, the tissue is fixed in 10% formalin, embedded in paraffin, cut and stained with hematoxylin & eosin and with reticulin stains. For immunohistochemical studies, immunostaining is performed according to avidin-biotinperoxidase complex technique. Five microns paraffin sections are mounted on positively charged slides and then deparaffinised and dehydrated. Endogenous peroxidase activity is blocked using a 3% hydrogen peroxide in methanol for 10 minutes. Then they are treated with microwave heating for 20 minutes in citrate buffer (2.1 g/100ml, ph 6) for antigen retrieval before rinsing briefly in tap water. The sections are incubated with the following antibodies: CD34 (QBEND/10 Oxoid, Basingstoke, UK) diluted 1 in 50, CD31 (JC 70/A Dako) diluted 1 in 10 and Von Willebrand factor ( Dako, High Wycomb, UK) diluted 1 in 50. After overnight incubation at 4ºC and washing in PBS (ph 7.4), the tissues are incubated with biotin-conjugated secondary antibody and then with the streptavidin-biotin-system (Histostain) for 30 minutes at room temperature. The reactions are visualized by diaminobenzidine tetrahydrochloride. The sections are counterstained using hematoxylin stain, then cleared and mounted. QBEND/ 10 do not require protease digestion. Negative controls consisted of omission of the primary antibodies. The mitotic rate is expressed as the average mitotic count present in 50 high-power fields [7,10]. RESULTS Clinicopathologic Features: Kaposiformhemangioendothelioma (KHE): In Case 1, a young adult male (22 years old) demonstrated a painless enlargement of the cervical lymph nodes. Case 2 was a 35-year old woman with a painless subcutaneous nodule on the chest wall. Case 3 was a seven-month-old infant who demonstrated a subcutaneous nodule in the left arm. Histopathologically, all cases showed a well-circumscribed tumor with a lobular architecture. The individual tumor nodules were composed of cellular fascicles of densely-packed spindle-shaped tumor cells separated by fibrous bands (Fig. 1). The spindled tumor cells contained scarce and ill-defined eosinophilic cytoplasm and fusiform, and elongated nuclei with finely distributed chromatin without conspicuous nucleoli. These spindle cells were associated with small endothelial lined vascular spaces forming slit-like and sievelike spaces (Fig. 2), similar to that seen in KS. In Case 1, in spindle cell lobules, scattered nodules consisted of plumper, more epitheloid tumor cells (Fig. 3). Also, scattered fibrin thrombi and ectatic blood vessles were found in the periphery of the tumor lobules. Reticulin stain confirmed the vasoformative architecture even in spindled area (Fig. 4). Areas of hemorrhage and hemosidrin deposits were found. No cellular atypia was seen. Mitotic activity ranged from one to three mitoses per 50 HPFs. Necrosis was absent. Kaposi Sarcoma (KS): Traditionally, KS are divided into patch, plaque or nodular lesions. In our study, all the biopsy specimens were nodular lesions. The age of the patients ranged from 53 to 67 years. The male to female ratio was 9:1. Sixteen specimens were skin lesions and the remaining four cases were soft tissue lesions. Histopathologically, nodular KS was formed of spindle cells arranged in interwoven fascicles with erythrocytes scattered in the interstices. In some areas, numerous small capillaries were cut in cross-sections to give the appearance of a sieve (Fig. 5). Cellular atypia was seen in fourteen cases. Mitotic activity ranged from five mitoses per 50HPFs in twelve cases to eight mitoses per 50HPFs in the remaining eight cases. Immunohistochemistry: Kaposiform hemangioendothelioma KHE: CD34 and CD31 antibodies stained the endothelial cells lining small slit-like vascular spaces and the well-formed capillaries. The spindle shaped tumor cells were focally positive in all three cases (Fig. 5).
