Open Access

Imaging and histological appearance of pleomorphic hyalinizing angiectatic tumors: A case series and literature review

  • Authors:
    • Couger Jimenez Jaramillo
    • John Wojcik
    • Kristy Weber
    • Ronnie Sebro
  • View Affiliations

  • Published online on: February 2, 2018     https://doi.org/10.3892/ol.2018.7929
  • Pages:4720-4730
  • Copyright: © Jaramillo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Pleomorphic hyalinizing angiectatic tumors (PHATs) are rare mesenchymal soft tissue tumors of uncertain lineage and intermediate malignancy. The present study assesses two cases of PHAT and discusses the histological and immunophenotypical features, as well as the imaging appearance of these tumors on ultrasound, computed tomography (CT), magnetic resonance imaging and positron emission tomography/CT scans. The current study also reviews the literature and discusses the clinical management of these tumors. Wide local excision with tumor free margins is the current recommended treatment for PHAT. Surgical excision may be combined with low‑dose radiation to reduce the risk of local recurrence. Patients should be followed up with serial imaging, as PHAT lesions tend to recur locally.

Introduction

Pleomorphic hyalinizing angiectatic tumors (PHATs) were first described by Smith et al (1) in 1996, and are rare mesenchymal tumors of uncertain lineage and intermediate malignancy (13). PHATs are defined by the presence of clusters of variably-sized thin-walled ectatic vessels that are infiltrated and surrounded by amorphous fibrin-rich hyaline material (1,2). The angiectatic vessels characteristic of PHATs are surrounded by spindle-shaped, plump and round pleomorphic cells commonly arranged in sheets or, more rarely, in fascicles (1). Often, a subset of cells adjacent to the vessels contains intracytoplasmic hemosiderin. The pleomorphic cellular population is composed of large single and multinucleate cells with abundant cytoplasm, enlarged irregular nuclei and, in certain cases, large intranuclear inclusions (1). Mitotic figures are rare (1). PHATs contain a mixed chronic inflammatory infiltrate that is notable for the presence of mast cells, but also includes lymphocytes, plasma cells and eosinophils (1,3). The main mass of a PHAT may be accompanied by a partially myxoid spindle-cell component on the periphery, a potential precursor lesion to a classical PHAT that was described as an early PHAT by Folpe and Weiss in 2004 (2). The first cytogenetic PHAT data published revealed an unbalanced translocation of chromosomes 1 and 3 and chromosomes 1 and 10, with breakpoints mapped to transforming growth factor-β receptor 3 (TGFBR3) and meningioma-expressed antigen 5 (MGEA5) (4). Subsequent fluorescence in situ hybridization and single nucleotide polymorphism analyses of PHATs demonstrated that some, but not all, are characterized by TGFBR3 and MGEA5 gene rearrangements (57).

There are few published reports describing the imaging appearance of PHATs. A PHAT typically appears as a soft tissue mass without osseous changes or calcification (810). In cases in which magnetic resonance imaging (MRI) is utilized, the PHAT presents as a soft-tissue mass that may be accompanied by edema or hematoma. The PHAT appears hypointense-isointense on T1-weighted sequences, heterogeneously isointense-hyperintense on T2-weighted sequences, and exhibits enhancement following administration of intravenous contrast (4,8,1118). The current study presents an assessment of two patients with similar PHATs, and describes the key imaging, histological and immunophenotypical findings of these tumors.

