Clinicopathological and genetic features of anastomosing haemangioma of the kidney
Review Article: Medical Tests and Health Care: Pathology

Clinicopathological and genetic features of anastomosing haemangioma of the kidney

Ayo O. Omiyale^, James Carton

Department of Cellular Pathology, Imperial College Healthcare NHS Trust, Charing Cross Hospital, Fulham Palace Road, London, UK

Contributions: (I) Conception and design: AO Omiyale; (II) Administrative support: None; (III) Provision of study materials or patients: AO Omiyale; (IV) Collection and assembly of data: AO Omiyale; (V) Data analysis and interpretation: Both authors; (VI) Manuscript writing: Both authors; (VII) Final approval of manuscript: Both authors.

^ORCID: 0000-0001-9955-9207.

Correspondence to: Ayo O. Omiyale. Department of Cellular Pathology, Imperial College Healthcare NHS Trust, Charing Cross Hospital, Fulham Palace Road, London, UK. Email: ayodeji.omiyale@nhs.net.

Abstract: Anastomosing haemangioma of the kidney is a benign vascular neoplasm composed of thin-walled anastomosing blood vessels. Anastomosing haemangiomas are exceptionally rare. Approximately 75 cases have been described in the literature. The mean age of patients at diagnosis is 49 years (range, 10–83 years). There is a slight male predominance with a male-to-female ratio of 2:1. Patients present with non-specific symptoms including abdominal pain, haematuria, and abdominal mass. Anastomosing haemangiomas are spongy and well circumscribed mahogany brown masses without necrosis. These tumours are usually unilateral and solitary. Microscopically, the tumours are composed of anastomosing capillary-sized blood vessels lined by a single layer of bland endothelial cells. Anastomosing haemangiomas are positive for ERG, CD31, CD34, factor VIII-related antigen and FLI1. These tumours harbour recurrent somatic mutations in the GNAQ gene and its paralogue, GNA14. The considerable overlap of clinical features and imaging characteristics between anastomosing haemangioma and other vascular tumours of the kidney, particularly primary renal angiosarcoma, makes diagnosis quite challenging. Unlike primary renal angiosarcoma, anastomosing haemangioma has an excellent prognosis with no risk of recurrence or metastasis. For this reason, anastomosing haemangioma must be distinguished from primary renal angiosarcoma. Awareness of anastomosing haemangioma of the kidney is essential to avoiding misdiagnosis of primary renal angiosarcoma and preventing unnecessary aggressive treatment.

Keywords: Cancer of kidney; anastomosing haemangioma of the kidney; kidney tumour; vascular neoplasm; angiosarcoma of the kidney

Received: 27 November 2020; Accepted: 18 March 2021; Published: 25 September 2021.

doi: 10.21037/amj-20-181

Introduction

Anastomosing haemangioma is a benign neoplasm composed of anastomosing sinusoidal capillary-sized vessels (1). Initially described in the genitourinary system, the tumour has since been reported in various anatomical sites including the ovary (2,3), adrenal gland, liver, mesentery, testis, spermatic cord, para-aortic tissue, perirenal tissue (3), small and large bowel (4), paraspinal soft tissues, anterior mediastinum, uterine cornu, upper arm and infundibular pelvic ligament (5). Because anastomosing haemangioma mimics primary renal angiosarcoma—a known diagnostic pitfall with implications on management and outcome—there is a need to better understand this neoplasm.

For this narrative review, we extensively searched the English literature for all cases of anastomosing haemangioma of the kidney. This article summarizes state-of-the-art knowledge on the epidemiology, clinical and pathologic features of anastomosing haemangioma of the kidney as well as treatment, prognosis, and differential diagnosis.

Epidemiology

Anastomosing haemangioma of the kidney is extremely rare. To date, approximately 75 cases have been reported in the literature, mostly as case reports or series (1-25). The mean age of patients at diagnosis is 49 years (range, 10–83 years) (6,11,12). There is a slight male predilection with a male-to-female ratio of 2:1 (6). There is no known racial association.

