Distant metastasis of intracranial solitary fibrous tumor preceding resection: illustrative case

Abstract

BACKGROUND

Postsurgical distant metastasis of intracranial solitary fibrous tumors (ISFTs) is not uncommon and often leads to poor prognosis. However, presurgical distant metastasis has not been previously reported.

OBSERVATIONS

This case details a male patient who presented with seizures at age 26 years. Diagnosed with a space-occupying lesion in the right temporal lobe, suspected to be a meningioma, he underwent Gamma Knife treatment. Seven years later, MRI revealed slight growth of the lesion, leading to another Gamma Knife procedure. At age 40 years, the patient developed a tumor on the left chest wall, requiring total resection and rib reconstruction. Pathology confirmed it was a solitary fibrous tumor. At age 41 years, he experienced headaches and epilepsy, with MRI showing an enlarged lesion in the right temporal lobe with peritumoral edema, necessitating surgery. Pathological analysis confirmed an ISFT.

LESSONS

ISFTs can metastasize distantly over time, even without surgery. Differentiating ISFT from meningioma via imaging is challenging. Therefore, Gamma Knife treatment without definitive pathological diagnosis requires careful follow-up, monitoring both the intracranial tumor and peripheral organs for potential metastasis.

https://thejns.org/doi/10.3171/CASE24846

The intracranial solitary fibrous tumor (ISFT), originating from meningeal mesenchyme, is a rare neoplasm with a low incidence, representing just 0.4% of primary CNS tumors.¹ This malignancy is primarily treated through surgical intervention, but it often recurs postoperatively and frequently leads to extracranial distant metastasis after several recurrences, significantly impacting patient prognosis.^2,–,4 Notably, there are no reported cases of extracranial metastasis in patients with ISFT who underwent radiotherapy as the sole treatment without surgery. Here, we present a unique case of chest wall metastasis from an ISFT that occurred 14 years after Gamma Knife therapy at our institution. We discuss this case in conjunction with relevant literature.

Illustrative Case

The patient, a male, experienced seizures at the age of 26 years in 2003. Cranial MRI revealed a lesion occupying the right temporal space, which was approximately 2.2 × 2.1 cm in size (unfortunately, the image data were lost). Given the possibility of a meningioma, surgical intervention was recommended. However, the patient expressed concern about the risks associated with craniotomy and opted for Gamma Knife treatment instead. Following the Gamma Knife procedure, the patient was prescribed oral valproate sustained-release tablets, taken twice daily, resulting in no further seizures or symptoms of high intracranial pressure.

Seven years later, in 2010, at the age of 33 years, the patient underwent a cranial MRI reexamination, which revealed that the tumor had grown slightly larger than before. Consequently, he underwent Gamma Knife treatment once again.

Fourteen years later, in 2017, when the patient reached the age of 40 years, he discovered a mass on his left chest wall accompanied by localized pain and gradual enlargement. As a result, he sought treatment at the Department of Thoracic Surgery in our hospital. Chest CT imaging revealed a space-occupying lesion on the left anterior chest wall (Fig. 1A–C). Consequently, a left chest wall tumor resection was performed, followed by a 3D-printed rib reconstruction. The surgery was a success, and the patient made a full recovery before being discharged. Subsequent chest wall CT imaging confirmed the complete removal of the tumor and the intact reconstruction of the chest wall (Fig. 1D and E). The pathological examination revealed a grade 2 solitary fibrous tumor (SFT) in the left chest wall, exhibiting highly active cell proliferation in certain regions (Fig. 1F).

FIG. 1.

A–C: Chest CT scans revealing a space-occupying lesion on the left anterior chest wall. D and E: Postoperative chest CT scans showing that the tumor was completely removed. F: The pathological examination revealed a grade 2 SFT in the left chest wall, exhibiting highly active cell proliferation in certain regions. H&E, original magnification ×400.

