Case Report A case of renal angiomyolipoma with intracardiac extension and asymptomatic pulmonary embolism
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1 Int J Clin Exp Pathol 2013;6(6): /ISSN: /IJCEP Case Report A case of renal angiomyolipoma with intracardiac extension and asymptomatic pulmonary embolism Xiaoman Li 1, Qingchang Li 2, Yuan Miao 2, Hongtao Xu 2, Yang Liu 2, Xueshan Qiu 2, En-Hua Wang 2 1 Key Laboratory of Medical Cell Biology, Ministry of Education, China Medical University, Shenyang, , China; 2 Department of Pathology, the First Affiliated Hospital and College of Basic Medical Sciences, China Medical University, Shenyang, , China Received March 24, 2013; Accepted March 29, 2013; Epub May 15, 2013; Published June 1, 2013 Abstract: Angiomyolipoma (AML) is the most common benign tumor of the kidney, which is composed of a mixture of three tissue components: blood vessels, smooth muscle and adipose cells. Occasionally, AML may extend into the renal vein or the vena cava, but so far at least, intracardiac extension was rarely reported. We herein present one case of renal AML with intracardiac extension and pulmonary embolism simultaneously in a 52-year-old Chinese female patient. Contrast-enhanced computed tomography revealed a well-demarcated heterogeneous mass in the right kidney which extended into the right atrium through the right renal vein and inferior vena cava and resulted in embolization in the right pulmonary artery. The renal mass together with the thrombus was resected. The renal mass and thrombus in vena cava and right atrium shared the similar histological features: mature adipose tissue, smooth muscle and thick-walled vessels. The thrombus in the right pulmonary artery was mainly composed of mature adipose tissue. These histological features and the result of positive immunostaining for HMB-45, Melan-A, and smooth muscle actin supported the diagnosis of AML. The component of epithelioid cells was less than 5% and mitosis was rarely seen. Intracardiac extension is often observed in the malignant tumor and only seldom seen in benign tumors. Our case reminds the rare possibility of intracardiac extension in renal AML, which may potentially result in fatal complications if not appropriately managed. Keywords: Angiomyolipoma, perivascular epithelioid cell, intracardiac extension, pulmonary embolism, kidney Introduction Angiomyolipoma (AML) is a benign mesenchymal tumor composed of a variable proportion of adipose tissue, spindle and epithelioid smooth muscle cells and abnormal thick-walled blood vessels [1]. AMLs occur both sporadically and in association with tuberous sclerosis. The kidney is the most common site of involvement. Although the term AML was first used by Morgan et al. in 1951 [2], the renal lesion that histologically corresponds to a renal AML was first described by Grawitz in 1900 [3]. Initially, AML was thought to be a hamartoma, an abnormal proliferation of tissues that frequently arose from the kidney. Recently, AML is believed to belong to a family of lesions characterized by proliferation of perivascular epithelioid cells (PEC). Molecular studies have demonstrated its clonality, and moreover both immunohistochemical and ultrastructural studies support the histogenesis from a single cell type [1]. Histologically, most AMLs are composed of three classic components described above and therefore denominated as classic or triphasic AML, while some AMLs were mainly composed of the epithelioid cells and designated as epithelioid AML (EAML). EAML, as a variant of AML, is a potentially malignant mesenchymal neoplasm. The smooth muscle cells in AML appear to emanate from blood vessel walls in a radial fashion and demonstrate an expansile growth thereafter. The smooth muscle cells are frequently spindled without significant atypia. Rarely, striking degrees of nuclear atypia may be seen in these cells, raising the possibility of malignancy. Immunohistochemically, AMLs are characterized by a coexpression of melanocytic markers (HMB45 and Mart1/Melan-A) and smooth muscle actin (SMA). Renal AML typically do not extend beyond the kidney. However, rarely the renal AML may show intracardiac extension [4-9] or pulmonary
