Aggressive regrowth and parenchymal invasion following multiple subtotal resection of giant calvarial hemangioma: A rare complication

Abstract

Background:

Skull hemangioma is a rare benign bone tumor, arises from the diploic vessels, and exhibits outward growth pattern, usually sparing the inner table. This is the world’s first report of it’s kind to exhibit aggressive growth pattern of hemangioma following subtotal resection, subsequently invades the brain parenchyma, and leads to catastrophic outcome.

Case Description:

This 25-year-old gentleman presented with progressive enlargement of a painless scalp swelling within a period of 8 years. Computed tomography scan of brain demonstrated a giant, sclerosed, cauliflower like swelling, having “sunburst pattern” involving fronto-temporo-parietal region. Magnetic resonance imaging showed mixed intensity in both T1- and T2-weighted images with “spoke wheel” appearance. He then underwent subtotal resection for 3 times within a period of 2 years. However, due to rapid aggressive growth involving major part of the calvaria and right orbit, patient party refused to undergo further intervention. He became bed bound and died 6 months after 3^rd resection.

Conclusion:

This case highlighted the aggressive and invasive clinical course of a benign lesion following subtotal resection. Surgery may play a role in tumor dedifferentiation to more aggressive form; therefore, gross total resection should be attempted in the earlier stage of the disease.

INTRODUCTION

Cavernous hemangiomas of the skull represent a rare pathological finding, making up 0.2% of bone tumors and 7% of skull tumors.[1,2,6] These lesions are commonly encountered in fourth to fifth decade of life with slight female predominance. Typically, these benign vascular lesions arise from the diploic vessels, affect frontal and parietal bone, and exclusively fed by the branches of external carotid artery.[11] Radiologically, the appearance of sunburst pattern supports the diagnosis. Although the classic pattern involves the diploic space and outer table of the skull, they can rarely breach the inner table and exhibit intradural extension.[10,11] As a benign lesion, complete surgical resection is regarded as curative.[6,10,11] This report discusses an unusual case of a cavernous hemangioma located in the fronto-parietal bone, who underwent multiple subtotal resections over 2 years and later exhibited an aggressive clinical progression, involving extensive bone involvement of bilateral calvarium, orbit followed by invasion of brain parenchyma. To the best of our knowledge, this is the largest aggressive and invasive calvarial hemangioma ever documented in the English literature, that goes against it’s benign nature. This case underscores the potential for an aggressive progression of this uncommon benign lesion which warrants further research in this field.

CASE REPORT

History and physical examination

A 25-year-old right-handed male was admitted in February 2020 with a progressive enlargement of a non-tender scalp swelling that had been present for 8 years. The swelling initially was the size of a peanut but gradually increased to its current size. Due to the cosmetic deformity and a sensation of heaviness in his head, he sought medical attention. On local examination, there was a large non-tender, bony-hard swelling in the right fronto-temporo-parietal region, accompanied by superficially engorged scalp veins [Figure 1]. There were no signs of focal neurological deficits, and the systemic examination results were unremarkable.

Figure 1:

(a and b) Photograph of the patient demonstrated a huge scalp swelling of right frontotemporo-parietooccipital region with superficial engorged scalp veins, before ungoing elective surgery. (c) Photograph taken after 3^rd time subtotal decompression.

Neuroimaging

Preoperative computed tomography (CT) imaging of the brain in axial section revealed a mostly sclerotic extracranial mass located in the right fronto-parietal region, displayed the characteristic “sunburst pattern” radiating from the parietal bone [Figures 2a and b]. The 3D reconstruction exhibited a “popcorn appearance” that had already crossed the midline, affecting the opposite fronto-parietal bone while leaving the orbit intact [Figure 2c]. CT angiogram demonstrated that the lesion was fed by both superficial temporal artery and occipital artery [Figure 2d]. Magnetic resonance imaging (MRI) of brain, T1-weighted image axial section demonstrated a giant extracalvarial, heterogeneously hypointense lesion and patchy islands of hyperintense area involving the hemicranium with contralateral extension [Figure 3a]. The lesion become heterogeneously hyperintense, having sunburst pattern in T2WI [Figure 3b]. After administration of the contrast, there was heterogenous honeycomb-like enhancement, evident in axial section, and spoke wheel appearance sagittal section [Figures 3c and d].

