Accepted Manuscript Intraventricular hemangiopericytoma: a case report and literature review James E. Towner, MD, Mahlon D. Johnson, MD, PhD, Yan Michael Li, MD, PhD PII:
S1878-8750(16)00144-3
DOI:
10.1016/j.wneu.2016.01.056
Reference:
WNEU 3660
To appear in:
World Neurosurgery
Received Date: 24 October 2015 Revised Date:
11 January 2016
Accepted Date: 11 January 2016
Please cite this article as: Towner JE, Johnson MD, Li YM, Intraventricular hemangiopericytoma: a case report and literature review, World Neurosurgery (2016), doi: 10.1016/j.wneu.2016.01.056. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
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Title:
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Intraventricular hemangiopericytoma: a case report and literature review.
3 Authors:
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James E. Towner, MD1; Mahlon D Johnson, MD, PhD2; Yan Michael Li, MD, PhD1
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Affiliations:
(1) Department of Neurosurgery, University of Rochester School of Medicine and Dentistry, Rochester, NY 14620
(2) Department of Pathology and Laboratory Medicine, University of Rochester School of Medicine
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and Dentistry, Rochester, NY 14620
Corresponding Author:
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James E. Towner
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Department of Neurosurgery
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601 Elmwood Ave
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Rochester NY 14642
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[email protected] 19
Phone: 256.651.2971
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Fax: 585.756.5183
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Publication History:
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Neither this manuscript nor any portion of it has been previously published in any form.
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Key words:
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Hemangiopericytoma; intraventricular; lateral ventricle; solitary fibrous tumor
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Abbreviation List:
29 30 31 32 33 34 35 36 37
CNS - central nervous system DSA - digitial subtraction angiography EMA – epithelial membrane antigen EVD - external ventricular drain Gy - gray GTR - gross total resection HPC - hemangiopericytoma SFT - solitary fibrous tumor WHO - World Health Organization
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Background
39
Hemangiopericytomas (HPC) are vascular mesenchymal tumors, classified by the World-Health
40
Organization (WHO) as grade II or, if anaplastic elements are identified, grade III neoplasms. The term
41
HPC was coined by Stout and Murray1 in 1942 to describe a malignant soft tissue tumor of primarily the
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thigh, buttocks and retroperitoneum with high vascularity composed of capillary endothelial pericytes. In
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1954, the first intracranial HPC was reported by Begg and Garrett2, who described a left parietal HPC.
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Begg and Garrett felt that entities which had previously been described as angioblastic meningiomas in
45
fact originate from pericytes and should be reclassified as HPC. It was not until 1993 that the WHO
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revised its classification such that those CNS neoplasms previously termed angioblastic meningiomas
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were categorized as HPC. Today, CNS HPC are understood to be clinically and pathologically distinct
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from meningiomas.
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Intraventricular locations are exceedingly rare for CNS HPC. Only 11 case reports of intraventricular
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HPC have been described in the literature. Table 1 summarizes the reported cases, including the following
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case.3-13 The average age of diagnosis for intraventricular HPC is 41 and is congruent with the reported
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age of diagnosis of intracranial HPC located outside the ventricles. The youngest patient with a
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ventricular HPC was in a 9-year-old, which was discovered at autopsy.9 The following case, in a 23-year-
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old, involves one of the youngest patients to undergo treatment for an intraventricular HPC.
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Case Description
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History and Physical Examination
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VO is a 23-year-old, right-handed male who presented with a chief complaint of 4 weeks of bifrontal
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headache. He described his headache as pulsating or throbbing, worse in the morning and improved by
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evening. The headache became persistent after 2 weeks. On further questioning, he endorsed occasional
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photophobia, blurry vision, nausea, and emesis. He also reported intermittent episodes of difficulty with
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word-finding and naming, as well as transient episodes of numbness of the right face, arm, and hand. On
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physical exam, he was found to have a right homonymous hemianopia and mild right arm weakness with
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a right-sided pronator drift.
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Radiographic Evaluation
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A computed tomography scan was obtained, revealing a large mass in the left lateral ventricle; a
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representative image is shown in Figure 1. Follow-up magnetic resonance imaging was performed, with
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representative T1, T2, and T1 post-contrast images shown in Figures 2a-c, respectively. A digital
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subtraction angiography (DSA) was then performed to delineate the vascular supply and drainage of the
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mass. The DSA showed the mass was supplied laterally by left middle cerebral artery branches, inferiorly
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by left anterior choroidal branches, and posteriorly by left posterior choroidal branches; venous drainage
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appeared to be primarily into the internal cerebral vein and basal vein of Rosenthal.