2 A 52-year-old woman was admitted to the First Affiliated Hospital of China Medical University in June of 2012 for right flank pain. Physical examination showed a solid mass in the right flank with a slight tenderness. Chemical studies showed no abnormality. Contrast-enhanced Computed Tomography revealed a well-demarcated heterogeneous mass ( cm) in the lower pole of the right kidney. The renal pelvis and calices were compressed and distorted. A hypodense cystic change ( cm) was found in the right anterior lobe of the liver. Lowdensity lesion in the right atrium and fatty density in inferior vena cava were also observed. Echocardiography also revealed a mass in the right atrium with the filling defects (Figure 1A). The spleen, pancreas, and left kidney were without any focal lesions. Radical nephrectomy and cardiothoracic surgery were performed simultaneously. A thrombus in right pulmonary artery was found and resected during the surgery. The patient was alive with no evidence of disease at 6 months of follow-up. Gross features Gross examination revealed a cm irregular red and yellowish mass in the lower pole of right kidney (Figure 1B). The renal mass had a medium texture and the cut surface is colorful (Figure 1C). A tumor thrombus, measuring 17 cm long, extending from renal vein through the vena cava into the right atrium was also found. The thrombus in the vena cava and right atrium was floating and waterweed-like. Microscopic features Figure 1. Echocardiography of the right atrial mass and morphology of the right renal mass. A: Echocardiography revealed a mass in the right atrium. B: A mass was found in the lower pole of the right kidney. C: Gross examination showed a cm irregular mass in the right kidney with a tumor thrombus, 17 cm long, extending into the right atrium. The cut surface is red and yellowish. embolism [10-12]. Here we reported the first case of AML with both intracardiac extension and pulmonary embolism. Case presentation Clinical history The neoplasm showed an expanding growth pattern with subcapsular hemorrhage (Figure 2A), and was demarcated from the surrounding kidney tissues with a slightly irregular border (Figure 2B). The tumor was composed of three components: mature adipocytes, thick-walled blood vessels and smooth muscle cells (Figure 2C). The smooth muscle cells appeared to emanate from blood vessel walls in a radial fashion, and assumed an expansile growth pattern in a fascicular fashion (Figure 2C and 2D). The cells close to the vessels were rounded epithelioid cells with clear cytoplasm and small nucleoli whereas the cells far away from the vessels were mainly spindled cells. In the central area of the neoplasm, hemorrhage (Figure 2E) and necrosis (Figure 2F) were observed. Epithelioid cells accounted for less than 5% of tumor cells and showed moderate atypia. Rare mitotic figures were identified in the epithelioid tumor cells (Figure 2G). No nuclear pleomorphism and mitotic figures were seen in spindled tumor 1181 Int J Clin Exp Pathol 2013;6(6):
3 Figure 2. Histological features. A, B: The neoplasm showed an expanding growth pattern with subcapsular hemorrhage, and was demarcated from the surrounding kidney tissues with a slightly irregular border. C: The tumor was composed of three components: mature adipocytes, thick-walled blood vessels and smooth muscle cells. D: The smooth muscle cells appeared to emanate from blood vessel walls in a radial fashion, and assumed an expansile growth pattern in a fascicular fashion. E, F: In the central area of the neoplasm, hemorrhage and necrosis were observed. G: The epithelioid cells with moderate atypia were focally observed and accounted for less than 5% of the whole neoplasm. H, I: The tumor in the right atrium shared the similar histological features with the tumor in kidney, while the pulmonary thrombus was mainly composed of mature adipocytes. cells. The tumor in the right atrium shared the similar histological features with the tumor in the kidney (Figure 2H), while the pulmonary thrombus was mainly composed of mature adipocytes (Figure 2I). Immunohistochemistry The immunohistochemical study showed that the smooth muscle cells were negative for AE1/ AE3 (Figure 3A), strongly and diffusely positive for vimentin (Figure 