Figure 2:

Preoperative computed tomography (CT) scan of brain, (a) axial section demonstrated a predominantly sclerotic extracranial lesion located in right fronto-parietal region. (b) Bone window sequence demonstrated classic “sunburst pattern” emerging from the parietal bone. (c) 3D reconstruction is consisting with “pop-corn appearance” which already crossed the midline involving contralateral frontoparietal bone, sparing the orbit. (d) CT angiography showing predominant feeding vessel from superficial temporal artery (marked by blue arrowhead) with an anastomotic twig from occipital artery (marked by orange arrowhead.

Figure 3:

Magnetic resonance imaging of brain, (a) TI-weighted axial section demonstrated a giant extracalvarial, heterogeneously hypointense lesion and patchy islands of hyperintense area involving the hemicranium with contralateral extension. (b) The lesion becomes heterogeneously hyperintense, having sunburst pattern in T2-weighted. (c) After administration of the contrast, there was heterogenous honeycomb-like enhancement, evident in axial section and (d) spoke wheel appearance sagittal section.

Surgical procedure and follow-up

Before undergoing definitive surgical procedure, digital subtraction angiogram followed by preoperative embolization of the feeding arteries planned to minimize intraoperative hemorrhage. However, due to financial constraint, patient party refused to undergo embolization procedure and consented for surgical management only. Considering the size and extension of the lesion, it was impossible to remove the lesion as en bloc. Therefore, staged surgical resection with adjuvant radiotherapy planned. On March 2020, he underwent partial decompression of the tumor. The tumor appeared reddish, sclerosed with massive bleeding from the resected zone [Figure 4]. Due to excessive intraoperative bleeding (approximately 2,000 mL) and extension of the pathology, gross total removal could not be possible. Patient tolerated the procedure well and discharged in 5^th postoperative day. Due to rapid enlargement of the lesion with progressive involvement of orbit, he additionally underwent subtotal resection for 2 times in 2021. During resection, there were approximately 2,000 mL and 2,400 mL intraoperative blood loss in 2^nd and 3^rd resection, highlighting the surgical challenge for attempting maximum resection. Sequential follow-up CT scans taken at 6 months [Figure 5a], 1 year [Figure 5b], 1.5 years [Figure 5c], and 2 years [Figure 5d] demonstrated significant growth of the hemangioma, even after three subtotal resections. However, in January 2022, patient developed convulsion and hemiparesis, therefore again admitted into our hospital for further evaluation and definitive management. The most recent CT scan in coronal view revealed an aggressive and invasive growth pattern, infiltration through the inner table and considerable intracranial extension along with invasion of the brain tissue with contralateral midline shifting. In addition, multiple dispersed hypodense regions were observed on the same side, indicating ischemic changes [Figure 5d]. Patient deemed inoperable and referred to oncologist for further management. Due to possibility of non-favorable outcome and economic constraint, patient party refused for further management. In April 2022, he became bed bound and expired thereafter within a month.

Figure 4:

Intraoperative photograph demonstrated (a) gross appearance of the tumor after elevating skin flap, (b) after subtotal decompression, and (c) sample preparation for histopathology and immunohistochemistry.

Figure 5:

Sequential follow up CT scan at at (a) 6 months, (b) 1 year, (c) 1.5 year and (d) 2 years showed aggressive growth of the hemangioma, despite of subtotal resection for 3 times. (a) Patient had no involvement in the orbital region (marked by blue arrowhead), whereas (c) 1.5 years follow up CT scan demonstrated involvement of right orbit and ipsilateral zygomatic bone (marked by red arrowhead). (d) Last CT scan, coronal section demonstrated an aggressive and invasive growth pattern, breaching the inner table with significant intracranial extension and parenchymal involvement (scattered bony ingrowth and invasion marked by orange arrow). Multiple scattered hypodense areas are also noted in the same side, signifies ischemic change (marked by blue arrow).