Aetiology

The aetiology is not known. Unlike haemangioma of the bladder, there is no established association with cutaneous haemangiomas, tuberous sclerosis, Klippel-Trenaunay syndrome and Sturge-Weber syndrome (13-15). However, anastomosing haemangioma has been reported in patients with end stage renal disease (ESRD). In a study of 20 nephrectomies from 16 patients with ESRD, there were 36 renal haemangiomas, and all except one were anastomosing haemangiomas (16). Despite the association between ESRD and anastomosing haemangioma, a clear pathogenetic link is yet to be established and the occurrence of anastomosing haemangioma is not unique to ESRD.

Clinical features

Most anastomosing haemangiomas of the kidney are discovered incidentally during imaging or examination of nephrectomies for other renal neoplasms (6). There are no symptoms unique to this tumour. Patients may present with haematuria, abdominal pain, abdominal mass (6) and lower urinary tract symptoms (LUTs) (13). Rarely, patients may present with retroperitoneal haematoma (16,17) or life-threatening haemorrhage (17,18).

This tumour may co-exist with other renal neoplasms including papillary adenoma (16,19,20), metanephric adenoma, papillary renal cell carcinoma, clear cell renal cell carcinoma (21) and acquired cystic disease-associated renal cell carcinoma (16).

There are no imaging features unique to anastomosing haemangiomas. CT imaging shows well-circumscribed, hyperdense and heterogeneous masses with avid post-contrast enhancement (3,22). The considerable overlap of imaging features with other renal tumours makes image-based diagnosis challenging.

Pathology

Grossly, the tumours are well circumscribed masses. They are mostly unencapsulated with fleshy and spongy mahogany brown or haemorrhagic cut surface. The tumours are often small, averaging 2.2 cm in diameter (range, 0.1–12 cm) (6,12). Typically, anastomosing haemangiomas are unilateral and solitary lesions. However, bilateral (2,16,19) and multifocal tumours have been described (16,21). Rarely, gross extension of tumours into the renal vein (1,2,23) or segmental branches of the renal vein (16,24) may be seen. Additionally, the tumours may invade renal sinus fat (16) and perinephric fat (1).

Microscopically, the tumours are well demarcated with a vaguely lobular architecture on low power examination. They are composed of anastomosing sinusoidal capillary-sized vessels lined by a single layer of bland endothelial cells (shown in Figure 1). The vascular channels are separated and supported by loose stroma.

Figure 1 Anastomosing heamangioma of the kidney. The tumour consists of anastomosing blood vessels lined by hobnail endothelial cells (H&E staining, ×200).

Extramedullary haematopoiesis is a common feature in these tumours (1,2,16,25). Rarely, some tumours may contain hyaline globules reminiscent of those seen in Kaposi’s sarcoma (1,2,16). Tumours may feature areas with sclerosis, fibrin thrombi, haemorrhage (1,13,20) and minimal inflammatory infiltrate composed of lymphocytes (1,2). Typically, anastomosing haemangiomas lack features of malignancy including abnormal mitotic figures, marked cytologic atypia, endothelial multilayering and papillary tufting (6).

The lesional cells are positive for CD31 (shown in Figure 2), CD34 (shown in Figure 3), ERG, FLI1 and factor VIII-related antigen. The supporting stromal cells express smooth muscle actin. The lesional cells are negative for HHV-8, a marker for Kaposi’s sarcoma (6).

Figure 2 Anastomosing heamangioma of the kidney. The tumour shows immunolabelling for CD31 (×200).
Figure 3 Anastomosing heamangioma of the kidney. The tumour is positive for CD34 (×200).

Genetics

Anastomosing haemangiomas harbour recurrent somatic mutations in the GNAQ gene and its paralogue, GNA14 (26,27). GNAQ encodes Gαq protein (guanine nucleotide-binding protein G(q) subunit alpha). The protein is part of the heterotrimeric G protein complex. Heterotrimeric G proteins are signal transducers that relay diverse extracellular signals received by G protein coupled receptors (GPCRs) to downstream intracellular effectors (28,29). The heterotrimeric G protein complex comprises 3 subunits: α, β and γ. Gαq is the alpha subunit of the complex and in its inactive state, is bound to guanine diphosphate (GDP) (29).