3B), HMB-45 (Figure 3C), Melan-A (Figure 3D), SMA (Figure 3E), and focally positive for CD68 (Figure 3F). The tumor cells were also negative for p53 and Ki67 index was less than 5% (Figure 3G and 3H). The pulmonary thrombus was negative for HMB-45 and Melan-A. Discussion Intracardiac extension of infradiaphragmatic tumors is an uncommon phenomenon. The tumors, either benign or malignant, that can extend into the intrathoracic vena cava (IVC) and the heart include uterine leiomyomatosis, renal AML, renal cell carcinoma (RCC), Wilms tumor, renal pelvis transitional cell carcinoma, renal or retroperitoneal sarcomas, hepatic tumors, adrenal tumors, and lymphoma [13, 14]. Among these tumors, RCC is by far the most common one. There were several literature reports describing involvement of renal AML, but renal AML with intracardiac extension is rare. To our knowledge, there were only seven reported such cases [4-9]. Renal AML may also rarely show pulmonary embolism [10-12]. In 1182 Int J Clin Exp Pathol 2013;6(6):
4 Angiomyolipoma with intracardiac extension Figure 3. Immunohistochemical staining. A: The tumor cells showed negative staining for AE1/AE3. B-E: The tumor cells including the epithelioid cells showed strong diffuse positive staining for vimentin, HMB-45, Melan-A and SMA, respectively. F: Scattered tumor cells were positive for CD68. G: The tumor cells showed negative staining for p53. H: Ki67 index was less than 5%. our study we described the first case of renal AML demonstrated both cavoatrial extension and asymptomatic pulmonary embolism simultaneously. Renal AML should be distinguished with other tumors such as RCC, Wilms tumor, renal pelvis transitional cell carcinoma and renal sarcoma because cavoatrial extension may be occasionally seen in these tumors. Histologically, renal AML typically shows a triphasic pattern and should be easily distinguished from other tumors. However, in some particular cases, RCC may occasionally have an angiomyolipoma-like pattern which makes it nearly impossible to be distinguished with AML just based on morphologic grounds [15]. In this situation, immunohistochemical staining is helpful. In contrast to AML, RCC is usually negative for SMA, HMB45 and Melan-A. AML predominantly composed of smooth muscle cells should be 1183 distinguished with Wilms tumor because the latter may exhibit locally skeletal or smooth muscle differentiation and other stromal differentiation including adipose tissues. A variety of stromal patterns of Wilms tumor may occur and may cause diagnostic difficulties when blastemal and epithelial differentiation are scant [1]. In such cases, extensive sampling should be performed to identify blastemal and epithelial components. In addition, HMB45 and Melan-A will be helpful to make the diagnosis. The renal pelvic transitional cell carcinoma (sarcomatoid variant) may be confused with AML because of the spindled morphology (with the presence or absence of heterologous elements). Immunohistochemical staining will also be helpful to these cases. Epithelial elements react with cytokeratin antibodies, whereas stromal elements react with vimentin antibodies or specific markers corresponding to the mesenchymal differentiation. Int J Clin Exp Pathol 2013;6(6):
5 Table 1. Comparison of Brimo Model and Nese Model to predict the malignancy of EAML Brimo Model Nese Model 1. 70% atypical epithelioid cells 1. TSC and/or concurrent AML 2. 2 mitotic figures per 10 hpf 2. Tumor size (>7 cm) 3. Atypical mitotic figures 3. With Carcinoma-like Growth 4. Necrosis 4. Extrarenal extension and/or involvement of renal vein 5. Necrosis Three or more of the above features predict increased risk of clinically malignant behavior. Intermediate-risk group (2-3 of the above features) Low-risk group (0-1 of the above features ) High-risk group (4-5 of the above features) Some AMLs may be composed almost entirely of thick-walled blood vessels, smooth muscle cells or mature adipose tissues which resemble vascular malformation, leiomyomas or liposarcoma, respectively. However, the latter lesions or tumors do not express HMB45 and Melan-A. The vast majority of renal AMLs are benign except EAMLs. EAML is a potentially malignant neoplasm. As described in World Health