Fifteen years after, in 2018, when the patient was 41 years of age, he presented to the Department of Neurosurgery with primary complaints of paroxysmal epilepsy, headache accompanied by nausea, and vomiting persisting for 1 month. A cranial MR examination revealed that the lesion area had expanded beyond its previous size following Gamma Knife treatment for the right temporal lobe tumor, and it was now accompanied by peritumoral edema (Fig. 2A–C). Given that 15 years had passed since the lesion was first detected and treated with Gamma Knife therapy, and despite the current imaging results not aligning with typical meningioma characteristics, we maintained that this represented the long-term outcome of Gamma Knife treatment. Furthermore, we continued to hold the belief that the lesion was possibly a meningioma. Consequently, a right temporal lobe tumor resection was completely executed, and the surgery was a success with favorable recovery (Fig. 2D and E). The pathological examination indicated a WHO grade 2 ISFT, with notable active cell proliferation (Fig. 2F).

FIG. 2.

A: Axial cranial CT scan showing a neoplastic lesion in the right temporal lobe with peritumoral edema. B and C: Axial cranial MR images revealing that the lesion area had expanded beyond its previous size following Gamma Knife treatment for the right temporal lobe tumor. D and E: Axial cranial CT scan (D) and MR image (E) showing that there was no residual tumor in the right temporal lobe after tumor resection. F: The pathological examination indicated a WHO grade 2 ISFT. H&E, original magnification ×400.

Seventeen years later, in 2020, when the patient was 43 years of age, he presented to our hospital with a 1-month history of lumbar pain. Lumbar spine MRI was performed and revealed alterations in the L4 lumbar vertebrae, suggestive of metastasis (Fig. 3A and B). An abdominal CT scan further indicated multiple abnormal signal shadows in the liver, also suggestive of metastasis (Fig. 3C and D). A biopsy of the liver lesions was subsequently conducted, and the pathological examination confirmed the presence of an SFT, leading to the consideration of multiple metastases of SFT (Fig. 3E). The patient underwent radiotherapy for both lumbar and liver metastases, followed by three courses of systemic chemotherapy with ifosfamide and epirubicin. Afterward, the patient was prescribed targeted drug therapy with anlotinib hydrochloride capsules at a daily dosage of 12 mg for oral administration.

FIG. 3.

A and B: Sagital lumbar spine CT scan and MR image revealing alterations in the L4 lumbar vertebrae, suggestive of metastasis. C and D: Abdominal CT scans further indicating multiple abnormal signal shadows in the liver, also suggestive of metastasis. E: A biopsy of the liver lesions was subsequently conducted, and the pathological examination confirmed the presence of a solitary fibrous tumor. H&E, original magnification ×400. F–H: With aggressive treatment, the metastatic lesions in the liver, pancreas, and lumbar spine appeared smaller than previously observed.

After 21 years, in 2024, the patient, who was now 47 years of age, exhibited an acceptable general condition with a Karnofsky Performance Status score of 90. On reexamination, head MRI did not indicate any tumor recurrence. Additionally, the metastatic lesions in the liver, pancreas, and lumbar spine appeared smaller than previously observed (Fig. 3F–H). Presently, the patient continues to undergo targeted drug therapy and remains under medical follow-up.

Informed Consent

The necessary informed consent was obtained in this study.

Discussion

Observations

Currently, there are numerous reports discussing ISFT, a disease recognized for its recurrence and risk of distant metastasis, as agreed on in various studies.^2,–,4 Typically, cases involve the initial discovery of intracranial space-occupying lesions, followed by surgical intervention to establish a pathological diagnosis. Many patients experience multiple recurrences of intracranial tumors, often culminating in distant extracranial metastasis in the later stages of the illness after undergoing repeated surgeries. This late-stage development signifies a poor prognosis and can even lead to the patient’s death.^2–5

In the presented case, the patient opted for Gamma Knife radiation therapy instead of surgery on initial discovery of intracranial lesions. Fourteen years later, a chest wall lesion was identified and surgically removed, histologically confirmed as SFT. A year after that, an increase in size of the intracranial lesion was observed, necessitating surgical intervention. Pathological analysis once again confirmed SFT. Given that both lesions originated from the same pathological results, we postulate that the chest wall lesion is a metastatic tumor from the ISFT. This case marks the first reported instance of ISFT metastasizing before any surgical intervention.