Upon activation of GPCRs by ligand binding, Gαq releases GDP in exchange for guanine triphosphate (GTP), separates from the complex and activates downstream signalling pathways that are important in the regulation of cell proliferation, survival, protein synthesis and development of blood vessels (30). This signalling is turned off by intrinsic GTPase activity which converts GTP to GDP. Activating somatic mutations in GNAQ impairs the ability of the altered Gαq protein to return to its inactive state. As a result, Gαq remains in its active GTP-bound state and downstream signalling pathways are constantly turned on (26,27,29-31).

Of the 15 anastomosing haemangiomas studied using next generation DNA sequencing, 9 harboured GNAQ p.Q209H mutation; 1 had GNAQ p.Q209L mutation; 4 showed GNA14 p.Q205L mutation; and 1 had neither GNAQ nor GNA14 mutation (26,27). No other pathogenic mutations particularly mutations seen in angiosarcomas were identified in these studies (26). Q205 in GNA14 is a hotspot and the equivalent residue to Q209 in GNAQ (27).

Interestingly, these mutations are not unique to anastomosing haemangiomas. Mutations in GNAQ and its paralogues including GNA11 and GNA14 have been identified in hepatic small vessel neoplasm (HSVN) (32), congenital haemangiomas (33), non-syndromic port wine stains, Sturge-Weber syndrome (34), cherry haemangiomas (35) and melanocytic lesions such as primary uveal melanoma and blue nevi (29).

Prognosis

The vast majority of anastomosing haemangioma of the kidney were treated with radical nephrectomy and only few cases were treated with partial nephrectomy (Table 1). This probably reflects a tendency to overtreat renal anastomosing haemangiomas, probably because most cases have a preoperative diagnosis of renal cell cancer.

Table 1

Treatment and outcome of anastomosing haemangioma of the kidney

Author PMID/Ref No Treatment Follow-up (months) Outcome
Wetherell et al. 23250038 Nephrectomy 1 DFUD
Omiyale et al. 26435872 Nephrectomy 10 NED
Montgomery & Epstein 19606014 Nephrectomy 12 NED
Montgomery & Epstein 19606014 Nephrectomy 36 NED
Montgomery & Epstein 19606014 Nephrectomy NA NA
Montgomery & Epstein 19606014 Excision 8 NED
Brown et al. 20534992 Nephrectomy 72 NED
Brown et al. 20534992 Nephrectomy 24 NED
Brown et al. 20534992 Partial nephrectomy NA NA
Brown et al. 20534992 Nephrectomy 24 NED
Brown et al. 20534992 Nephrectomy NA NA
Tran & Pernicone 24578924 Nephrectomy NA NA
Mehta et al. 23090628 Nephrectomy 3 NED
Mehta et al. 23090628 Nephrectomy 12 NED
Mehta et al. 23090628 Nephrectomy 3 NED
Tahir & Folwell 25041271 Nephrectomy 1 NED
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Kryvenko et al. 24548339 Nephrectomy NA NA
Pantelides et al. (7) Nephrectomy 6 NED
Heidegger et al. 24650180 Nephrectomy 156 NED
Buttner et al. 23020314 Nephrectomy NA NA
Buttner et al. 23020314 Nephrectomy NA NA
Buttner et al. 23020314 Nephrectomy NA NA
Buttner et al. 23020314 Nephrectomy NA NA
Buttner et al. 23020314 Nephrectomy NA NA
Buttner et al. 23020314 Nephrectomy NA NA
Buttner et al. 23020314 Nephrectomy NA NA
Buttner et al. 23020314 Nephrectomy NA NA
Al-Maghrabi & Al-Rashed 28286335 Partial nephrectomy 12 NED
Caballes et al. 30369288 Nephrectomy 18 NED
Kryvenko et al. 21846922 Nephrectomy 7 NED
Kryvenko et al. 21846922 Nephrectomy 6 NED
Kryvenko et al. 21846922 Nephrectomy 3 NED
Kryvenko et al. 21846922 Nephrectomy 122 NED
Cheon et al. 29962849 Nephrectomy 6 NED
Abboudi et al. 29279869 Nephrectomy <1 NED
Silva et al. 28727378 Resection NA NA
Berker et al. 28436289 Partial nephrectomy 10 NED
Berker et al. 28436289 Nephrectomy 4 NED
Bean et al. 28084343 Nephrectomy 9 NED
Bean et al. 28084343 Nephrectomy 84 NED
Bean et al. 28084343 Nephrectomy 107 NED
Zhang et al. 25973131 Partial nephrectomy 16 NED
Perdiki et al. 28118845 Partial nephrectomy 25 NED
Perdiki et al. 28118845 Nephrectomy 14 NED
Chou et al. 23816823 Nephrectomy 8 NED
Chou et al. 23816823 Nephrectomy 14 NED
Zhao et al. 23573324 Nephrectomy 12 NED
Tao et al. 25102914 Nephrectomy 21 NED
Downes et al. (8) Nephrectomy NA NA
Downes et al. (8) Biopsy NA NA
Chandran et al. (9) Nephrectomy NA NA
Cha et al. (10) Nephrectomy 5 NED
Lee et al. 11752931 Nephrectomy NA NA
Memmedoglu & Musayev 26623154 Nephrectomy 12 NED
Memmedoglu & Musayev 26623154 Nephrectomy 12 NED
O’Neil et al. 26960722 NA NA NA
O’Neil et al. 26960722 NA NA NA
O’Neil et al. 26960722 NA NA NA
O’Neil et al. 26960722 NA NA NA
O’Neil et al. 26960722 NA NA NA
O’Neil et al. 26960722 NA NA NA
O’Neil et al. 26960722 NA NA NA
Johnstone et al. 32111399 Nephrectomy NA NA
Manohar et al. 32317537 Nephrectomy 24 NED