Organization Blue Book, the smooth muscle cells in AML are mainly spindle cells but may appear as round epithelioid cells [1]. There are two issues regarding this description: (1) what percentage of epithelioid cells required to make the diagnosis of an AML, and (2) whether the amount of epithelioid components and other adverse pathologic features including tumor necrosis, mitosis, and nuclear atypia have any impact on the biologic behavior. There are few recent studies addressing these two major issues [16-18]. In terms of what percentage of epithelioid cells is required to diagnose EAML, different studies adopted different numbers. For example, Aydin et al. proposed that percentage of epithelioid cells for the diagnosis of EAML should be more than 10% [19], while Brimo et al. suggested that the minimal percentage of epithelioid cells for the diagnosis should be 5% [16]. Other authors insist that EAML should be composed of purely epithelioid cells, meanwhile both adipocytes and abnormal blood vessels should be absent [17]. Recently, Nese et al. proposed a nomenclatural system for reporting the renal AML based on the experience and published literature. (a) Tumors that are triphasic/typical histologically classic AML; (b) pure or predominant epithelioid histology of >95%-pure EAML of the kidney; and (c) AML with components of EAML histology of <95%-specify the percentage of epithelioid areas in the report [18]. This nomenclatural system helps minimizing the confusion about the diagnostic criteria of AML or EAML. The next problem is whether the amount of epithelioid components and other adverse pathologic features can have any impact on the biologic behavior. Brimo et al. [16] proposed a predictive model and use 4 features to predict the increased risk of clinically malignant behavior of EAML, while Nese et al. [18] use 5 features to predict the malignant behavior of EAML (Table 1). In addition, Brimo et al. also indicated that renal vein involvement was an important feature for the prognosis of EAML. Two key features, necrosis and renal vein involvement, were shared in these two predictive models. Recently, several reports indicated that p53 and ki67 may useful for judging the malignancy of the EAML [20-22]. In the current case, triphasic components of AML were found in the primary site and the extension to the right atrium. Although epithelioid cells with moderate atypia were found locally, the proportion was no more than 5%. In addition, the tumor cells were negative for p53 and Ki67 index was less than 5%. Taken these together, the final diagnosis was classic AML. The results of immunohistochemical staining also confirmed the diagnosis of AML. However, the necrosis and long thrombus extending into the inferior vena cava and right atrium indicate the potential of poor prognosis. Retroperitoneal hemorrhage from the AML can lead to shock in up to 20% of the patients [23]. In addition, the extension of a renal AML into the renal vein, inferior vena cava, or right cardiac chambers is a significant point of morbidity in this disease Int J Clin Exp Pathol 2013;6(6):
6 Although the pulmonary embolism did not cause any obvious symptoms, it still indicated the high lethal risk. Conclusion This case illustrated a rare example of a renal benign tumor associated with intracardiac extension and asymptomatic pulmonary embolism. Considering the life-threatening complications (tumor immobilization, IVC obstruction), surgical intervention is indicated as early as possible. Because of the fragile nature of the AML thrombus, the risk of embolization is high. This must be considered when choosing the surgical technique. Acknowledgements Written informed consent was obtained from the patient for publication of this case report and accompanying images. A copy of the written consent is available for review by the Editorin Chief of this Journal. Competing interests The authors declare that they have no conflict interests. Address correspondence to: Dr. En-Hua Wang, Department of Pathology, the First Affiliated Hospital and College of Basic Medical Sciences, China Medical University, Shenyang, , China. Tel: ; Fax: ; wangeh775@gmail.com References [1] Ebele JN, Sauter G, Epstein JI and Sesterhenn