Case reports

Case A

A 50-year old male presented in 2016 to our institution with an 18-month history of an enlarging right buttock mass. The patient first noticed the mass following trauma and subjectively considered that the mass grew to be the size of a grapefruit. The patient denied experiencing any pain, except when sleeping on the right side; at the time of presentation, the patient was taking no pain medication and denied any radicular symptoms, night pain or weight loss. The patient also had normal muscle strength in the right lower extremity. A physical examination revealed a palpable, non-tender mobile mass in the right buttock. A contrast-enhanced computed tomography (CT) scan of the pelvis revealed an 8.0×7.7×8.6 cm heterogeneously enhancing subcutaneous soft tissue mass overlying the right gluteus maximus (Fig. 1A). There was a prominent feeding artery noted as arising from the right profunda artery (Fig. 1B). MRI was performed using a Siemens Verio 3T MRI machine (Siemens AG, Munich, Germany). T1-weighted sequences (repetition time (TR)/echo time (TE), 700/24 ms; slice thickness, 3 mm; interslice gap, 0.9 mm; acquisition matrix, 448×336); short-tau inversion recovery (STIR) sequences (TR/TE, 3400/48 ms; slice thickness, 3 mm; interslice gap, 0.9 mm; and acquisition matrix, 256×192); and T1-weighted contrast-enhanced sequences with fat saturation (TR/TE, 638/23 ms; slice thickness, 4 mm; interslice gap, 0.4 mm; and acquisition matrix 320×256) were obtained. T1-weighted imaging revealed the presence of a heterogeneous predominantly isointense mass (Fig. 2A) with multiple areas of T1 signal hyperintensity (possibly representing areas of hemorrhage) and multiple areas of T1 signal hypointensity. The lesion was superficial to the right gluteus maximus fascia and present in the subcutaneous tissues (Fig. 2B). Multiple flow voids consistent with small arteries were observed in the lesion (Fig. 2C). There was no lymphadenopathy and no osseous involvement. The mass exhibited heterogeneous enhancement following administration of intravenous contrast (Fig. 2D). The lesion was heterogeneously hypoechoic with internal globular and punctate hyperechoic foci when evaluated by ultrasound (Fig. 3).

Histologic sections 5 µm thickness were deparaffinized and stained at room temperature with hematoxylin (5 min) and eosin (40 sec) on a Tissue Tek Prisma Automatic Stainer (Sakura Finetek USA, Inc., Torrance, CA, USA). On examination with light microscopy (variable objectives, magnification range 25–400×), the sections revealed a spindle cell lesion with sparsely sampled, hyalinized vessels. The cellular component was largely bland and spindled, with intermixed hemosiderin-laden macrophages and scattered large, atypical cells. Immunohistochemistry on formalin-fixed, paraffin-embedded tissue was performed using a Leica Bond-IIITM instrument using the Bond Polymer Refine Detection System according to the manufacturer's protocols (DS9800; Leica Microsystems, Inc., Buffalo Grove, IL, USA). Heat-induced epitope retrieval was performed for 20 min with ER1 or ER2 solution (Leica Biosystems) according to the manufacturer's protocols. The tissues were then incubated with the following primary antibodies at room temperature for 15 min: CD34 (ready to use dilution; cat no. PA0354; Leica Biosystems GmbH, Wetzlar, Germany), pancytokeratin (dilution 1:75; cat no. MU357-UC; BioGenex Laboratories, Inc., San Ramon, CA, USA), S100 (ready to use dilution; cat no. IR50461; Dako; Agilent Technologies, Inc., Santa Clara, CA, USA), smooth muscle actin (dilution, 1:600; cat no. M0851; Dako), epithelial membrane antigen (dilution, 1:100, cat no. M0613, Dako) and collagen IV (dilution 1:100; cat no. M0785; Dako). All interpretation of immunohistochemical stains was conducted with routine light-microscopy (variable magnification, ×25-400). On initial biopsies, immunohistochemical studies were inconclusive with respect to line of differentiation. No high-grade features were seen. Given the small sample size and the lack of definitive histological features, the non-specific diagnosis of ‘spindle-cell neoplasm’ was determined, with a differential diagnosis that included PHAT. Positron-emission tomography/computed tomography (PET/CT) demonstrated a mildly hypermetabolic lesion (maximum standardized uptake value of 4.2) with no evidence of hypermetabolic metastases (Fig. 4). The lesion was resected with wide surgical margins. The excised specimen contained a circumscribed tumor with prominent thin-walled, hyalinized vessels (Fig. 5). There were areas of hemorrhage and vascular thrombosis. An intermediate density of bland ovoid cells with rounded nuclear contour and occasional small nucleoli, along with admixed hemosiderin-laden cells and scattered large single- and multi-nucleated atypical cells was also observed. Mitotic activity was low (<1/10 mitoses per high-power field). On the basis of these morphological findings, the patient was diagnosed with PHAT.