NA, not available; NED, no evidence of disease; DFUD, died from unrelated disease.

Of the 75 cases described in the literature, follow-up data were available for 38 patients (50.7%). The mean follow-up time was 24.8 months (range, <1–156 months). One patient died from unrelated disease—embolic cerebrovascular event (13). There was no evidence of recurrence, metastasis or tumour-related death (Table 1).

Differential diagnosis

Anastomosing haemangiomas must be distinguished from primary angiosarcoma of the kidney, Kaposi’s sarcoma, intravascular papillary endothelial hyperplasia (IPEH) and angiomyolipoma (Table 2).

Table 2

Differential diagnosis of anastomosing haemangioma of the kidney

Differential diagnosis Histological findings Immunohistochemistry Prognosis
Anastomosing haemangioma Anastomosing capillary-sized blood vessels, single layer of hobnail endothelial cells, no atypia, extramedullary haematopoiesis ERG+, CD31+, CD34+, FLI1+, HHV8− Excellent prognosis, no metastasis and recurrence
Angiosarcoma Anastomosing blood vessels, endothelial cell multilayering and papillary tufting, atypia, abnormal mitotic figures ERG+, CD31+, CD34+, FLI1+, HHV8− Highly aggressive tumour with limited response to surgery, chemotherapy and radiotherapy
Angiomyolipoma (AML) Variable mixture of mature adipose tissue, poorly organised thick-walled blood vessels and smooth muscle HMB45+, Melan A+, SMA+, Calponin+ Classic AMLs are benign with an excellent prognosis
Epithelioid AMLs can show aggressive behaviour
Kaposi sarcoma Thin-walled blood vessels, slit-like spaces containing extravasated red blood cells, spindled cells, DPAS-positive hyaline globules, plasma cells HHV8+, ERG+, CD31+, CD34+, FLI1+ Outcome depends on the extent of disease and visceral involvement
Intravascular papillary endothelial hyperplasia (Masson’s tumour) Usually arises within a blood vessel, papillary formations, organizing thrombi, exuberant endothelial proliferation, no atypia ERG+, CD31+, CD34+, FLI1+, HHV8− Considered a benign and reactive lesion with an excellent prognosis

Primary renal angiosarcoma is a key differential diagnosis. It shares similar clinical features with anastomosing haemangioma including abdominal mass, haematuria, flank pain and rarely, retroperitoneal haematoma. The imaging features of both tumours are non-specific. They also share similar anastomosing pattern on histology and are positive for CD34, CD31, ERG, FLI1 and factor VIII-related antigen (36).