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Operative Description
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A left parieto-occipital craniotomy was performed for a superior parietal transcortical approach to the
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tumor. Once the mass was exposed, a central debulking was performed. An intracapsular piecemeal
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resection of the remaining tumor followed, resulting in a radiographic gross total resection (GTR), as
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illustrated in Figure 3. A left-sided external ventricular drain (EVD) was placed to aid in drainage of post-
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operative hemorrhage in the resection cavity and ventricles.
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Pathologic Findings
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The sections of tumor revealed a hypercellular, diffuse spindle cell tumor which, in the majority of areas,
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exhibited ovoid nuclei, little cytoplasm and numerous slit-like blood vessels, as illustrated in Figure 4a.
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The reticulin stain showed extensive pericellular staining, as seen in Figure 4b. Multifocal necrosis and
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areas of anaplasia were found with up to 16 mitoses per 10 high-power fields. The Ki-67 labeling was
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approximately 29% and there was no pigmentation. Tumor cell staining was highly positive for vimentin
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and CD99, patchy for epithelial membrane antigen, scattered for BCL-2 and rare for CD34. A diagnosis
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of HPC/solitary fibrous tumor (SFT) WHO grade III with predominate HPC features was made.
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Post-operative Course and Follow-up
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The EVD was weaned over 12 days. Following surgery, the patient underwent radiation treatment,
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receiving 60 Gray (Gy) of local radiation over 30 fractions. Post-operatively, the patient had an initial
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worsening of his expressive aphasia that progressively improved before resolving prior to discharge. He
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experienced rapid resolution of his right hand weakness after surgery. His headaches improved
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substantially, fully resolving at follow-up, while his right homonymous hemianopia remained relatively
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unchanged post-operatively and at six-month follow-up.
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No evidence of recurrence or metastasis has been found at six-month follow-up scans, which include MRI
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of the neuraxis and positron emission tomography CT. Figure 5 represent the patient’s follow-up brain
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MRI.
96
Discussion
97
Interestingly, this is the second case of an intraventricular HPC treated at our institution with the prior
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being the first case of an intraventricular HPC described in the literature in 1957.3 The first case was
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treated with surgical resection via temporoparietal craniotomy resulting in gross total resection followed
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by 50 Gy of adjuvant local radiation. Tissue was sent to Dr. Arthur Purdy Stout, the surgeon and
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pathologist that originally coined the term HPC, who confirmed the diagnosis. The patient was followed
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for 21 years and died of unrelated causes. A post-mortem autopsy was performed with no evidence of
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HPC recurrence or metastasis.
104
On imaging, this solid mass was heterogeneously hyperdense on CT and isointense on T2 weighted MRI;
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it exhibited mixed intensity on T1 MRI and was heterogeneously enhancing post-gadolinium contrast.
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The differential diagnosis based on radiographic evaluation was broad and included meningioma, solitary
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fibrous tumor, high grade glioma, ependymoma, choroid plexus papilloma, and metastasis, particularly of
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renal cell carcinoma. According to one study, renal cell carcinoma involved intraventricular spread in
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37.5% percent of all patients who had brain metastasis compared to 0.8% for all other pathologies
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involving brain metastasis.14
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Grossly, HPC are soft, lobulated tumors. Microscopically, HPC are classically highly vascular, with an
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abundance of slit-like capillaries and pathognomonic clusters of dilated branching blood vessels that are
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characterized as a “staghorn” pattern. Prominent basal lamina, illustrated with reticulum or collagen IV
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stains, is also characteristic of HPC and helps differentiate them from meningiomas.
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Immunohistochemically, HPC often have focal CD34 positivity and are negative for epithelial membrane
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antigen (EMA); in comparison, meningiomas are generally negative for any CD34 and are positive for
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EMA. Intraventricular HPC are thought to originate from pericytes located in the tela choroidea of the
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stroma of the choroid plexus.5 Approximately 91% of intraventricular HPC are located in the lateral
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ventricles, likely because – similar to the propensity of intraventricular meningiomas to originate from the
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lateral ventricles – the choroid plexus is bulkier there compared to the third and fourth ventricles.15
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SFT are spindle cell neoplasms characterized by both hypocellular collagenic areas and hypercellular
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areas with HPC-like vasculature. Immunohistochemically, they are often strongly positive for CD34.16
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SFT were first described in 1996 by Carneiro et al.17 Outside of the CNS, HPC are now considered to be
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on the same neoplastic continuum as SFT.16 While the WHO still distinguishes between CNS HPC and
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SFT, Bouvier et al.18 argued in their retrospective comparison of CNS SFT and HPC that the two
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neoplasms are merely different histologic grades of the same neoplasm based on radiographic, pathologic,
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and prognostic similarities. Considering SFT and HPC as a common entity would add 18 cases of
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intraventricular lesions to the literature – 8 in the lateral ventricle, 1 in the foramina of Monro, 2 in the
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third ventricle, and 7 in the fourth ventricle.19,20 Of note, there appears to a relatively equal distribution of
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SFT between the infratentorial intraventricular system and the supratentorial intraventricular system. This
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is not the case with intraventricular tumors identified as HPC, which are predominantly supratentorial.