3 Mona El-Sayed & Mohammad Ramadan 125 The antibody to factor VIII associated antigen stained only the well-formed capillaries but did not stain the endothelial cells lining small slit-like vascular spaces and spindle-shaped tumor cells (Fig. 6). Kaposi sarcoma: CD34 antibody stained all elements within the lesions of KS. The sievelike areas were particularly well visualized. CD34 antibody also labeled focally the spindle cells with weak staining in only three cases (Fig. 7). With CD31 antibody, the sieve-like areas and spindle cells were weakly and focally stained in fourteen cases, and were negative in the remaining six cases (Fig. 8). The antibody to factor VIII associated antigen stained only the well-formed capillaries but did not stain the sieve-like areas or the spindle cells. CD31 labeling was cytoplasmic, granular, and less easy to define than CD34. Also, factor VIII associated antigen was localized throughout the cytoplasm of endothelial cells. Fig. (1): A case of L.N. Kaposiform hemangioendothelioma showing spindle cell tumor lobules separated by fibrous bands (Hx & E X 40). Fig. (2): A case of L.N. Kaposiform hemangioendothelioma showing spindle-shaped tumor cells separated by slit-like vascular spaces mixed with well-formed capillaries (Hx & E X 200). Fig. (3): A case of L.N. kaposiform hemangioendothelioma showing spindle cell lobules with scattered nodules composed of plumper more epitheloid tumor cells (Hx & E X 400). Fig. (4): A case of skin kaposiform hemangioendothelioma showing the vasoformative nature even in spindle cell areas (Silver Reticulin X 100).
4 126 Fig. (5): A case of L.N. kaposiform hemangioendothelioma showing positive staining of the well-formed capillaries and the sieve-like vascular spaces for CD34 (Immunoperoxidase X 200). Fig. (6): A case of L.N. kaposiform hemangioendothelioma showing positive staining of the well-formed capillaries only for factor VIII associated antigen (Immunoperoxidase X 200). Fig. (7): A case of nodular Kaposi sarcoma showing positive staining of all vascular elements and focal staining of spindle tumor cells for CD34 (Immunoperoxidase X 100). Fig. (8): A case of nodular Kaposi sarcoma showing positive staining of the well-formed capillaries, the sieve-like area and spindle cells for CD31 (Immunoperoxidase X100). DISCUSSION Vascular tumors occurring in adults show a broad spectrum of histologic features and clinical behavior. Whereas the diagnosis and prognosis of ordinary capillary hemangiomas and classic cutaneous angiosarcoma are usually straightforward, the group of vascular lesions characterized by unusual morphologic features and unpredictable prognosis has increased during the last few years, and this has led to the delineation of a number of previously unrecognized entities and variants. Such accurate recognition facilitates more reliable prognostication and provision of appropriate therapy [10]. Despite its benign histology, KHE displays borderline behavior in that it is a locally invasive and frequently aggressive vascular neoplasm [11]. More than 60 patients with such a tumor have been reported so far, and while many have died as a result of extensive disease and severe coagulopathy, the long-term biologic behavior of this tumor remains undetermined [1]. In our study, we examined three cases of KHE, one affecting the cervical lymph nodes of a young adult male, and the second and the third cases affecting the skin of the chest wall and the arm of an adult female and a seven-month-old infant, respectively. KHE has been described as occurring almost exclusively in infants and young children with most cases occurring in the first decade of life, especially during the first two years [12]. However, many cases have been reported in adults in the last few years [1,10,11, 13,14]. KHE has been reported in the skin, deep
