Abstract
Purpose
Angiosarcoma (AS) is an aggressive malignant tumour of endothelial origin, most frequently compelling the skin. The kidney is a rare site of primary occurrence of AS with a quite challenging diagnosis and poor prognosis, mainly due to its raw metastasising power. We described our first case of AS treatment. A comprehensive literature review in this field is also carried out.
Patients and methods
We report the case of a 56-years-old man with radiological appearance of an 11 cm poor vascularised left renal mass. The pre-operative imaging ruled out distant metastases and inferior vena cava thrombosis. Thus, after radioembolization, we performed a transperitoneal open radical nephrectomy with regional lymphadenectomy with the removal of the middle portion of the ileo-psoas muscle, followed by two lines of adjuvant chemotherapy. We analysed all the papers concerning primary kidney AS until December 2018.
Results
Estimated intraoperative blood loss was 200 mL with an operative time of 100 minutes. No postoperative complications were recorded, with the patient discharge in the 8th postoperative day. The pathological assessment showed a pT3a N0, M0 tumour compatible with AS of the kidney. An immune-histochemical study showed a vascular positive for CD31, CD34, Fli-1 with a Ki-67/Mib 1 of 50%. One month after surgery the patient began adjuvant chemotherapy with gemcitabine. After 45 days from surgery, a Computed Tomography scan showed lung and liver metastases with disease relapse in the left kidney lodge. The response to the first-line treatment was excellent, unlike the second-line, encountering a chemo-refractory disease. The cancer-specific survival was of 15 months. We included 66 cases in our review.
Conclusion
This is the first case of treatment of kidney AS performed at our Institute. Our findings added new information about the unclear biology and progression of this subset of tumours, demonstrating an abysmal prognosis.
1 Introduction
Angiosarcoma (AS) is a rapid growth tumour of endothelial origin, which accounts for less than 2% of soft tissue sarcomas [1]. Most cases happen in older white men with an extremely high mortality rate mainly due to distant metastasis at the time of diagnosis or shortly afterwards. According to the World Health Organization (WHO), mean survival of 7.7 months was met [2].
Endothelial cells are considered the source of AS, but an origin from circulating stem cells recruited from bone marrow or extra-medullary hematopoiesis is argued [3, 4]. The skin accounts for approximately one-third of cases, especially in the head and neck region or the extremities [5]. Regardless of the primary organ affected, the five years overall survival rate is estimated to be 10-35%, with metastases found commonly in the lungs, liver, and bone, because of early hematogenous dissemination [6].
The bulk of the related literature describes the origin in a healthy kidney as a site of uncommon primary occurrence, reporting only a case of primary AS associated with a renal angiomyolipoma [7]. Some pathological conditions were listed as predisposing factors, but no direct causal relationship was ever demonstrated [8, 9, 10], as well as vinyl chloride, thorium dioxide, or radiation exposition [9]. The role of some genes involved in the receptor protein tyrosine kinase pathway was recently described [11].
The radiological diagnosis of this neoplasm is quite challenging because of the various overlapping characteristics with other tumoural subtypes. Thus, pathological examination with immune-histochemical findings remains essential. The surgical approach seems to ensure the more significant advantage in terms of prognosis, with adjuvant radio- and chemotherapy proposed to improve the cancer-specific survival, even if no standard treatment can be still set. However, in advanced renal disease, the role of surgery is still debated, mainly due to the significant morbidity and the development of effective adjuvant systemic therapies.
This study aimed to describe the first case of AS with extensive necrosis occurring in our Institute, interesting the left kidney. The follow-up was of 15 months until the patient died of the disease. In an attempt to identify prognostic factors and optimal treatment strategy, we also performed a comprehensive literature review, thus improving the knowledge about the aggressive behaviour of this tumour.
2 Material and methods
To provide helpful information to treat our case, we searched the published papers with the terms of ‘primary angiosarcoma of the kidney’ and ‘primary renal angiosarcoma’ in PubMed, Scopus, Google Scholar, and Embase databases, without language limitation. All articles and case reports of primary AS of the kidney until December 2018 were included. We obtained clinical and pathological data, including maximum tumour dimension measured in centimetres, laterality, and immune-histochemical expression of the tumour cells.
Informed consent has been obtained from patient included in this study.
Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance the tenets of the Helsinki Declaration.
3 Case report
A 56-years-old male patient presented to the “Santa Maria della Misericordia” Hospital (Perugia, Italy) with left flank pain. An abdominal ultrasound scan detected a mass in the middle third of the left kidney measuring 8 x 10 cm, toward the lower pole, relatively round shaped. A whole-body Computed Tomography (CT) scan confirmed the presence of 11 cm lower pole mass in the left kidney. It appeared poorly vascularized by the appearance of large central collapsed area with signs of the infiltration of perirenal fat and perirenal band and various small lymph nodes under centimetres at the level of the mesenteric fan (Figure 1). The rapid peripheral enhance-wash-out of the contrast agent in the early arterial phase suggested a
Renal Cell Carcinoma (RCC). No signs of the infiltration of the arterial-venous vascular peduncle or distant metastases were detected, confirmed after that by a bone scan.
The patient presented a single preoperative episode of macroscopic hematuria after diagnostic imaging. One day before surgery, we performed a left renal artery catheter embolisation using a Haemostatic Absorbable Gelatin Sponge (Spongostan, Ethicon™, Somerville, NJ, USA) and polyvinyl alcohol to decrease intraoperative bleeding risk. Then the patient underwent open radical nephrectomy with hilar and para-aortic lymph node dissection made by an expert urologist surgeon (EM) [12, 13, 14]. We removed the perirenal fat tissue, the ipsilateral adrenal gland, a 25 mm tract of the ureter, and the middle portion of the ileo-psoas muscle.
According to our review, radical nephrectomy is the most effective treatment for primary AS (Table 1); surgery was not listed as primary treatment in only 2 cases [15, 16].