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The initial standard treatment of aggressive surgical resection is the same for both tumors, but only 10%
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of patients with intracranial SFT receive adjuvant radiation,19 whereas 35% of patients with intracranial
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HPC receive adjuvant radiation.21 Overall, when compared to HPC, SFT exhibit lower rates of
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malignancy (6%19 compared to 12-55%22), lower rates of recurrence (26% compared to as high as 90%22),
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and longer time to recurrence of 19 months.19,22 Microscopically, this particular patient’s tumor was
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predominantly consistent with HPC architecture.
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CNS HPC composes 0.4% of all intracranial neoplasms and 2-3% of all primary tumors of the dura.21
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HPC have no sex predilection. The majority (65%-76%) are located in the supratentorial compartment
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and the average age of diagnosis is 41.21-25 Intracranial HPC have a high incidence of recurrence ranging
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from 34% to 90% and a tendency to metastasize, ranging from 12% to 55%.22 The most common sites of
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metastasis, in order of decreasing frequency, are bone, lung, and liver.26 Average time to recurrence was
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64 months, with grade III neoplasms recurring at 59 months compared to 95 months in the grade II
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neoplasms.25 The mean survival is 13 years with 5- and 10-year survival estimates of 82% and 60%,
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respectively,21 and 10-year progression-free survival ranging from 29%10 to 39%.22 The largest single
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institution case series concerning CNS HPC comes from MD Anderson Cancer Center, which reviewed
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their experience treating 63 cases over a 30-year period.25
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Overall survival and progress-free survival are prolonged with complete surgical resection, which remains
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the major emphasis in treatment strategies. The rates of intracranial HPC GTR range from 38%-83%.22,23
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However the overall rate of GTR for intraventricular HPC is 91% despite their deep location and rarity;
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this is likely due in part to their lack of venous sinus involvement and relatively intact tumor capsule. The
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most common approaches to lateral ventricle HPC are the transcortical superior parietal lobule and
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transcortical middle temporal gyrus approaches. During surgical planning, it is especially important to
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consider risk to surrounding eloquent cortex, white matter tracts, and vascular supply to the tumor. A
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middle temporal gyrus approach requires traversing the least amount of cortex to reach tumors in the
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trigone of the lateral ventricle, as well as allowing for early control of anterior choroidal feeding vessels;
157
however, this operative course carries a higher risk for language or vision deficits. A superior parietal
158
lobule approach is safer when considering risk of damage to Wernicke’s area and traversing optic
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radiations; this method is more commonly utilized for dominant hemisphere lesions.27 Compared to
160
subtotal resection, GTR is associated with a significant increase in both overall survival, from 175 to 235
161
months, and recurrence-free survival, from 54 to 117 months.25 Patients receiving adjuvant radiation did
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not experience significant increase in overall survival,21 but did experience prolonged recurrence-free
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survival of 108 months, compared to 64 months in patients not receiving radiation therapy.24,25,29 Ideal
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dosage of adjuvant radiation has yet to be elucidated, with patients receiving >50 Gy having higher
165
mortality than patients receiving ≤50 Gy.21 However, patients receiving ≥60 Gy radiation had improved
166
local tumor control.24 There is no current role for chemotherapy in the treatment of intracranial HPC, but
167
it has been described in the treatment of peripheral metastatic HPC. Interestingly, neither gross total
168
resection nor adjuvant radiation appear to confer a significant benefit in prolonging time to development
169
of metastasis,22,28 which should further emphasize the need to maintain close follow-up and surveillance
170
of these patients with a high index of suspicion for metastatic potential even with successful local control.