5 Mona El-Sayed & Mohammad Ramadan 127 soft tissues, bone and thymus [1,10,15], but to our knowledge, this is the first report of KHE in a cervical lymph node. The histopathologic features of our cases were similar to previously reported KHE cases. However, none of our studied cases showed lymphangiomatous changes (variable dilated thin-walled lymphatic channels, ramifying irregularly and lined by bland endothelial cells) or amianthoid-like fibrosis. One of our studied KHE cases was identified in a lymph node of a young adult in which the diagnosis of nodular KS was suspected instantly and, at least initially, was harder to exclude. However, the lymphadenopathic forms of KS that occur mostly in young children are generalized, while those that arise in middle-aged adults favor the lower limbs [10]. Although KS and KHE share histological features in the form of slit-like and sieve-like vascular spaces between densely packed spindled tumor cells, the lobular growth pattern, the presence of nodules composed of more rounded endothelial cells, the presence of fibrin microthrombi and the lack of chronic inflammatory infiltrate are helpful morphologic clues for distinguishing these entities [16]. In addition, transcripts similar to human papilloma virus 16 have been described in KS, occurring both in the setting and outside the setting of AIDS. In two studied cases of KHE, these transcripts were not identified as providing additional evidence for the separate nature of the two diseases [17]. Immunohistochemical study of CD34 expression in KHE and KS showed that CD34 labeled all elements within these lesions, the well-formed capillaries, the small slit-like vascular spaces and the sieve-like areas. The spindle cells were also focally labeled by anti-cd34 but with weak staining of three cases of KS. Russel Jones, et al. [7], Mentzel, et al. [10], Wilken, et al. [15] and Flope, et al. reported similar observations [18]. In addition, Ramani, et al. [19], in a study of 40 cases, reported positive CD34 labeling of lymphangiomatoid elements with variable staining of spindle cell elements. Using antibodies to CD31 in KHE, anti- CD31 labeled the endothelial cells lining small slit-like vascular spaces and the walls of wellformed capillaries. The spindle-shaped tumor cells were only weakly focally positive. On the other hand, in KS, anti-cd31 labeled the sievelike areas and spindle cells weakly in 14 of 20 cases (70%) and was negative in the remaining six cases (30%). Consistent with our results, Russel Jones, et al. [7] found that CD31 labeling of spindle cells within the nodular lesions of KS was weak and patchy in five of eleven cases (45.4%) and negative in the remaining six cases. In addition, Mentzel, et al. [10] and Flope, et al. [18] observed CD31 expression in all cases of KHE. Also, Flope, et al. [18] found CD31 expression in 12 of 13 cases (92%) of KS. Immunohistochemical study of factor VIII associated antigen expression in KHE and KS showed that factor VIII antibody stained only the well-formed capillaries, but did not stain the endothelial cells lining small slit-like, sievelike vascular spaces and spindle shaped tumor cells in both KHE and KS. Russel Jones, et al. [7], Mentzel, et al. [10] and Wilken, et al. reported similar observations [15]. However, Andrew, et al. [18] reported that factor VIII related antigen was expressed in four of five (80%) of KHE and ten of thirteen (77%) of KS cases. This discrepancy in the results may be due to technical factors and the lack of standard immunohistochemical assays, including different clones of the antibodies [7]. CD34 is said to be present on normal venular, but not lymphatic, endothelium and has been reported as negative in lymphangiomas [8]. If so, this would strongly indicate a vascular origin for the spindle cell elements in KS and KHE. However, Ramani, et al. [19] have reported that five of eight cases of lymphangioma were focally positive for CD34. Also, Russel Jones, et al. [7] found positive labeling of lymphangiomatoid elements with negative labeling of adjacent normal lymphatics and suggested that adhesion molecules are expressed more strongly in pathological states. Similar considerations apply to anti-cd31, which is also thought to label vascular rather than lymphatic endothelium and is absent in lymphangiomas and lymphoepithelial cysts [20]. However, Nickoloff [21] and Russel Jones, et al. [7] found CD31 labeling on both vascular and lymphatic epithelium. It seems, therefore, that CD34 and CD31 do not help in distinguishing between cells derived from lymphatic or vascular endothelium.