Author | Age (yy) | Sex | Side | Clinical presentation | Size (cm) | Mets | Sites (initial and subsequent mets) | Treatment | Follow-up (months) | Outcome |
---|---|---|---|---|---|---|---|---|---|---|
Qayyum et al.[14] | 86 | M | R | wl, fatigue, dizziness | 12.3 | Yes | Liver, lungs | Palliative (patient’s wish) | NA | NA |
Zhang et al.[39] | 52 | M | L | fp, left leg pain | 8 | Yes | Liver, bone | Nephr | NA | NA |
Liu et al.[38] | 75 | M | R | hematuria | 4 | No | No | Nephr, RT | 6 | NED |
Brown et al.[43] | 68 | M | R | NA | 24 | Yes | Liver | NA | 6 | DOD |
Brown et al.[43] | 64 | M | L | NA | 30 | No | No | NA | 11 | DOD |
Brown et al.[43] | 71 | M | L | NA | 10 | Yes | Peritoneal and periaortic LN | NA | 1 | DOD |
Brown et al.[43] | 72 | M | L | NA | NA | No | No | NA | NA | NA |
Brown et al.[43] | 29 | F | L | NA | 3.7 | NA | NA | NA | 1 | DOD |
Brown et al.[43] | 62 | M | NA | NA | NA | NA | NA | Nephr | NA | NA |
Brown et al.[43] | 67 | M | R | NA | NA | NA | NA | Nephr | NA | NA |
Brown et al.[43] | 95 | M | R | NA | 15.5 | NA | NA | Nephr | 2 | DFUD |
Cason et al.[18] | 46 | M | L | fp, wl | 13 | No | Bone, liver, abdominal soft tissue | Nephr, chemotherapy, RT | 10 | DOD |
Allred et al.[44] | 67 | M | R | fp, hematuria | 13 | Yes | Lungs, liver | Nephr, chemotherapy | 3 | DOD |
Peters et al.[45] | 74 | M | L | wl | 19 | Yes | Lungs, liver, abdominal wall, head | Nephr | 2 | DOD |
Prince et al.[17] | 51 | M | L | fp, hematuria | 10 | No | No | Nephr, RT | NA | A&W |
Sabharwal et al.[40] | 67 | M | L | loin pain, wl, loss of appetite | 13 | Yes | Spleen | Nephr, chemotherapy | 1 | NA |
Chaabouni et al.[46] | 59 | M | R | fp, hematuria | 6.5 | No | No | Nephr | 1 | DOD |
López Cubillana et al.[47] | 72 | M | R | hematuria | 13 | No | Bone and lung | Nephr, chemotherapy | 5 | DOD |
Singh et al.[33] | 83 | M | L | hematuria | 13 | No | No | NA | NA | NA |
Askari et al.[48] | 24 | M | R | hematuria, ureteric obstruction | 9 | No | No | Nephr | 4 | DOD |
Douard et al.[49] | 60 | M | R | NA | NA | Yes | Bone, lung | Nephr | 3 | DOD |
Terris et al.[36] | 47 | M | L | fp | 19 | Yes | Diaphragm, renal artery, liver and bone | Nephr, RT | 10 | DOD |
Zenico et al.[50] | 56 | M | L | incidental finding | 20 | No | No | Nephr | 4 | DOD |
Desai et al.[51] | 54 | M | L | fp, hematuria | 21 | No | Bone | Nephr, chemotherapy | 4 | DOD |
Johnson et al.[15] | 50 | M | L | fp, hemoptysis | 9 | Yes | Liver, lung | Rapid deterioration | NA | DOD |
Kern et al.[52] | 69 | M | L | fp, wl, hematuria | 26 | Yes | Lung | Nephr | 1.5 | DOD |
Kern et al.[52] | 52 | M | L | hematuria | 8 | Yes | Lung | Nephr | 3 | DOD |
Fukunaga et al.[32] | 61 | M | L | incidental finding | 8 | No | Liver, bone and retroperitoneum | Nephr | 13 | DOD |
Adjiman et al.[53] | 36 | M | R | hemoptysis, fp, fever | 10.5 | Yes | Chest wall, skin | Nephr | NA | DOD |
Papadimitriou et al.[9] | 68 | M | L | fp, dysuria, hematuria | 10 | No | No | Nephr | NA | A&W |
Tsuda et al.[54] | 77 | M | L | hematuria, renal failure | 10 | No | Retroperitoneum, liver | Nephr | 21 | DOD |
Leggio et al.[34] | 60 | M | L | post-trauma abd pain | 12 | No | Spleen, peritoneum | Nephr | 8 | DOD |
Mordkin et al.[55] | 75 | M | L | fever, wl | 19 | Yes | Spleen, bone, liver, soft tissue, oral cavity | Nephr, chemotherapy, S | NA | NA |
Akkad et al.[35] | 58 | M | R | incidental finding | 4.5 | No | No | Nephr | 30 | NED |
Cerilli et al.[56] | 67 | M | R | fp, hematuria | 12.5 | Yes | Renal vein | Nephr, RT | 6 | DOD |
Aksoy et al.[57] | 55 | M | L | abd pain, rupture with retroperitoneal hematoma | 13 | No | No | Nephr, S | 3 | DOD |
Hiratsuka et al.[19] | 59 | F | R | hematuria | 4.5 | No | No | Nephr | 29 | NED |
Aydogdu et al.[58] | 77 | M | L | NA | NA | NA | NA | Nephr | NA | NA |
Martinez- Pineiro et al.[37] | 66 | M | L | abd pain, anorexia, asthenia | 11.5 | No | Bone, liver, lungs | Nephr | 5 | DOD |
Lee et al.[28] | 63 | M | NA | NA | NA | NA | NA | NA | NA | NA |
Berretta et al.[59] | 67 | M | NA | NA | NA | NA | NA | Nephr, chemotherapy | NA | NA |
Souza et al.[60] | 75 | M | L | wl, fp, hematuria | 15 | No | No | Nephr | NA | DFUD |
Costero-Barrios et al.[61] | 71 | M | L | hematuria, fp | 18 | No | Liver and retroperitoneum | Nephr, chemotherapy, RT | 12 | Recurrence |
Grapsa et al.[62] | 65 | M | R | fever, fatigue, dyspnea | 13.8 | Yes | Liver, lung | NA | NA | NA |
Carnero Lopez et al.[22] | 29 | F | L | Hemoptysis | 11 | Yes | Lungs | Nephr, chemotherapy | 5 | DOD |
Sesar et al.[63] | 65 | M | L | incidental finding | 4.5 | NA | NA | Nephro- | NA | NA |