Case B

A 72-year-old male presented to our institution in 2013 with a mass along the right buttock that had been slowly growing for almost 30 years. The mass was mildly uncomfortable when the patient sat. The patient also reported no unintentional weight loss or lymphadenopathy. A physical examination revealed a palpable, mobile, non-tender mass measuring approximately 10 cm in size. MRI was performed using a Siemens Espree 3T MRI (Siemens AG). T2-weighted sequences (TR/TE, 6,721/167 ms; slice thickness, 5 mm; interslice gap, 1 mm; and acquisition matrix, 320×320) and T1-weighted gradient imaging with fat saturation following administration of intravenous contrast (TR/TE, 170/2.37 ms; slice thickness, 5 mm; interslice gap, 1 mm; and acquisition matrix, 256×218) were obtained. The lesion was superficial to the fascia of the right gluteus maximus and measured ~6.3×10.4×10.2 cm. The lesion exhibited a heterogeneously hyperintense T2 intensity signal (Fig. 6A) and heterogeneous enhancement following administration of intravenous contrast; there were two prominent arterial vessels originating from the right internal iliac artery supplying the lesion (Fig. 6B and C). The patient underwent gross total resection of the tumor with negative margins. The histological findings were similar to those in case A, although this patient had reduced cellularity and more prominent areas of myxoid stroma (Fig. 7). As in case A, the tumor was composed of a mixture of bland spindle cells with occasional large irregular cells that had retained cytoplasm and large atypical nuclei. There was no discernable mitotic activity or necrosis (Fig. 7). In the immunohistochemical studies, the spindled tumor cells were positive for cluster of differentiation CD34 expression, focally positive for pancytokeratin expression, and negative for the expression of S100, smooth muscle actin, epithelial membrane antigen and collagen IV. The final histological diagnosis was a PHAT.

The requirement for patient consent for publication of the study was waived and ethical approval was provided by the Institutional Review Board of the University of Pennsylvania (Philadelphia, PA, USA).

Discussion

To date, <100 cases of PHAT have been reported worldwide (14,19). The World Health Organization currently classifies PHAT as a benign neoplasm of uncertain differentiation (3). No reports of metastatic PHATs exist; however, it has been known to recur as sarcoma in rare cases (2,20). Owing to its locally aggressive behavior and high recurrence rate (33–50%), it has been argued that a PHAT should be classified as a mesenchymal tumor of intermediate malignancy (2).

PHAT was first described by Smith et al (1) in 1996. The etiology of PHAT is not well understood and a number of competing theories persist regarding the formation of classic PHAT (13). The original description of the tumor by Smith et al (1) posited that the encroachment of a developing PHAT onto the vessels of healthy tissue leads to the release of the plasma contents of damaged endothelial cells, and precipitates a process of organization that results in the tumor's characteristic perivascular hyalinization (1). Smith et al (1) further proposed that the release of vasoactive mast cell products in response to tissue injury from a developing PHAT may be a cause of increased vessel permeability during development (1). Alternately, Folpe and Weiss (2) argue that early PHAT, characterized by low-medium spindle cell density, rare pleomorphic cells and myxoid extracellular matrix, is a precursor lesion to classic PHAT (2). PHAT typically presents in the subcutaneous tissues of the lower extremities, but may also develop intramuscularly, and has been documented in the arm, axilla, back, buccal mucosa, buttock, chest, hand, perineum, popliteal fossa and retroperitoneum (2,3,13,21). The most common locations of PHATs, based on the published literature, include the leg (18/97; 18.6%), thigh (17/97; 17.5%), foot (14/97; 14.4%) and the ankle (10/97; 10.3%) (141). PHAT typically presents in adults; the cases presented in the published literature (97 patients) range in age from 10–89 years, with a median age of 57. PHAT demonstrates a slight predilection for females over males; the literature reviewed in the present study demonstrates a male to female ratio of 3:4 out of 97 reported cases (2,22,23). No information is currently available concerning race and, as <10% of reported cases include this metric, no claims can be made regarding a predilection. Table I presents a list of all previously published cases of PHAT, including data on age, sex, race, tumor size, location and treatment (1,2,4,5,841).

Table I.

List of published studies of PHAT.

Table I.

List of published studies of PHAT.