171
While there is no consensus protocol for follow-up assessments of patient’s with these rare tumors, life-
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long follow-up is recommended, given their unpredictable and aggressive behavior. One proposed
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regimen includes close clinical follow-up, biannual or annual MRI of the brain and chest X-ray, with
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complaints of bone pain prompting more extensive work-up for metastasis.29 It would seem intuitive that
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given the aggressive natural history of intracranial HPC, intraventricular lesions would be prone to
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disseminating throughout the neuraxis via cerebrospinal fluid. However, the only case in which this has
177
been illustrated was in a 19 year old male who presented after his intraventricular HPC hemorrhaged.13
178
Five months after he underwent GTR and adjuvant local radiation, he developed widespread spinal
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metastasis, which likely were seeded from the initial tumor hemorrhage.13 While long term follow-up for
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patients with intraventricular HPC is sparse, 5 cases in the literature had follow-up > 1 year, with 2
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having follow-up >5 years and the longest being 21.5 years that all showed no evidence of local
182
recurrence or distant metastsis.3,8,10-12 Based on reports in the literature, intraventricular lesions do not
183
seem to require more aggressive adjuvant therapies, such as whole spine radiation. However, this could be
184
considered in cases where there is evidence of pre-operative hemorrhage or spinal metastasis.
185
Conclusions
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Intraventricular HPC are rare neoplasms in a rare location. Aggressive surgical resection with a goal for
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GTR should be the foundation of treatment for all HPC, regardless of location. The rate of GTR for
188
intraventricular HPC is higher than the reported rates for other intracranial HPC. The majority of cases
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reported in the literature pursue adjuvant radiation, though the role of radiation is not completely defined.
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Regardless of extent of resection or adjuvant treatment, close follow-up to evaluate for evidence of local
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recurrence and distant metastasis is essential.
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7. Al-Brahim N, Devilliers R, Provias J. Intraventricular hemangiopericytoma. Ann Diagn Pathol. 2004;8(6):347-351.
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13. Krajewski KL, Matschke J, Humke N, Börm W, Westphal M, Schmidt NO. A 19-year old male with an intraventricular tumor. Brain Pathol. 2015;25(5):657-658.
14. Shapira Y, Hadelsberg UP, Kanner AA, Ram Z, Roth J. The ventricular system and choroid plexus as a primary site for renal cell carcinoma metastasis. Acta Neurochir (Wien). 2014;156(8):1469-1474. 15. Bhatoe HS, Singh P, Dutta V. Intraventricular meningiomas: a clinicopathological study and review. Neurosurg Focus. 2006;20(3):E9.
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16. Park MS, Araujo DM. New insights into the hemangiopericytoma/solitary fibrous tumor spectrum of tumors. Curr Opin Oncol. 2009;21(4):327-331. 17. Carneiro SS, Scheithauer BW, Nascimento AG, Hirose T, Davis DH. Solitary fibrous tumor of the meninges: a lesion distinct from fibrous meningioma. A clinicopathologic and
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18. Bouvier C, Métellus P, de Paula AM, et al. Solitary fibrous tumors and hemangiopericytomas of
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21. Rutkowski MJ, Sughrue ME, Kane AJ, Aranda D, Mills SA, Barani IJ, Parsa AT. Predictors of
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mortality following treatment of intracranial hemangiopericytoma. J Neurosurg.
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22. Chen LF, Yang Y, Yu XG, Gui QP, Xu BN, Zhou DB. Multimodal treatment and management strategies for intracranial hemangiopericytoma. J Clin Neurosci. 2015:22(4):718-725.
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23. Damodaran O, Robbins P, Knuckey N, Bynevelt M, Wong G, Lee G. Primary intracranial
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haemangiopericytoma: Comparison of survival outcomes and metastatic potential in WHO grade
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24. Ghia AJ, Allen PK, Mahajan A, Penas-Prado M, McCutcheon IE, Brown PD. Intracranial hemangiopericytoma and the role of radiation therapy. Neurosurgery. 2013;72(2):203-209. 25. Melone AG, D'elia A, Santoro F, Salvati M, Delfini R, Cantore G, Santoro A. Intracranial hemangiopericytoma—our experience in 30 years: a series of 43 cases and review of the
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29. Guthrie BL, Ebersold MJ, Scheithauer BW, Shaw EG. Meningeal hemangiopericytoma: histopathological features, treatment, and long-term follow-up of 44 cases. Neurosurgery.
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1989;25(4):514-522.
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Figure 1. Non-contrast, axial head CT demonstrating a 6 x 5 x 5.5 cm heterogeneous, primarily
263
hyperdense solid appearing lesion located in the left lateral ventricle.
264 Figure 2. MRI sequences demonstrating a 6 x 5 x 5 cm mass in the trigone of the left lateral ventricle.
266
A. Sagittal T1 sequence showing heterogeneous signal intensity.
267
B. Axial T2 fluid-attenuated inversion recovery sequence of the mass showing homogenous signal that is
268
isointense to grey matter.
269
C. Axial T1-Cube post-contrast sequence showing heterogeneous enhancement of the mass.
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Figure 3. Post-operative non-contrast, axial head CT showing no residual tumor.