Pauli et al.[63] | 57 | M | L | hemoptysis | 15 | Yes | Lungs, bone | ureterectomy Nephr, RT | 2 | DOD |
Yoshida et al.[64] | 78 | M | L | fp | 18 | Yes | Liver, bone | Nephr, immunotherapy | 13 | DOD |
Juan et al.[65] | 81 | F | NA | hematuria | 5 | Yes | Liver, bone | Nephr, chemotherapy, RT | 9 | DOD |
Xuan et al.[66] | 63 | M | L | pain and costal swelling | 10 | NA | NA | Nephr | NA | NA |
Yau et al.[67] | 38 | F | R | hematuria, bone pain | 13 | Yes | Bone, LN | Nephr, chemotherapy, RT | 3 | DOD |
Garmendia et al.[68] | 51 | M | NA | NA | NA | NA | NA | NA | NA | NA |
Nguyen et al.[69] | 53 | M | L | hematuria, fp | 7 | Yes | Lung | Nephr, chemotherapy | 18 | DOD |
Limmer et al.[70] | 48 | M | L | fp | 10 | No | Lung, soft tissue, muscle | Nephr | 1 | DOD |
Matter et al.[71] | 62 | M | L | fp, abd mass | 18 | No | Lung | Nephr, chemotherapy, RT | 18 | DOD |
Sanyal et al.[72] | 30 | M | NA | NA | NA | No | No | Nephr, RT | 24 | DOD |
Testa et al.[73] | NA | NA | NA | NA | NA | NA | NA | NA | NA | NA |
Yamamoto et al.[74] | 68 | M | R | incidental finding | 7 | No | No | Nephr, RT | 19 | NED |
Rüb et al.[75] | 59 | M | L | hematuria, wl | 18 | No | Lungs, liver | Nephr, chemotherapy | 12 | AWD |
Celebi et al.[76] | 57 | M | R | fp, hematuria | 14 | No | Lungs, pelvis | Nephr, chemotherapy | 13 | DOD |
Li et al.[77] | 69 | F | L | NA | NA | NA | NA | NA | NA | NA |
Witczak et al.[78] | 44 | F | NA | hematuria | NA | NA | NA | Nephr | NA | NA |
Cuadra-Urteaga et al.[79] | 44 | M | R | hematuria | 7.5 | No | No | Nephro- ureterectomy | 2 | DOD |
Iannaci et al.[26] | 56 | M | L | lower back pain and hematuria | 4 | Yes | Lungs | Nephr | NA | DOD |
Su[80] | 53 | F | R | right lower abd pain | 8.5 | No | Local advanced | Nephr, chemotherapy | NA | DFUD |
Gourley et al.[10] | NA | M | R | acute right fp | 12.5 | No | No | Nephr | NA | NA |
Guan et al. | 64 | F | L | fp, fatigue, wl | 18 | No | Local advanced | Mass excision, chemotherapy | 4 | DOD |
-
Notes:
Abbreviations: Mets, metastases; dx, diagnosis; M, male; F, female; L, left; R, right; NA, not available; abd, abdominal; fp, flank pain; wl, weight loss; LN, lymph node; Nephr, Nephrectomy; NED, no evidence of disease; DFUD, died from unrelated disease; AWD, alive with disease; DOD, died of disease; RT, radiotherapy; S, splenectomy; A&W, alive and well.
4 Results
Estimated intraoperative blood loss was 200 mL and operative time was 100 minutes. The hospital stay was eight days long. Seven days after surgery, serum creatinine and eGFR were 0.98 mg/dL and 81 mL/minute, respectively; after three months, these parameters were the same. No postoperative complications occurred. The surgical specimen consisted of the entire left kidney, weighing 1,080 g and measuring 16 x 11.5 x 7 cm with a portion of the striated muscular belly of ileo-psoas, measuring 3.6 x 2.5 cm. The visible appearance of the solid tumour, located in the lower middle third of the kidney, was a cavitated hemorrhagic necrotising mass of about 14 x 9 cm (Figure 2). Specimens were fixed in 10% formalin, embedded in paraffin wax, sectioned at four μm, and stained with hematoxylin and eosin. Histopathological examination showed vasoformative areas with ramifying channels lined by atypical endothelial cells together with more solid areas lacking vasoformative and composed by high-grade spindle-shaped cells with large hyperchromatic nuclei and prominent nucleoli (Figure 3a). The psoas muscle tissue, surgical margins, ureter, renal artery and vein, and left para-aortic lymph nodes did not appear infiltrated by the tumour. The immune-histochemical study showed strongly and diffusely positive staining for CD31 (Figure 3b), CD34, Fli-1, and remained harmful for pan-cytokeratin, MelanA, HMB45, PGM1, PAX8, GATA3, CD10, racemase, p63, smooth muscle actin, desmin, HHV8; Ki-67/ Mib 1:50%. These findings indicated that the tumour was an AS of the kidney. Ipsilateral adrenal adenoma was also detected.
After 45 days from the surgical procedure, the patient developed hemoptysis. A total body CT scan was then performed with the evidence of a nodular mass of about 3 cm in the left kidney lodge (Fig. 4) and at the level of the left parietal-colic ligament, both showing contrast enhancement after administration of contrast medium. Furthermore, it showed several nodular opacities of the lungs with ground glass opacity (Fig. 5), and multiples hypodense liver lesions (Fig. 6), suggestive of distant metastases. Therefore, the patient underwent bronchoscopy with bioptic samples. The histological report was negative for neoplastic proliferation. In some macrophages, there was the presence of hemosiderin.