Author, yearSexAgeRaceLocationTreatmentImagingSize, cmPre-operative duration(Refs.)
Smith et al, 1996M33NRShoulderWide excision + XRTNR3.5NR(1)
F78NRLegLocal excision then amputationNR8NR
F62NRChest wallSimple excision + XRTNR2.5NR
F33NRAnkleExcision + XRTNR5.5NR
M70NRThighSimple excisionNR4.5NR
F32NRLegSimple excisionNRNRNR
F59NRThighAnucleationNR6NR
M72NRThighSimple excisionNR4.5NR
M60NRThighExcisionNR6NR
F58NRChest wallNRNR≥2NR
F78NRArmSimple excisionNRRecurrence, 6NR
M57NRButtockExcisionNRNRNR
M83NRThighExcisionNR2.3NR
F51NRAnkleExcisionNRRecurrence, ≥2.5NR
Folpe and Weiss, 2004F39NRHandNANRNRUnknown(2)
F30NRAnkleLocal excisionNRNRUnknown
M42NRForearmWide excision and XRTNRNRMany years
F46NRFootWide excisionNR13Unknown
M10NRFootWide excisionNRNR1 year
F51NRAnkleLocal excision, then wide excision and XRTNRNRUnknown
F44NRAnkleLocal excisionNR‘Large’Unknown
M67NRLegNANR4Unknown
F32NRLegNANR6Unknown
M36NRThighLocal excisionNR7Unknown
F50NRAnkleLocal excisionNR2.52 months
F53NRFootNANR7Unknown
F84NRLegNANR0.3Unknown
F57NRFootWide excisionNR10.216 years
F49NRLegLocal excisionNRNRUnknown
M56NRAxillaNANRNRUnknown
M49NRThighLocal excisionNRNRUnknown
M79NRPelvisLocal excision, then wide excision and XRTNR14Unknown
M60NRAnkleNANR52–3 years
M27NRThighNANR5.6Many years
M66NRAnkleLocal excision, then wide excision and XRTNR76 months
M54NRFootLocal excision followed by amputation following recurrenceNR3.2Unknown
F32NRLegLocal excision and re-excisionNR52 years
F46NRLegLocal excision and re-excisionNR2Unknown
F77NRThighLocal excision and re-excisionNR14Unknown
F79NRFootWide excisionNR1.8Unknown
F77NRThighNANR4.23 months
M67NRArmNANR5.8Unknown
M89NRLegLocal excision and re-excisionNR3.5Unknown
M74NRButtockLocal excision and re-excisionNR5.5Unknown
F75NRThighNANRNR2 years
M49NRInguinalNANR4Many years
M63NRInguinalNANR113 years
F38NRBackNANR3Unknown
F51NRFootNANR6.5Unknown
M32NRArmNANR6Unknown
M44NRButtockLocal excision and re-excisionNR‘Large’11 years
F67NRAnkleLocal excision and re-excisionNR6.1Unknown
F59NRLegLocal excision, then wide excision and XRTNR6.5Unknown
F42NRFootLocal excision followed by wide excision following recurrenceNR2Unknown
M43NRLegWide excisionNR2020 years
Wei et al, 2012F37CaucasianFootSurgical resection followed by two subsequent re-excisions and external beam radiation to a total of 60 Gy in 30 fractions for recurrencesMRI5NR(4)
Mohajeri et al, 2012F58NRFootSurgical excision with a marginal marginNR0.3×1.5×1.51 year(5)
M33NRThighSurgical excision with a narrow marginNR0.5×3.5×2.5NR
Suzuki et al, 2014F68NRThighWide resection was performed for the internal lesion, whereas an intralesional resection was performed for the outer lesionRadiography, MRI10.5×4.5×3.52 months(8)