Histopathology and immunohistochemistry (IHC)

IHC result of the resected specimen showed positive for Vimentin, CD34 in blood vessels. Pancytokeratin (AE1/AE3) and CD31 were focally positive in tumor cells. Beside this, tumor cells were negative for S-100 and EMA. IHC features were consistent with hemangioma.

DISCUSSION

Calvarial cavernous hemangiomas are benign vascular lesion, which arise from the diploic vessel that classically exhibits outward growth pattern with relative sparing of the inner table.[6,11] Rarely, they can grow in both direction to involve the inner table, preserving the dura matter.[10,11] In contrast to this classic behavior, our patient exhibited rapid, aggressive regrowth after repeated subtotal resections, with eventual erosion of the inner table and frank parenchymal invasion, which is an atypical and catastrophic course for a lesion usually regarded as benign. This divergence from the expected biology indicates that incomplete resection may, in select circumstances, precede accelerated growth and intracranial extension. Previously reported atypical cases of dural extension/invasion are summarized and presented in Table 1.

Table 1:

Reported cases of skull hemangioma with dural extension/invasion till date.

Uemura et al. described a patient with a calvarial cavernous hemangioma who presented with an epidural hemorrhage in which the inner table was completely eroded and the lesion was in direct contact with intact dura mater.[10] Till now, a very few report documented dural infiltration and intradural extension of the tumor.[1,5] Khanam et al. reported a right sphenoid wing hemangioma with involvement of adjacent dura whereas Gottfried et al. presented a case of a 50-year-old man in whom a symptomatic subdural hematoma resulting from a cavernous hemangioma of the calvaria.

During surgery, the dura mater was observed to be eroded, just adjacent to the skull hemangioma.[1,5] Another case of dural adhesion was described by Nasi et al. in a 5-month-old girl who exhibited rapid enlargement of an occipital hemangioma within a period of 3 months.[7] The atypical presentation of our case consists in the extensive involvement of the bilateral calvarium and orbit with aggressive inward growth pattern invading the brain parenchyma.

Calvarial hemangiomas are usually presented as small asymptomatic lesion. However, enlargement and involvement of neurovascular structures can lead to focal neurological deficit depending on the location.[1,2,5,7,9,10] The classic appearance of a hemangioma on radiographs are a “honeycomb” pattern, denoting rounded area of rarefaction.[3] This pattern can be also appreciated on bone windows of a CT scan. Our reported case also exhibit “popcorn appearance” in 3D reconstruction, which denote it’s sclerosing nature. This atypical imaging presentation is also a new observation that can be a valuable addition to our existing literature. Enhancement with contrast material is intense on both CT and MRI. On MRI imaging, these lesions show an intermediate to high T1 signal intensity and a high, heterogeneous T2 signal intensity.[3,9] The classic “sunburst pattern” and “spoke wheel appearance” are also well demonstrated in our reported case. Sometimes, the classic radiographic appearances are not evident; therefore, diagnosis should be established only after histopathology and IHC.

Complete surgical resection, followed by cranioplasty, is considered gold standard to treat this benign lesion. To prevent recurrence, removal of the lesion plus a 1-cm-wide margin of uninvolved bone is always recommended. This method allows the removal of the tumor intact, obviating the risk of significant bleeding because the sinusoids are undisturbed. Alternative therapies used for the treatment of cranial hemangiomas include surgical percutaneous embolization, curettage, and radiotherapy.[3,8] Our imaging at later follow-up showed intraparenchymal invasion with contralateral midline shift and scattered hypodensities consistent with ischemic changes – findings that may reflect a “steal” phenomenon after acquisition of pial supply. While true dedifferentiation or sarcomatous transformation cannot be concluded from a single case, the clinical trajectory warrants caution and further study of biological drivers in incompletely resected calvarial hemangiomas. Resource constraints precluded embolization and detailed venous mapping. Across three subtotal procedures, blood losses were substantial (approximately 2,000 mL and 2,400 mL during the second and third operations), and gross total resection (GTR) was not feasible given the size and extent. This experience reinforces two practical lessons: (i) where feasible, early GTR before circumferential calvarial spread may prevent a progression to inoperability; and (ii) when GTR is not initially feasible, preoperative embolization and meticulous venous assessment (Magnetic resonance venogram [MRV]/Digital subtraction angiogram [DSA]) are critical adjuncts to mitigate bleeding risk and guide staged planning.