We presented the case within the Italian Rare Cancer Network (IRCN), and the patient started first-line chemotherapy with Gemcitabine (1000 mg/mq, day 1-8-15, IV every 21 days) after two months from the surgical procedure, followed by an immediate clinical improvement after the first cycle. The CT scan evaluation performed three months later, showed a brilliant partial response according to the Response Evaluation Criteria in Solid Tumors (RECIST) 1.1 criteria, [17] namely with an almost complete abdominal response and a significant reduction of several lung lesions. A re-assessment CT scan, performed in May 2018, after 11 cycles of therapy, pointed out a severe lung and soft tissue progression. Thus, the patient started second-line chemotherapy with Olaratumab (15 mg/Kg, day 1-8) and Doxorubicin (75 mg/kg, day 1-8) given intravenously every 21 days. Unfortunately, a fast-worsening disease occurred with an impressive progression in lungs, liver, and soft-tissues, confirmed by a total body CT scan assessed after three cycles. The chemotherapy regimen was switched to a weekly Paclitaxel schedule (80 mg/mq). At last, the patient died after four cycles due to hepatic insufficiency. The flow-chart reports the clinical sequence of the patient.
5 Discussion
Over the past few years, significant concerns emerged about the standard treatment of AS, mainly due to the advances in the understanding of its aggressive behaviour [1]. AS unusually harbours from the kidney, and it was first described by Prince in 1942 [18], after a clear definition of this heterogeneous group of the tumour was set [19, 20]. Numerous overlapping radiological characteristics could be observed in particular with RCC [14, 21, 22].
Nowadays, we noted a prevalence of incidental diagnosis in the RCC, while the most common clinical presentation of AS includes macroscopic hematuria (81%), flank pain (38%), or a palpable renal mass (31%) [23]. Its typical histopathological features are the presence of aberrant vascular structures with malignant endothelial cells.
Primary renal AS has a poor prognosis with a high mortality rate mainly due to local recurrence and an early hematogenous spread. Metastases are usually found at the time of diagnosis or develop within a couple of months after surgery. Thus, the absence of detectable metastases at the time of operation does not improve the survival rate, with a minimal number of patients surviving more than one year [8].
Several substances such as thorium dioxide (Thorotrast®) for cerebral angiography, insecticides, and vinyl chloride were linked to the induction of hepatic AS [6, 24, 25, 26]. Conditions associated with the development of AS were radiotherapy, filariasis, chronic lymphedema of any cause (Stewart-Treves syndrome), and von Recklinghausen’s disease, with a recently reported case of AS arising in schwannoma of the kidney [5, 27]. Another example was said to origin in a polycystic kidney [10]. However, none of these risk factors has been proven to have a direct causal relationship with renal AS. The role of some genes, such as p53, VEGF, Ras, Myc, and MDM2, have been explored but their interaction in the development of tumoral phenotype is far to be found [11, 28].
Even if no stable radiological features exist for renal AS, in case of enhancing hypervascular rim and a non-enhancing centre with fast wash-out of the contrast medium, a differential diagnosis with angiomyolipoma shall be done. After that, an advanced RCC and carcinosarcoma should be ruled out [14, 29]. In the latter case the interphase sarcomatous component and carcinomatous one result sharp. In the literature, only one instance of a
Von-Hippel-Lindau negative patient exists, showing the presence of minute clear cell carcinomas between AS and non-tumoral renal parenchyma [30]. To our knowledge, one case of fine-needle aspiration cytology with the application of immune-histochemical analysis was reported in an 83-year-old man, referred to the oncologists for primary chemotherapy [31].
The demonstration of endothelial cell line molecules, like CD31, CD34, and human hematopoietic progenitor cell antigen, was accounted with high specificity and sensitivity [32]. Furthermore, the presence of numerous anastomosing small vessels enveloped by polymorphic tumour cells was probably the consequence of the non-hypoxia induced intratumoral activation with an autonomous, non-dependent by Vascular Endothelial Growth Factor (VEGF) tyrosine kinase receptor activation [33]. Cavernous hemangioma-like, sinusoidal and papillary arrangements might also arise in the tumour [30].
Regarding the treatment of the soft tissue sarcomas, it always involves radical surgery, as margin negativity is crucial for the cure. The role of chemotherapy and radiotherapy remains controversial, even if the latter has demonstrated to improve local control of the disease [34].
The present is an exceptional primary case of AS of the kidney, which updates the limited literature in this field. Beyond its rarity, the lack of information available makes this tumour very difficult to treat. This case occurred in the left kidney of a 56-year-old white man, free of genetic syndromes. He underwent cerebral angiography with thorium dioxide for a cerebrovascular study about thirty years before AS occurrence.
The disease developed insidiously, starting with flank pain, gross hematuria one week before surgery, and weight loss (10 kg in 15 days). Its clinical presentation is in line with that expected by previous reports. Metastases were not detectable at the preoperative CT scan, even if one was suspected in ipsilateral adrenal gland together with infiltration of the psoas muscle. These acquisitions did not stop us from performing a primary surgical strategy to remove all the pathologic tissue since it was demonstrated to be the most effective treatment approach [35]. Based on the histopathological analysis, we found the presence of a benign adenoma, without the involvement of the adrenal gland and the absence of infiltration of the psoas muscle.
The endothelial nature of the neoplastic cells in our case was verified by diffuse positive immune-histochemical staining for the highly sensitive vascular marker CD-34 in 100% of the tumour cells [9, 35]. The raising proliferative nature of the tumour is suggested by the Ki-67 index reported to be 30% [36], 40% (9) [37], and >80% [38] respectively. In our specimen, the Ki-67 index was about 50%, and we now confirm it to indicate a high aggressiveness of this tumour.