Cimino-Mathews and Ali, 2011M46NRLegWide local surgical excisionRadiograph3×1×12 months(9)
Illueca et al, 2012F37NRAnkleSurgical excisionX-ray3.5×2×1.52 months(10)
Lin and Crapanzano, 2005F45NRThighSurgical excisionMRI3.5×2.8×1.53 months(11)
Subhawong et al, 2012M46HispanicLegRadical excisionMRI1.9×1.7×2.1NR(12)
F49African AmericanFootRadical resectionMRI9.5×3.4×7.04 years
F87NRArmSurgical resectionMRI4.8×4.6×5.83 years
Chu et al, 2016F26NRPelvisRadical excisionMRI, CT9.4×9.1×9.5Unknown(13)
Brazio et al, 2016M22NRForearmExcise without wide margins (to retain hand function)MRI16.7×24.2×262 years(14)
Felton and Ramlogan, 2015M62NRLegNRMRI5×65 years(15)
Lee et al, 2005M63NRBreastTotal mastectomy radiologyMRI,25.6×8.3×26.34 years(16)
Fujiwara et al, 2004M69Asian (Japanese)BackSurgical resectionMRI723 years(17)
Fukunaga and Ushigome, 1997M58Asian (Japanese)AxillaMarginal ExcisionUltrasound, MRI, X-Ray82 months(18)
Changchien et al, 2014M76HungarianArmSurgical removalNR4.6×4.5×35 months(19)
Kazakov et al, 2007F76NRAxillaSurgical excisionNR3.5Unknown(20)
Ide et al, 2004F86NRBuccal mucosaSurgical excisionNR3×3×22.5 years(21)
El-Tal and Mehregan, 2005F60NRFootSurgical excisionNR2.2×2.1×1.1NR(22)
Matsumoto and Yamamoto, 2002F83NRThighSurgical resectionNR5.0×5.0×2.010 years(23)
Tallarigo et al, 2009M75NRBreastRadical mastectomy and axillary node clearanceMammograph, ultrasound8Several years(24)
Labanaris et al, 2011M68NRScrotumInguinal radical orchiectomy with high ligation of the spermatic cordUltrasound, CT18×15NR(25)
Capovilla et al, 2006M66NRButtockSurgical excisionNR4NR(26)
Groisman et al, 2000F41NRLegSimple excision for diagnosis then wide local excisionNRNR3 years(27)
F44NRLegSimple excision for diagnosis then wide local excisionNRNR1 year
Gallo et al, 1997F88NAThighNANANANA(28)
Silverman and Dana, 1997F59NRFootLocal ExcisionNR2Unknown(29)
Husek and Veselý, 2001M63NAForearmSurgical excisionNA4.0×3.5×2.5NA(30)
Jaggon and Aitken, 2007F77NRFlankWide local excisionNR8×62 years(31)
Parameshwarappa et al, 2010F65NRForearmWide local excisionNR5×413 years(32)
Peng et al, 2010M49NRButtockSurgical excision followed by wide excision for recurrenceCT of recurrence14×6×3.5NR(33)
Idrees et al, 2013F71CaucasianRenal HilumRight radical nephrectomy and limited retroperitoneal lymph node dissectionCT4.2×6NR(34)
Kuang, 2013F35NRNeckSurgical removalCT3.4×4×56 months(35)
Rekhi and Aggarwal, 2013F63NRLegSurgical resectionNR4×3×33–4 years(36)
Fan et al, 2015F51NRChest wallNRNR2×11 year(37)
Morency et al, 2015F55NRFootNANANANA(38)
Yorita et al, 2015M56Asian (Japanese)ThighSurgical resectionCT6.5×3.8×3.58 months(39)
Kane et al, 2016M35NAHandSurgical excisionNANANA(40)
Onyemkpa and Oyasiji, 2016F79African AmericanInguinalWide localCT excision4.9×7.2×10.77 years(41)