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Figure 4. HPC/SFT WHO grade III.
274
A. Hematoxylin and eosin staining showing hypercellular tumor with slit like vasculature (original
275
magnification 200x).
276
B. Reticulin staining highlighting blood vessels and pericellular reticulin (original magnification 400x).
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Figure 5. Post-operative axial T1-cube post-contrast MRI sequences demonstrating gross total resection
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of the left lateral ventricle HPC.
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ACCEPTED MANUSCRIPT Summary of cases of intraventricular HPC in the literature. Reference
Age
Location
/Se
Size
Approach
(cm)
Surgical
Adjuvant
Follow-
Presenting
Results
Radiotherapy
up
Symptoms/Pre-
x
op Deficits
55/
Trigone
Terry,
M
of R
Neurology, 1961
3.5
Transcortical
GTR
temporo-parietal
lateral
3
50 Gy of focal
No
L hemiparesis,
radiation over 7
evidence
L
days
ventricle
RI PT
McDonald,
of local
quadrantanopia,
recurrence jargon aphasia or
41/
Trigone
al, Neurol
M
of L
Transcortical
lateral
(Tokyo),
ventricle
4
40/
Third
1
et al, J
M
ventricle
Hattingen
43/
Trigone
et al,
F
of L
19995
Al-Brahim et al, Ann Diagn
years -
R upper
radiation over
extremity
30 fractions
paresthesia, HA, mild speech disturbance
GTR
ND
-
HA
Not described
GTR
ND
-
HA
Transcortical
GTR
ND
-
R temporal
EP
5
M AN U
Muttaqin et
SC
metastasis
ventricle
53/
Atrium
F
of R
4.5
temporo-parietal
visual field
lateral
Pathol,
constriction,
ventricle L hemiparesis,
20047
gait ataxia, Desai et al,
40/
Trigone
Neurol
M
of R
7
Transcortical superior parietal
GTR
60 Gy of local
No local
L homonymous
radiation over
recurrence hemianopia, HA
ACCEPTED MANUSCRIPT Med. Chir
lateral
(Tokyo),
ventricle
2004
30 fractions
metastasis
8
Bunai et al,
or
at 1 year 9/M
Am J
R lateral
0.5
NP
NP
NP
5
Transcortical
GTR
NP
-
HA
ventricle
Med Pathol,
31/
Trigone
al, Neurol
F
of R
middle temporal
Med Chir
lateral
gyrus
(Tokyo),
ventricle
200910 Sumi et al,
65/
Body of
Acta
F
bilateral
Neurochir
lateral
(Wien),
ventricles
5
Anterior
transcallosal
67/
Trigone
al, Neurol
F
of L lateral
(Tokyo),
ventricle
12
Krajewski et al, Brain Pathol, 2015
19/
R lateral
ND
AC C
2011
M
Transcortical
ventricle
GTR
L upper
recurrence quadrantanopia, blurred vision,
metastasis
L 6th nerve
at 4 years
palsy, HA
55 Gy of local
No local
Gait disturbance
radiation
recurrence
NP
at 5 years
No local
R
inferior
recurrence quadrantanopia,
temporal gyrus
or
R hemiparesis,
metastasis
motor aphasia,
EP
Med Chir
6
TE D
201011 Tanaka et
GTR
No local
or
M AN U
Suzuki et
SC
20089
RI PT
Forensic
Transcortical
at 2 years GTR
Fractionated
Death 5
L hemiparesis,
temporo-parieto-
radiation –
months
HA, nausea
occipital
radiation dose
post-op
ND
with widesprea d spinal metastasis
Present
23/
Trigone
case, 2015
M
of L lateral
6
Transcortical parieto-occipital
GTR
60 Gy of local
No local
R homonymous
radiation over
recurrence hemianopia,
30 fractions
or
word finding
ACCEPTED MANUSCRIPT ventricle
metastasis
difficulty,
at 9 months
R paresthesia, HA
AC C
EP
TE D
M AN U
SC
RI PT
GTR, gross total resection; HA, headache; L, left; ND, not described; NP, not performed; R, right; STR, subtotal resection.
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
ACCEPTED MANUSCRIPT
ACCEPTED MANUSCRIPT
EP
TE D
M AN U
SC
RI PT
Intraventricular hemangiopericytomas originate from tela choroidea pericytes. Hemangiopericytomas are rarely located intraventricularly. Aggressive surgical resection is the primary treatment modality. The role of adjuvant radiation is not completely defined, but it is often pursued. Close monitoring for local recurrence and distant metastasis is imperative.
AC C
• • • • •