After the patient was referred to the oncologist, he performed a two months follow-up CT scan showing local recurrence in the kidney lodge measuring 3 cm and peritoneal, liver, and lung metastases. Although the first line chemotherapy regimen of choice for metastatic AS included anthracyclines plus ifosfamide, often it can be difficult to administer for a suboptimal performance status (PS ECOG 3-4) or advanced age [17].
In this case, the fast-worsening clinical presentation induced to use gemcitabine as the first line, following a retrospective experience collected by the IRCN [39]. As above mentioned, the patient presented an excellent response to the treatment with good progression-free survival of 12 months, but the following line of therapy did not determine any effect, encountering a chemo-refractory disease with a cancer-specific survival of 15 months.
6 Conclusion
Primary AS of the kidney represents a rare variant of renal parenchymal cancer with a high potential of malignancy, profoundly affecting cancer-specific survival. Our findings add new information about the biology and progression of these neoplasms in the attempt to achieve the definition of a standard approach to this tumour.
Acknowledgements
The authors want to thank all the Urologic Clinic and Section of Oncology for patient’s care and all the Section of Anatomic Pathology and Histology of the University Hospital of Perugia for its fundamental contribution in histopathological examination of specimens. The authors are grateful to the patient’s family, in his loving memory.
-
Author Contributions: AB, EM, GC, MT, and RC were responsible for data collection and literature review, ADG and JARDV for oncologic data collection, GB, EL, and AS for acquisition of histopathological data. MDZ provide an entire manuscript formal review. All authors had full access to all the study data and took part in the designing and drafting of the work. All of them reviewed the entire manuscript and take responsibility for the accuracy of the content.
-
Disclosure: None of the authors reports conflicts of interest in this work.
References
[1] Temple WJ, Bramwell V, Eisenhauer E, Jenkin RD, Langer F, Worth AJ: Guidelines for the surgical management of soft-tissue sarcoma. Report of the Canadian Sarcoma Group. Canadian Journal of surgery Journal canadien de chirurgie 1988, 31(6):410-412Search in Google Scholar
[2] Nachman J, Simon MA, Dean L, Shermeta D, Dawson P, Vogelzang NJ: Disparate histologic responses in simultaneously resected primary and metastatic osteosarcoma following intravenous neoadjuvant chemotherapy. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 1987, 5(8):1185-119010.1200/JCO.1987.5.8.1185Search in Google Scholar
[3] Young RJ, Brown NJ, Reed MW, Hughes D, Woll PJ: Angiosarcoma. The Lancet Oncology 2010, 11(10):983-99110.1016/S1470-2045(10)70023-1Search in Google Scholar
[4] Cohen SM, Storer RD, Criswell KA, Doerrer NG, Dellarco VL, Pegg DG, Wojcinski ZW, Malarkey DE, Jacobs AC, Klaunig JE et al: Hemangiosarcoma in rodents: mode-of-action evaluation and human relevance. Toxicological sciences : an official journal of the Society of Toxicology 2009, 111(1):4-1810.1093/toxsci/kfp131Search in Google Scholar
[5] Cui L, Zhang J, Zhang X, Chang H, Qu C, Zhang J, Zhong D: Angiosarcoma (Stewart-Treves syndrome) in postmastectomy patients: report of 10 cases and review of literature. International journal of clinical and experimental pathology 2015, 8(9):11108-11115Search in Google Scholar
[6] Mark RJ, Poen JC, Tran LM, Fu YS, Juillard GF: Angiosarcoma. A report of 67 patients and a review of the literature. Cancer 1996, 77(11):2400-240610.1002/(SICI)1097-0142(19960601)77:11<2400::AID-CNCR32>3.0.CO;2-ZSearch in Google Scholar
[7] Gourley E, Digman G, Nicolas M, Kaushik D: Primary renal angiosarcoma. BMJ case reports 2018, 201810.1136/bcr-2017-222672Search in Google Scholar
[8] Oskrochi Y, Razi K, Stebbing J, Crane J: Angiosarcoma and Dialysis-related Arteriovenous Fistulae: A Comprehensive Review. European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery 2016, 51(1):127-13310.1016/j.ejvs.2015.08.016Search in Google Scholar
[9] Omiyale AO: Clinicopathological features of primary angiosarcoma of the kidney: a review of 62 cases. Translational andrology and urology 2015, 4(4):464-473Search in Google Scholar
[10] Papadimitriou VD, Stamatiou KN, Takos DM, Adamopoulos VM, Heretis IE, Sofras FA: Angiosarcoma of kidney: a case report and review of literature. Urol J 2009, 6(3):223-225Search in Google Scholar
[11] Styring E, Seinen J, Dominguez-Valentin M, Domanski HA, Jonsson M, von Steyern FV, Hoekstra HJ, Suurmeijer AJ, Nilbert M: Key roles for MYC, KIT and RET signaling in secondary angiosarcomas. British journal of cancer 2014, 111(2):407-41210.1038/bjc.2014.359Search in Google Scholar
[12] Cochetti G, Barillaro F, Boni A, Del Zingaro M, Ettore M: Robot assisted laparoscopic excision of a paraganglioma: new therapeutic approach. International braz j urol : official journal of the Brazilian Society of Urology 2014, 40(2):279-28010.1590/S1677-5538.IBJU.2014.02.21Search in Google Scholar