Curettage is associated with an increased risk of hemorrhage and recurrence, since residual tumor can be left behind, therefore not recommended in giant aggressive lesion. Radiotherapy, typically used when resection is not possible, has been shown to decrease the size of hemangiomas, but not reduce the risk of hemorrhage and is associated with radiation induced carcinoma.[3,8] However, in our reported case, considering the initial extensive involvement of bilateral calvarial bone, gross total resection was not possible. Therefore, we had planned for staged surgical resection with intermittent radiotherapy.

Despite of multiple subtotal resection, the tumor demonstrated rapid aggressive growth pattern and invade the brain parenchyma leads to significant mass effect. Beside this, multiple scattered hypodense ischemic areas noted which was believed to be due to acquisition of the pial feeders and consequently lead to steal phenomenon. In our patient, adjuvant radiotherapy had been considered within a staged plan, yet continued aggressive growth and subsequent intracranial invasion ultimately rendered the lesion inoperable. These observations align with the principle that adjuvant measures should be individualized and, when used, coupled with rigorous surveillance for early detection of inward progression.

On the basis of this report, neurosurgeon must be aware on the possibility of an aggressive course of this rare benign pathology and possibility of sarcomatous transformation, warranting further research in this field. Based on the literature and our experience, we advocate (1) early definitive resection with osseous margin when the lesion is still localized; (2) preoperative angiography with selective embolization for giant or highly vascular tumors; (3) systematic evaluation of venous sinuses and emissary veins; (4) avoidance of piecemeal subtotal debulking when a safe path to GTR exists; and (5) close postoperative imaging surveillance to detect early signs of inward progression. We summarize these steps in a pragmatic treatment algorithm [Figure 6] to support decision-making in complex, atypical presentations.

Figure 6:

Recommended treatment algorithm of the giant skull hemangioma, based on previously published cases and Author’s own experience.

Limitation of the study

This is a single-patient experience with resource limitations that affected imaging and embolization options, and causal inferences regarding subtotal resection and acceleration of growth cannot be definitively established. Due to economic constraint of the patient party, we could not go for preoperative DSA, followed by embolization which would be beneficial to devascularize this giant tumor and would facilitate total resection during 1^st surgery. Furthermore, we did not go for MRV despite of contralateral fronto-parietal extension of tumor. Our limited assessment and denial of the patient party to undergo embolization leads to repeated subtotal resection, followed by aggressive regrowth of this tumor resulting in non-favorable neurological outcome. Based on our experience and previously published atypical cases of skull hemangioma, we have recommended a treatment algorithm [Figure 6]. Future work should explore molecular and angiogenic profiles of residual calvarial hemangiomas after partial resection, including potential genetic determinants of aggressive behavior, and evaluate standardized pathways that integrate embolization and venous mapping into staged curative strategies.

Learning points

1. Giant intraosseous sclerosing hemangioma can demonstrate “popcorn appearance” in 3D bone reconstruction sequence of CT scan

2. Preoperative embolization should be considered in giant calvarial hemangioma with identifiable feeding vessels before ongoing definitive surgery

3. Subtotal resection can lead to aggressive and invasive disease course, invading the brain parenchyma which goes against their classic growth pattern.

4. Further research warrants genetic analysis to demonstrate the reason of their changing biological behavior.

CONCLUSION

Subtotal resection should be avoided as it acts as triggering factor for the rapid growth of the lesion which might lead to inoperable stage and consequently worst outcome.

Ethical approval:

The Institutional Review Board approval is not required.

Declaration of patient consent:

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship:

Nil.

Conflicts of interest:

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation:

The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.

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