6 128 The diagnosis of KHE is often made only on histopathological and immunohistochemical grounds. Differential diagnosis of KHE in adults, rather than KS, includes spindle cell hemangioendothelioma, tufted angioma, and angiosarcoma [10,22]. In tufted angioma, the individual nodules have the architecture of a lobular capillary hemangioma, composed of endothelial cells and pericytes, but are much less spindled and lack fibrin microthrombi [10]. However, Chu, et al. [23] reported a dynamic transformation between both tumors within a single patient, which suggests that they are two variants of the same vascular tumor. Sometimes, spindle cell differentiation is prominent in angiosarcoma, but usually markedly atypical cells are present [24]. Spindle cell hemangioendothelioma is seen mainly in the distal extremities, manifests often as multiple nodules frequently associated with adjacent hamartomatous vascular changes, lacks a lobular architecture and in addition to spindle cell areas, contains cavernous vascular spaces often with papillae and vacuolated endothelial cells [22]. Conclusion: KHE and KS are tumors of endothelial cell origin. Although KHE and KS share hitopathologic features in the form of slit-like and sievelike vascular spaces between densely-packed spindled tumor cells, the lobular growth pattern, the presence of nodules composed of more rounded endothelial cells and the lack of chronic inflammatory infiltrate in KHE are helpful morphologic clues for distinguishing these entities. CD34, and to a lesser extent CD31, antibodies are more reliable at labeling KS and KHE than the traditional endothelial marker factor VIII related antigen and can be used on routinely processed tissue for diagnosis of these vascular tumors, but not for differentiating between them. More cases of KHE with long follow-up information are necessary to decide whether KHE shows age-related prognostic differences. REFERENCES 1- Mac-Moune FL, To KF, Choi PC, Leung PC, Kumta SM, Yueu F, et al. Kaposiform hemagioendothelioma: Five patients with cutaneous lesion and long followup. Mod Pathol. 2001, 14 (11): Requena L, Sangueza OP. Cutaneous vascular proliferations. Part 3. Malignant neoplasm, other cutaneous neoplasms with significant vascular component and disorders erroneously considered as vascular neoplasms. J Am Acad Dermatol. 1998, 38 (2): Wabinga HR, Parkin DM, Wabwire-Mangen F, Mugerwa JW. Cancer in Kampala, Uganda in : changes in incidence in the area of AIDS. Int J Cancer. 1993, 54: Eberhard OK, Kliem V, Brunkhorst R. Five cases of Kaposi sarcoma in kidney graft recipient: Possible influence of the immunosuppressive therapy. Transplantation J. 1999, 1567 (1): Tappero JW, Canant MA, Wolfe SS, Berger TG: Kaposi sarcoma: Epidemiology, pathogenesis, histology, clinical spectrum, staging criteria and therapy. J Am Acad Dermatol. 1993, 28: Beral V, Peterman TA, Berkelman RL, Jaffe HW. Kaposi sarcoma among persons with AIDS: A sexually transmitted infection. Lancet. 1990, 335: Russel Jones R, Orchard G, Zelger B, Wilson Jones E. Immunostaining for CD31 and CD34 in Kaposi sarcoma. J Clin Pathol. 1995, 48: Sankey E, More L, Dhillon. QBEND/10: a new immunostain for the routine diagnosis of Kaposi sarcoma. J Pathol. 1990, 161: Louis S. Immunohistochemistry of soft tissue tumors. In: Enzenger SM, Weiss W, editors. Soft tissue tumors. 3 rd edition. Boston: Mosby. 1995, Mentzel T, Mazzoleni G, Deltos A, Fletcher CDM. Kaposiform hemangioendothelioma in adults: Clinicopathologic and immunohistochemical analysis of three cases. Am J Clin Pathol. 1997, 108 (4): Cooper JG, Edwards SL, Holmes JD. Kaposiform hemangioendothelioma, case report and review of the literature. Br J Plast Surg. 2002, 55 (2): Calonje E, Fletcher CDM. Tumors of blood vessels. In: Fletcher CDM, editor. Diagnostic histopathology of tumors. 2 nd edition. 2000, Zamecnik M, Mikleova Z, Michal M. Kaposiform hemangioendothelioma in adult: Report of a case with amianthoid-like fibrosis and angiectases. Cesk Pathol. 2000, 36 (4): Zamecnik M, Koys F, Mikleova Z, Michal M. Additional case of kaposiform hemangioendothelioma in adult. Cesk Pathol. 2001, 37 (3): Wilken JJ, Meier FA, Kornstein MJ. Kaposiform hemangioendothelioma of the thymus. Arch. Pathol. Lab Med. 2000, 124 (10): Chor PJ, Santa Cruz DJ. Kaposi sarcoma: a clinicopathologic review and differential diagnosis. J Cutan Pathol. 1992, 19: Zukerberg LR, Nickoloff BJ, Weiss SW. Kaposiform hemangioendothelioma of infancy and childhood: An
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Kaposi sarcoma. Immunostaining for CD31 and CD34 in. (QBEND/10 and anti-hpca-1) more extensively. Only limited studies of Kaposi sarcoma
Clin Pathol 1995;48:1011-1016 1011 St John's nstitute of Dermatology, St Thomas's Hospital, London R Russell Jones G Orchard E Wilson Jones Department of Dermatology, University of nnsbruck, Austria B
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