[13] Cochetti G, Barillaro F, Boni A, Mearini E: Immediate Radical Cystectomy for Massive Bleeding of Bladder Cancer. BioMed research international 201510.1155/2015/154392Search in Google Scholar
[14] Boni A, Cochetti G, Ascani S, Del Zingaro M, Quadrini F, Paladini A, Cocca D, Mearini E: Robotic treatment of oligometastatic kidney tumor with synchronous pancreatic metastasis: case report and review of the literature. BMC surgery 2018, 18(1):4010.1186/s12893-018-0371-xSearch in Google Scholar
[15] Qayyum S, Parikh JG, Zafar N: Primary renal angiosarcoma with extensive necrosis: a difficult diagnosis. Case reports in pathology 2014, 2014:41617010.1155/2014/416170Search in Google Scholar
[16] Johnson VV, Gaertner EM, Crothers BA: Fine-needle aspiration of renal angiosarcoma. Archives of pathology & laboratory medicine 2002, 126(4):478-48010.5858/2002-126-0478-FNAORASearch in Google Scholar
[17] Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M et al: New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 2009, 45(2):228-24710.1016/j.ejca.2008.10.026Search in Google Scholar
[18] Prince M: Concerning a Letter to Past Presidents of the California Medical Association and Reply thereto. California and western medicine 1942, 56(5):331Search in Google Scholar
[19] Cason JD, Waisman J, Plaine L: Angiosarcoma of kidney. Urology 1987, 30(3):281-28310.1016/0090-4295(87)90258-5Search in Google Scholar
[20] Hiratsuka Y, Nishimura H, Kajiwara I, Matsuoka H, Kawamura K: Renal angiosarcoma: a case report. Int J Urol 1997, 4(1):90-9310.1111/j.1442-2042.1997.tb00148.xSearch in Google Scholar PubMed
[21] Cochetti G, Puxeddu E, Del Zingaro M, D’Amico F, Cottini E, Barillaro F, Mearini E: Laparoscopic partial nephrectomy of thyroid cancer metastasis: case report and review of the literature. OncoTargets and therapy 2013, 6:355-36010.2147/OTT.S37402Search in Google Scholar PubMed PubMed Central
[22] Mearini E, Cochetti G, Barillaro F, Fatigoni S, Roila F: Renal malignant solitary fibrous tumor with single lymph node involvement: report of unusual metastasis and review of the literature. OncoTargets and therapy 2014, 7:679-68510.2147/OTT.S51664Search in Google Scholar PubMed PubMed Central
[23] Carnero Lopez B, Fernandez Perez I, Carrasco Alvarez JA, Lazaro Quintela ME, Lopez Jato C, Jorge Fernandez M, Gentil Gonzalez M, Vazquez Tunas L, Castellanos Diez J: Renal primary angiosarcoma. Clinical & translational oncology : official publication of the Federation of Spanish Oncology Societies and of the National Cancer Institute of Mexico 2007, 9(12):806-81010.1007/s12094-007-0144-ySearch in Google Scholar PubMed
[24] Popper H, Thomas LB, Telles NC, Falk H, Selikoff IJ: Development of hepatic angiosarcoma in man induced by vinyl chloride, thorotrast, and arsenic. Comparison with cases of unknown etiology. The American journal of pathology 1978, 92(2):349-376Search in Google Scholar
[25] Ho SY, Tsai CC, Tsai YC, Guo HR: Hepatic angiosarcoma presenting as hepatic rupture in a patient with long-term ingestion of arsenic. Journal of the Formosan Medical Association = Taiwan yi zhi 2004, 103(5):374-379Search in Google Scholar
[26] Alrenga DP: Primary angiosarcoma of the liver. Review article. International surgery 1975, 60(4):198-203Search in Google Scholar
[27] Iannaci G, Crispino M, Cifarelli P, Montella M, Panarese I, Ronchi A, Russo R, Tremiterra G, Luise R, Sapere P: Epithelioid angiosarcoma arising in schwannoma of the kidney: report of the first case and review of the literature. World journal of surgical oncology 2016, 14(1):2910.1186/s12957-016-0789-5Search in Google Scholar PubMed PubMed Central
[28] Yang J, Kantrow S, Sai J, Hawkins OE, Boothby M, Ayers GD, Young ED, Demicco EG, Lazar AJ, Lev D et al: INK4a/ARF [corrected] inactivation with activation of the NF-kappaB/IL-6 pathway is sufficient to drive the development and growth of angiosarcoma. Cancer research 2012, 72(18):4682-469510.1158/0008-5472.CAN-12-0440Search in Google Scholar PubMed PubMed Central
[29] Pansadoro A, Cochetti G, D’amico F, Barillaro F, Del Zingaro M, Mearini E: Retroperitoneal laparoscopic renal tumour enucleation with local hypotension on demand. World J Urol 2015, 33(3):427-43210.1007/s00345-014-1325-2Search in Google Scholar
[30] Fukunaga M: Angiosarcoma of the kidney with minute clear cell carcinomas: a case report. Pathology, research and practice 2009, 205(5):347-35110.1016/j.prp.2008.11.005Search in Google Scholar
[31] Singh C, Xie L, Schmechel SC, Manivel JC, Pambuccian SE: Epithelioid angiosarcoma of the kidney: a diagnostic dilemma in fine-needle aspiration cytology. Diagnostic cytopathology 2012, 40 Suppl 2:E131-13910.1002/dc.21762Search in Google Scholar
[32] Leggio L, Addolorato G, Abenavoli L, Ferrulli A, D’Angelo C, Mirijello A, Vonghia L, Schinzari G, Arena V, Perrone L et al: Primary renal angiosarcoma: a rare malignancy. A case report and review of the literature. Urologic oncology 2006, 24(4):307-31210.1016/j.urolonc.2005.10.002Search in Google Scholar
[33] Akkad T, Tsankov A, Pelzer A, Peschel R, Bartsch G, Steiner H: Early diagnosis and straight forward surgery of an asymptomatic primary angiosarcoma of the kidney led to long-term survival. Int J Urol 2006, 13(8):1112-111410.1111/j.1442-2042.2006.01490.xSearch in Google Scholar