[i] PHAT, Pleomorphic hyalinizing angiectatic tumors; NR, not reported; XRT, radiation therapy; MRI, magnetic resonance imaging; CT, computed tomography; NA, not applicable.

PHAT often rises to medical attention following several years of slow growth (13). Upon clinical examination, PHAT typically presents grossly as an oval-round lobulated mass that varies in color from tan to maroon, and which may be associated with bruising or surrounding hematoma (2,9,10). PHAT may present as partially or predominantly cystic (1,12), may be painless, painful or tender upon examination, and may be accompanied by necrosis in rare cases (1,14).

The imaging appearance of PHAT is non-specific. Typical evaluation of any soft-tissue mass includes radiography of the region, followed by contrast-enhanced MRI evaluation and then by biopsy if clinically warranted. Limited imaging studies of PHAT exist in the literature and the majority of data are in the form of single case reports. In cases in which radiographs are published, there is consensus that PHAT typically appears as a soft tissue mass without osseous changes or calcifications; however, a single case with calcifications has been reported (810,14,24). To the best of our knowledge, only three examples of the ultrasound appearance of PHAT have been described in the literature (18,24,25). All three describe PHAT as a hypoechoic lesion with an internal hyperechogenic appearance, characterized by hyperechoic tissue interrupted by hypoechoic bands, which are presumably blood vessels (18,24,25). In reports of PHAT using MRI, the tumor presents as a soft tissue mass that may be accompanied by edema or hematoma (8,1115). PHAT appears hypointense to isointense with T1 weighting, heterogeneously hyperintense to isointense with T2 weighting, and exhibits heterogeneous enhancement following the intravenous administration of gadolinium-based contrast (4,8,1113,1618). PHATs with well-demarcated and infiltrative borders have previously been described in the literature (9,12). The two cases presented in the current study exhibited prominent borderline ectatic arterial vessels supplying the tumors and well-demarcated tumor borders. The imaging differential diagnosis includes subcutaneous metastasis, melanoma or a soft tissue sarcoma.

PHAT is notable for the presence of clusters of ectatic vessels surrounded by fibrin-rich hyaline material and cuffed by lamellae of collagen that extend into the mass of the tumor and trap individual cells, potentially forming pockets of hyalinized material (1,2). PHATs contain spindle-shaped, plump and round pleomorphic cells (1,2). Cells exhibit hyperchromasia, nuclear pleiomorphism and a lack of cytoplasmic differentiation; they may also contain hemosiderin, nuclear inclusions and cytoplasmic vimentin filaments (9,26). Immunohistochemical analysis of PHATs typically reveal the presence of CD34 and may also detect expression of vimentin, B-cell lymphoma 2, factor XIIIa, vascular endothelial growth factor and CD99; PHAT lacks expression of S-100 protein, CD31, von Willebrand Factor, smooth muscle actin, desmin and epithelial membrane protein (1,2,11,22,27). PHAT cells stained for Ki-67 rarely exhibit positive staining, consistent with the histological observation of few mitotically active cells (1,22). Histological differential diagnoses include neurilemmoma, undifferentiated pleomorphic sarcoma (UPS), giant-cell angiofibroma and solitary fibrous tumor (SFT) (1,3,11,22,23). PHAT can be distinguished from neurilemmoma by the absence of S-100, lack of encapsulation, and the absence of Antoni A and B areas (11,22). PHAT can be distinguished from UPS by its infrequent mitotic figures and the presence of nuclear inclusions (1,9,22). PHAT can be distinguished from by the presence of clusters of thin-walled vessels, atypical cells with bland cytoplasm and intranuclear inclusions (11).

Wide local excision with tumor free margins is the recommended treatment for PHAT (1,2,16) as they may occur as a collision tumor with sarcomas such as myxofibrosarcomas (20). Surgical excision may be combined with low dose radiation to reduce the risk of local recurrence (1,2,4). The patients were followed with serial imaging, as these lesions have a tendency to locally recur. One patient was followed lost to follow up after one year, and the other remains under active imaging surveillance (follow up of 1 year).

The present study reported and discusses the ultrasound, CT, MRI and PET/CT imaging appearance and correlating histology of two histologically verified cases of PHAT. Biopsy remains a requirement because imaging features are non-specific.

Competing interests

The authors declare that they have no competing interests.

Glossary

Abbreviations

Abbreviations:

PHAT

pleomorphic hyalinizing angiectatic tumors

CT

computed tomography

MRI

magnetic resonance imaging

PET/CT

positron emission tomography/computed tomography

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April 2018
Volume 15 Issue 4

Print ISSN: 1792-1074
Online ISSN:1792-1082

2016 Impact Factor: 1.39
Ranked #68/217 Oncology
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APA
Jaramillo, C.J., Wojcik, J., Weber, K., & Sebro, R. (2018). Imaging and histological appearance of pleomorphic hyalinizing angiectatic tumors: A case series and literature review. Oncology Letters, 15, 4720-4730. https://doi.org/10.3892/ol.2018.7929
MLA
Jaramillo, C. J., Wojcik, J., Weber, K., Sebro, R."Imaging and histological appearance of pleomorphic hyalinizing angiectatic tumors: A case series and literature review". Oncology Letters 15.4 (2018): 4720-4730.
Chicago
Jaramillo, C. J., Wojcik, J., Weber, K., Sebro, R."Imaging and histological appearance of pleomorphic hyalinizing angiectatic tumors: A case series and literature review". Oncology Letters 15, no. 4 (2018): 4720-4730. https://doi.org/10.3892/ol.2018.7929