Unlike anastomosing haemangiomas, primary renal angiosarcomas are malignant vascular tumours. Most renal angiosarcomas occur in patients in their 6th or 7th decade of life, although a wide age range (24–95 years) has been reported (36). They are typically symptomatic and frequently metastasise to various anatomical sites including the liver, lungs, bone, skin, spleen, and lymph nodes. Angiosarcomas are usually large and comprises capillary-sized blood vessels lined by malignant endothelial cells. The neoplastic cells are pleomorphic with hyperchromatic nuclei. Multilayering, abnormal mitotic figures and necrosis are common features. The prognosis of primary angiosarcoma of the kidney is poor despite treatment with surgery, chemotherapy and radiotherapy (36).

Kaposi’s sarcoma is a vascular neoplasm associated with human herpesvirus-8 (HHV-8). Clinically, four variants have been described including classic, endemic, AIDS-associated, and iatrogenic. This tumour is extremely rare in the kidney (37). Microscopically, Kaposi’s sarcoma consists of thin-walled blood vessels, spindled cells, lymphoplasmacytic infiltrate, slit-like spaces containing extravasated red blood cells and DPAS-positive hyaline globules. Hemosiderin deposits may be present. Common to both Kaposi’s sarcoma and anastomosing haemangioma are the presence of thin-walled blood vessels, hyaline globules (although more frequently seen in Kaposi’s sarcoma), and the expression of vascular markers (CD31 and CD34). However, Kaposi sarcoma can be confirmed by the expression of HHV-8-associated protein LANA-1 (6). The outcome is related to the extent of disease and visceral involvement (37).

Intravascular papillary endothelial hyperplasia (Masson’s tumour) is a reactive lesion that commonly occurs within the extremities and head and neck. Rare cases have been reported in the kidney (38). The lesion is characterized by organizing thrombi, prominent papillary structures with hyalinised or fibrous stalks, and hyperplastic endothelial cells, often within the lumen of a large blood vessel, but also in haematomas, or haemangiomas. There are no mitotic figures, atypia or necrosis. These lesions are benign with an excellent prognosis (6,38).

Because anastomosing haemangioma may show fatty changes, they must be distinguished from angiomyolipoma (AML) (39). Angiomyolipoma is composed of thick-walled poorly organized blood vessels, mature adipose tissue and smooth muscle. Unlike anastomosing haemangioma, angiomyolipoma is characterized by the co-expression of smooth muscle markers (smooth muscle actin and calponin) and melanocytic markers (Melan-A, HMB-45 and microphthalmia transcription factor) (6). Classic AMLs are benign; however, epithelioid AMLs may show aggressive behaviour including recurrence and metastasis (40).

Conclusion

Anastomosing haemangiomas of the kidney share similar clinical and imaging features with other renal neoplasms thus making them radiologically indistinguishable. They mimic primary renal angiosarcomas which must be considered as a differential diagnosis and ruled out. Unlike primary renal angiosarcoma with a poor prognosis, anastomosing haemangioma is benign and has an excellent prognosis with no recurrent or metastatic disease during follow-up. Definitive diagnosis requires pathologic assessment. Awareness of this rare tumour and the recognition of its benign clinical course should allow for accurate diagnosis and consideration for nephron-sparing surgery.

Learning points

  • Anastomosing haemangioma of the kidney is a rare tumour.
  • The tumour is characterized by anastomosing capillary-sized blood vessels lined by bland endothelial cells.
  • Most anastomosing haemangiomas are discovered incidentally.
  • Anastomosing haemangioma can mimic other vascular tumours of the kidney, particularly primary renal angiosarcomas.
  • Anastomosing haemangioma harbours recurrent somatic mutations in the GNAQ gene and its paralogue, GNA14.
  • Histopathology is the gold standard for diagnosis.
  • Anastomosing haemangiomas have an excellent prognosis.

Acknowledgments

We would like to thank Philip Brown and Alexandra Roche for proofreading this article.

Funding: None.

Footnote

Conflicts of Interest: Both authors have completed the ICMJE uniform disclosure form (available at https://amj.amegroups.com/article/view/10.21037/amj-20-181/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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doi: 10.21037/amj-20-181
Cite this article as: Omiyale AO, Carton J. Clinicopathological and genetic features of anastomosing haemangioma of the kidney. AME Med J 2021;6:30.

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