[34] Terris D, Plaine L, Steinfeld A: Renal angiosarcoma. American journal of kidney diseases : the official journal of the National Kidney Foundation 1986, 8(2):131-13310.1016/S0272-6386(86)80126-3Search in Google Scholar
[35] Martinez-Pineiro L, Lopez-Ferrer P, Picazo ML, Martinez-Pineiro JA: Primary renal angiosarcoma. Case report and review of the literature. Scand J Urol Nephrol 1995, 29(1):103-10810.3109/00365599509180547Search in Google Scholar PubMed
[36] Liu H, Huang X, Chen H, Wang X, Chen L: Epithelioid angiosarcoma of the kidney: A case report and literature review. Oncology letters 2014, 8(3):1155-115810.3892/ol.2014.2292Search in Google Scholar PubMed PubMed Central
[37] Zhang HM, Yan Y, Luo M, Xu YF, Peng B, Zheng JH: Primary angiosarcoma of the kidney: case analysis and literature review. International journal of clinical and experimental pathology 2014, 7(7):3555-3562Search in Google Scholar
[38] Sabharwal S, John NT, Kumar RM, Kekre NS: Primary renal angiosarcoma. Indian journal of urology : IJU : journal of the Urological Society of India 2013, 29(2):145-14710.4103/0970-1591.114040Search in Google Scholar PubMed PubMed Central
[39] Stacchiotti S, Palassini E, Sanfilippo R, Vincenzi B, Arena MG, Bochicchio AM, De Rosa P, Nuzzo A, Turano S, Morosi C et al: Gemcitabine in advanced angiosarcoma: a retrospective case series analysis from the Italian Rare Cancer Network. Ann Oncol 2012, 23(2):501-50810.1093/annonc/mdr066Search in Google Scholar PubMed
[40] Brown JG, Folpe AL, Rao P, Lazar AJ, Paner GP, Gupta R, Parakh R, Cheville JC, Amin MB: Primary vascular tumors and tumor-like lesions of the kidney: a clinicopathologic analysis of 25 cases. The American journal of surgical pathology 2010, 34(7):942-94910.1097/PAS.0b013e3181e4f32aSearch in Google Scholar PubMed
[41] Allred CD, Cathey WJ, McDivitt RW: Primary fenal angiosarcoma: a case report. Human pathology 1981, 12(7):665-66810.1016/S0046-8177(81)80054-8Search in Google Scholar
[42] Peters HJ, Nuri M, Munzenmaier R: Hemangioendothelioma of the kidney: a case report and review of the literature. The Journal of urology 1974, 112(6):723-72610.1016/S0022-5347(17)59836-5Search in Google Scholar
[43] Chaabouni A, Rebai N, Chabchoub K, Fourati M, Bouacida M, Slimen MH, Bahloul A, Mhiri MN: Primary renal angiosarcoma: Case report and literature review. Canadian Urological Association journal = Journal de l’Association des urologues du Canada 2013, 7(5-6):E430-43210.5489/cuaj.1396Search in Google Scholar
[44] Lopez Cubillana P, Martinez Barba E, Server Pastor G, Prieto Gonzalez A, Ferri Niguez B, Cao Avellaneda E, Lopez Lopez AI, Nicolas Torroalba JA, Rigabert Montiel M, Tornero Ruiz J et al: [Fatal evolution of a renal angiosarcoma]. Archivos espanoles de urologia 2004, 57(4):425-426Search in Google Scholar
[45] Askari A, Novick A, Braun W, Steinmuller D: Late ureteral obstruction and hematuria from de novo angiosarcoma in a renal transplant patient. The Journal of urology 1980, 124(5):717-71910.1016/S0022-5347(17)55625-6Search in Google Scholar
[46] Douard A, Pasticier G, Deminiere C, Wallerand H, Ferriere JM, Bernhard JC: [Primary angiosarcoma of the kidney: case report and literature review]. Progres en urologie : journal de l’Association francaise d’urologie et de la Societe francaise d’urologie 2012, 22(7):438-44110.1016/j.purol.2011.11.006Search in Google Scholar PubMed
[47] Zenico T, Saccomanni M, Salomone U, Bercovich E: Primary renal angiosarcoma: case report and review of world literature. Tumori 2011, 97(4):e6-910.1177/030089161109700422Search in Google Scholar PubMed
[48] Desai MB, Chess Q, Naidich JB, Weiner R: Primary renal angiosarcoma mimicking a renal cell carcinoma. Urologic radiology 1989, 11(1):30-3210.1007/BF02926469Search in Google Scholar PubMed
[49] Kern SB, Gott L, Faulkner J, 2nd: Occurrence of primary renal angiosarcoma in brothers. Archives of pathology & laboratory medicine 1995, 119(1):75-78Search in Google Scholar
[50] Adjiman S, Zerbib M, Flam T, Brochard M, Desligneres S, Boissonnas A, Debre B, Steg A: Genitourinary tumors and HIV1 infection. European urology 1990, 18(1):61-6310.1159/000463869Search in Google Scholar PubMed
[51] Tsuda N, Chowdhury PR, Hayashi T, Anami M, Iseki M, Koga S, Matsuya F, Kanetake H, Saito Y, Horita Y: Primary renal angiosarcoma: a case report and review of the literature. Pathology international 1997, 47(11):778-78310.1111/j.1440-1827.1997.tb04457.xSearch in Google Scholar PubMed
[52] Mordkin RM, Dahut WL, Lynch JH: Renal angiosarcoma: a rare primary genitourinary malignancy. Southern medical journal 1997, 90(11):1159-116010.1097/00007611-199711000-00023Search in Google Scholar PubMed
[53] Cerilli LA, Huffman HT, Anand A: Primary renal angiosarcoma: a case report with immunohistochemical, ultrastructural, and cytogenetic features and review of the literature. Archives of pathology & laboratory medicine 1998, 122(10):929-935Search in Google Scholar
[54] Aksoy Y, Gursan N, Ozbey I, Bicgi O, Keles M: Spontaneous rupture of a renal angiosarcoma. Urologia internationalis 2002, 68(1):60-6210.1159/000048419Search in Google Scholar