IA. Pathology and Genetics of Tumours of the Urinary System and Male Genital Organs: WHO Classification of Tumours. Lyon: IARC Press [2] Morgan GS, Straumfjord JV and Hall EJ. Angiomyolipoma of the kidney. J Urol 1951; 65: [3] Grawitz P. Demonstration eines grossen Angio- Myo-Lipoms der Niere. Dtsch Med Wochenschr 1900; 26: 290. [4] Rothenberg DM, Brandt TD and D Cruz I. Computed tomography of renal angiomyolipoma presenting as right atrial mass. J Comput Assist Tomogr 1986; 10: [5] Tsai CC, Chou CY, Han SJ, Mo LR and Lin CC. Cardiac angiomyolipoma: radiologic and pathologic correlation. J Formos Med Assoc 1997; 96: [6] Ito H, Nakashima S, Toma H and Misaki T. Renal angiomyolipoma associated with inferior vena caval and right atrial thrombus. J Urol 1999; 162: [7] Toda F, Okuda H, Kondo N, Iguchi Y, Ryoji O, Ito F, Tanabe K, Goya N, Nakazawa H and Toma H. [Renal angiomyolipoma with a tumor thrombus extending into the right atrium--a case report]. Nihon Hinyokika Gakkai Zasshi 1999; 90: [8] Davydov MI, Matveev VB, Lukianchenko AB, Kudashev BV and Petrovichev NN. Renal angiomyolipoma extending into the right atrium. Urol Int 2001; 67: [9] Akcali Y, Karahan OI, Kahriman G, Ceyran H and Balkanli S. Angiomyolipoma with cavoatrial extension. Eur Urol 2006; 50: [10] Tan YS, Yip KH, Tan PH and Cheng WS. A right renal angiomyolipoma with IVC thrombus and pulmonary embolism. Int Urol Nephrol 2010; 42: [11] Sandstrom CK, Pugsley J and Mitsumori LM. Renal angiomyolipoma with nontraumatic pulmonary fat embolus. AJR Am J Roentgenol 2009; 192: W [12] Ban D, Yamamoto S, Kuno H, Fujimoto H, Fujita S, Akasu T and Moriya Y. A case of huge colon carcinoma and right renal angiomyolipoma accompanied by proximal deep venous thrombosis, pulmonary embolism and tumor thrombus in the renal vein. Jpn J Clin Oncol 2008; 38: [13] Almassi GH. Surgery for tumors with cavoatrial extension. Semin Thorac Cardiovasc Surg 2000; 12: [14] Chiappini B, Savini C, Marinelli G, Suarez SM, Di Eusanio M, Fiorani V and Pierangeli A. Cavoatrial tumor thrombus: single-stage surgical approach with profound hypothermia and circulatory arrest, including a review of the literature. J Thorac Cardiovasc Surg 2002; 124: [15] Kuhn E, De Anda J, Manoni S, Netto G and Rosai J. Renal cell carcinoma associated with prominent angioleiomyoma-like proliferation: Report of 5 cases and review of the literature. Am J Surg Pathol 2006; 30: [16] Brimo F, Robinson B, Guo C, Zhou M, Latour M and Epstein JI. Renal epithelioid angiomyolipoma with atypia: a series of 40 cases with emphasis on clinicopathologic prognostic indicators of malignancy. Am J Surg Pathol 2010; 34: [17] Martignoni G, Pea M, Reghellin D, Zamboni G and Bonetti F. PEComas: the past, the present and the future. Virchows Arch 2008; 452: Int J Clin Exp Pathol 2013;6(6):
7 [18] Nese N, Martignoni G, Fletcher CD, Gupta R, Pan CC, Kim H, Ro JY, Hwang IS, Sato K, Bonetti F, Pea M, Amin MB, Hes O, Svec A, Kida M, Vankalakunti M, Berel D, Rogatko A, Gown AM and Amin MB. Pure epithelioid PEComas (socalled epithelioid angiomyolipoma) of the kidney: A clinicopathologic study of 41 cases: detailed assessment of morphology and risk stratification. Am J Surg Pathol 2011; 35: [19] Aydin H, Magi-Galluzzi C, Lane BR, Sercia L, Lopez JI, Rini BI and Zhou M. Renal angiomyolipoma: clinicopathologic study of 194 cases with emphasis on the epithelioid histology and tuberous sclerosis association. Am J Surg Pathol 2009; 33: [20] Li J, Zhu M and Wang YL. Malignant epithelioid angiomyolipoma of the kidney with pulmonary metastases and p53 gene mutation. World J Surg Oncol 2012; 10: 213. [21] Habib SL, Yadav A, Mahimainathan L and Valente AJ. Regulation of PI 3-K, PTEN, p53, and mtor in Malignant and Benign Tumors Deficient in Tuberin. Genes Cancer 2011; 2: [22] Ooi SM, Vivian JB and Cohen RJ. The use of the Ki-67 marker in the pathological diagnosis of the epithelioid variant of renal angiomyolipoma. Int Urol Nephrol 2009; 41: [23] Isac VM, Silva MR, Beck AL, da Cruz PR, Carvalho ER, de Azevedo AE and Andrade JM. Renal angiomyolipoma with cardiac extension in patient with tuberous sclerosis complex. Circulation 2011; 124: e Int J Clin Exp Pathol 2013;6(6):
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