SFTs often recur after surgical intervention. In this case, the patient’s chest wall lesions were entirely excised, involving the removal of adjacent chest wall muscles and ribs, followed by a 3D-printed rib reconstruction. Postoperatively, local radiotherapy was not administered. Seven years later, there has been no local recurrence observed. Despite two previous Gamma Knife radiotherapy treatments for intracranial lesions and their complete removal during surgery, there has been no recurrence in the 6 years since the procedure. However, during postoperative follow-ups, multiple metastases were detected in the patient’s liver and lumbar vertebrae. The patient underwent radiotherapy, systemic chemotherapy, and targeted drug therapy, resulting in lesion shrinkage and disease stabilization. Currently, there is no recurrence of intracranial or chest wall tumors, and intrahepatic and bone metastases remain stable. We advocate for radiotherapy to control the recurrence of primary lesions and the growth of metastatic lesions following total resection. If recurrence trends are observed, radiotherapy can be repeated.^2,6,7 It is crucial to monitor for distant metastases throughout the body. On detecting metastatic lesions, small lesions can be managed with radiotherapy combined with systemic chemotherapy. For larger lesions, surgical removal followed by local radiotherapy and systemic chemotherapy is recommended.^2,3,8 Common chemotherapy drugs include temozolomide, bevacizumab, and anlotinib.^2,3,8–10

Currently, it is widely accepted that ISFT can develop distant metastasis, independent of its pathological grade.^5,11 However, studies suggest that high-grade ISFT carries a greater risk of metastasis.⁵ As the tumor progresses, its malignancy increases,¹² thereby elevating the risk of metastasis. Some experts postulate that the distant metastasis of ISFT is linked to the invasion of brain parenchyma, bone, soft tissue, or adjacent dural sinus by SFT.¹³ However, this patient’s tumor did not show these features, and extracranial metastasis still occurred. This underscores that ISFT is a potentially malignant tumor. Therefore, it is imperative to remain vigilant for local recurrence and peripheral metastasis, and to perform whole-body PET-CT scans when necessary to detect any distant metastasis.¹⁴

ISFT is prone to recurrence, and most patients develop distant metastasis following multiple recurrences and surgical interventions on the primary lesion.^2–5 Currently, there are three potential routes of extracranial metastasis documented in the literature:¹⁵ direct extension, lymphatic metastasis, and the most common, hematogenous pathway. All reported cases of distant ISFT metastases in the literature have occurred postoperatively, predominantly after multiple recurrent surgeries. This may be attributed to the shedding of tumor cells during surgery or the dissemination of tumor cells via blood, lymph, and CSF, leading to distant metastasis. This report presents the first instance of extracranial metastasis arising after conservative treatment. It is advisable that, on detecting intracranial space-occupying lesions where preoperative imaging cannot differentiate between meningioma and ISFT, close attention should be paid to follow-up if radiotherapy is administered. Besides monitoring the status of intracranial primary lesions, it is also crucial to observe the condition of peripheral organs, as these patients are susceptible to ISFT with peripheral organ metastasis. In the event of detecting peripheral neoplastic lesions, the possibility of extracranial metastasis from intracranial lesions should be considered.

The shortest reported time for distant metastasis in ISFT is 3 months postoperation,² whereas the longest is 372 months.¹⁶ The mean time stands at 91.33 ± 12.66 months.¹⁷ However, this patient did not undergo surgical treatment after discovery of the ISFT and received radiotherapy directly. It took 168 months from the initial lesion detection to distant metastasis. We speculate that the time of disease onset is a key factor affecting distant metastasis of the disease. With extension of the course of the disease, there is a possibility of systemic distant metastasis, regardless of whether surgical treatment is performed or not. The occurrence of distant metastasis signifies the terminal stage of the illness, elevating treatment complexity and considerably diminishing patient survival time.¹⁸

Lessons

Despite not undergoing surgical treatment, ISFTs may still exhibit extracranial distant metastasis. When performing preoperative imaging diagnosis for brain tumors, such as meningiomas and ISTF, and if Gamma Knife treatment is being considered, it is crucial to not only closely monitor intracranial lesions but also carefully observe the metastasis of peripheral organs.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: all authors. Acquisition of data: Yang, Li. Analysis and interpretation of data: Yang, Wang, Li. Drafting the article: Zhou, Wang, Feng, Li. Critically revising the article: Zhou, Feng, Li. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Yang. Statistical analysis: Li. Administrative/technical/material support: Zhou, Li. Study supervision: Yang, Zhou, Li.

Correspondence

Di Yang: Tangdu Hospital, Air Force Medical University, Baqiao District, Xi’an, Shanxi, China. yangdimed@163.com.