[55] Aydogdu I, Turhan O, Sari R, Ates M, Turk M: Coincidental acute myeloblastic leukemia in a patient with renal angiosarcoma. Haematologia 1999, 29(4):313-317Search in Google Scholar
[56] Lee TY, Lawen J, Gupta R: Renal angiosarcoma: a case report and literature review. The Canadian journal of urology 2007, 14(1):3471-3476Search in Google Scholar
[57] Berretta M, Rupolo M, Buonadonna A, Canzonieri V, Brollo A, Morra A, Berretta S, Bearz A, Tirelli U, Frustaci S: Metastatic angiosarcoma of the kidney: a case report with treatment approach and review of the literature. Journal of chemotherapy (Florence, Italy) 2006, 18(2):221-22410.1179/joc.2006.18.2.221Search in Google Scholar
[58] Souza OE, Etchebehere RM, Lima MA, Monti PR: Primary renal angiosarcoma. International braz j urol : official journal of the Brazilian Society of Urology 2006, 32(4):448-45010.1590/S1677-55382006000400011Search in Google Scholar
[59] Costero-Barrios CB, Oros-Ovalle C: [Primary renal angiosarcoma]. Gaceta medica de Mexico 2004, 140(4):463-466Search in Google Scholar
[60] Grapsa D, Sakellariou S, Politi E: Fine-needle aspiration cytology of primary renal angiosarcoma with histopathologic and immunocytochemical correlation: a case report. Diagnostic cytopathology 2014, 42(10):872-87610.1002/dc.23051Search in Google Scholar
[61] Sesar P UM, Šoša S et al.: Primary renal angiosarcoma. Acta clinica Croatica 2012, 51(182)Search in Google Scholar
[62] Yoshida K, Ito F, Nakazawa H, Maeda Y, Tomoe H, Aiba M: A case of primary renal angiosarcoma. Rare tumors 2009, 1(2):e2810.4081/rt.2009.e28Search in Google Scholar
[63] Juan CJ YC, Hsu HH, et al. : Visceral and non-visceral angiosarcoma: Imaging features and clinical correlation. Chin J Radiol 2000, 25:183-189Search in Google Scholar
[64] Y.Xuan: Primary renal angiosarcoma: one case report and literatures review. . Chin J Clin Oncol 2008, 5::229-30010.1007/s11805-008-0229-6Search in Google Scholar
[65] Yau T, Leong CH, Chan WK, Chan JK, Liang RH, Epstein RJ: A case of mixed adult Wilms’ tumour and angiosarcoma responsive to carboplatin, etoposide and vincristine (CEO). Cancer chemotherapy and pharmacology 2008, 61(4):717-72010.1007/s00280-007-0529-1Search in Google Scholar
[66] Garmendia JC, Lopez Garcia JA, Acinas Garcia O, Garrido Rivas C, Sanroma Ortueta C, Arocena Lanz F: [Angiosarcoma of the kidney]. Actas urologicas espanolas 1989, 13(3):223-224Search in Google Scholar
[67] Nguyen T, Auquier MA, Renard C, Cordonnier C, Saint F, Remond A: [Hemoptysis and spontaneous rupture of a primary renal angiosarcoma: a case report]. Journal de radiologie 2010, 91(12 Pt 1):1313-131710.1016/S0221-0363(10)70201-8Search in Google Scholar
[68] Limmer S, Wagner T, Leipprand E, Arnholdt H: [Primary renal hemangiosarcoma. Case report and review of the literature]. Der Pathologe 2001, 22(5):343-34810.1007/s002920100481Search in Google Scholar
[69] Matter LE, Flury R, Hailemariam S, Hauri D, Sulser T: [Angiosarcoma of the kidney. Case report and review of the literature]. Der Urologe Ausg A 1999, 38(1):65-6810.1007/s001200050248Search in Google Scholar PubMed
[70] Sanyal B, Mehrotra ML, Gupta S, Pant GC: Radiotherapy in renal angiosarcoma. Journal of the Indian Medical Association 1979, 72(4):85-86Search in Google Scholar
[71] Testa G TG, Tufano A, et al. : Primary renal angiosarcoma: a case report. . Acta Urologica Italica 1998, 12:225-227Search in Google Scholar
[72] Yamamoto Y, Izaki H, Harada A, Taue R, Kishimoto T, Tanimoto S, Fukumori T, Takahashi M, Nishitani MA, Kanayama HO et al: [A case of renal capsular hemangiosarcoma]. Hinyokika kiyo Acta urologica Japonica 2006, 52(3):215-217Search in Google Scholar
[73] Rub J, Bauer S, Pastor J, Noldus J, Palisaar RJ: [Primary renal angiosarcoma. Uncommon manifestation of a rare malignancy]. Der Urologe Ausg A 2015, 54(6):849-85310.1007/s00120-015-3809-0Search in Google Scholar
[74] Celebi F, Pilanci KN, Saglam S, Balci NC: Primary renal angiosarcoma with progressive clinical course despite surgical and adjuvant treatment: A case report. Oncology letters 2015, 9(4):1937-193910.3892/ol.2015.2902Search in Google Scholar PubMed PubMed Central
[75] Li N, Li W, Li Z: [Primary renal epithelioid angiosarcoma with transitional cell carcinoma in renal pelvis]. Zhonghua wai ke za zhi [Chinese journal of surgery] 1997, 35(5):294-295Search in Google Scholar
[76] Witczak W, Szubstarski F, Szymanski C, Rajca Z, Staszczyk S: [Renal hemangiosarcoma]. Polski tygodnik lekarski (Warsaw, Poland : 1960) 1993, 48(20-22):483-484Search in Google Scholar
[77] Cuadra-Urteaga JL, Font A, Tapia G, Areal J, Taron M: Carcinosarcoma of the upper urinary tract with an aggressive angiosarcoma component. Cancer biology & therapy 2016, 17(3):233-23610.1080/15384047.2016.1139237Search in Google Scholar PubMed PubMed Central
[78] Su YC: Angiosarcoma of kidney with calcification: A rare case report. The Kaohsiung journal of medical sciences 2017, 33(7):367-36810.1016/j.kjms.2017.03.009Search in Google Scholar PubMed
© 2019 Andrea Boni et al., published by De Gruyter
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.