|Year : 2022 | Volume
| Issue : 3 | Page : 820-826
Intracranial hemorrhages associated with meningiomas: Own experience and literature review
Zygmunt Siedlecki, Karol Nowak, Sebastian Grzyb, Maciej Śniegocki
Department of Neurosurgery and Neurotraumatology and Pediatric Neurosurgery, Collegium Medicum in Bydgoszcz of Nicolaus Copernicus University in Toruń, Toruń, Poland
|Date of Submission||11-Jul-2020|
|Date of Decision||29-Aug-2020|
|Date of Acceptance||21-Dec-2020|
|Date of Web Publication||25-Jul-2022|
Department of Neurosurgery, Neurotraumatology and Pediatric Neurosurgery, the Ludwik Rydygier Collegium Medicum in Bydgoszcz, The Nicolaus Copernicus University in Toruń, Toruń
Source of Support: None, Conflict of Interest: None
Intracranial hemorrhage associated with meningioma is rare. Relatively, few such cases are described in the source literature, and it is estimated that intracranial meningiomas presenting with hemorrhage account for about one percent of all meningiomas. Hemorrhage can occur in both meningioma tissue and on the tumor surface. It can lead to intracerebral, subdural and subarachnoid hematoma. This can in turn cause high intracranial pressure with rapid neurological deterioration. Urgent neurosurgical intervention is often necessary. In our department, three patients with meningioma-related hemorrhage were treated surgically from 2006 to 2020. One patient was operated on as an emergency, due to the patient's poor neurological condition, while the two others underwent surgery following supplementary diagnosis several days following their admission. The outcomes of the three patients were good. The three meningiomas associated with hemorrhage described in the present manuscript constitute 2.2% of all 136 meningiomas treated surgically from 2006 to 2020 at our department. All three hemorrhages described in this study were associated with WHO I convexity meningiomas. Similar data can be found in some sources also describing meningioma WHO I-related hemorrhages; nevertheless, other literature references indicate a higher risk of bleeding into meningiomas of a higher degree of malignancy. The hemorrhage mechanism remains unclear; however, the proposed mechanism is rupture of defective intratumoral blood vessels and stretching of the superficial veins including bridge veins by the growing tumor, leading to their rupture. Our observations regarding the incidence of meningioma hemorrhage and tumor location are consistent with the source literature data.
Keywords: Hemorrhage, meningioma, neurological state, neurosurgical treatment
|How to cite this article:|
Siedlecki Z, Nowak K, Grzyb S, Śniegocki M. Intracranial hemorrhages associated with meningiomas: Own experience and literature review. J Can Res Ther 2022;18:820-6
|How to cite this URL:|
Siedlecki Z, Nowak K, Grzyb S, Śniegocki M. Intracranial hemorrhages associated with meningiomas: Own experience and literature review. J Can Res Ther [serial online] 2022 [cited 2022 Sep 25];18:820-6. Available from: https://www.cancerjournal.net/text.asp?2022/18/3/820/348234
| > Introduction|| |
Intracranial hemorrhage in patients with meningioma is rare. It is reported that meningioma-associated hemorrhage occurs at the incidence of 0.5%–2.3% of all meningiomas., Intracranial hemorrhage associated with brain tumors is more common in malignant tumors. It is reported that hemorrhage associated with glioblastoma occurs approximately in seven percent of the cases of this tumor and in up to 30% of all patients with anaplastic oligoastrocytoma. For metastatic tumors, according to some reports, the percentage of tumors that manifest with hemorrhage may reach 50%. The highest rates of hemorrhage in metastatic tumors are reported for thyroid papillary and hepatocellular carcinomas. By contrast, tumors of low malignancy due to low dissemination of pathological blood vessels are characterized by a significantly lower percentage of hemorrhages. However, the higher incidence of hemorrhage from pituitary adenomas and pilocytic astrocytomas was reported as statistically significant.,, Although meningiomas are slow-growing and potentially highly vascularized, spontaneous hemorrhage in meningiomas is a rare event. Bleeding associated with meningiomas can occur inside the meningioma tissue and leads to intratumoral hemorrhage (ITH). Bleeding can also occur on the tumor surface and can lead to intracerebral hemorrhage (ICH), subdural hematoma (SDH) and subarachnoid hemorrhage (SAH). All such bleeding, regardless of its location, can cause high intracranial pressure with rapid neurological deterioration. Risk factors for meningioma-associated bleeding include age of more than 70 and <30, meningioma located in the convexity and within the ventricle., The risk of bleeding is also increased by coagulation disorders, hypertension, anticoagulant therapy, as well as fibrous and angioblastic histopathology of the meningioma. The proposed mechanism of hemorrhage is due to rupture of blood vessels during their dissemination in tumor angiogenesis. New blood vessels emerging inside the tumor are defective, and they have thin and fragile walls. For this reason, there is an increased risk of their rupture and hemorrhage. Another proposed mechanism is that of stretching the superficial cerebral veins and bridge veins by a growing tumor, leading to rupture of the veins, which most often leads to acute SDH. Despite published data from the literature, the mechanism of bleeding into meningiomas remains unclear.
Patients with meningioma-associated hemorrhages can present a variety of neurological conditions from good to severe, depending on the intracranial pressure and the extent of the hemorrhage. Focal neurological deficit and Glasgow Coma Scale (GCS) are assessed in these patients. The management of patients depends on their clinical state. Imaging diagnostics is computed tomography (CT) imaging with high sensitivity to intracranial bleeding. If urgent surgical treatment is required, CT is the basis for qualifying the patient for surgery. However, if the patient's condition is relatively good, then diagnostics is expanded to magnetic resonance imaging (MRI). MRI is the study of choice in the diagnosis of brain tumors.
Hemorrhages associated with meningiomas are so rare that they appear to be described as case reports in the literature. Bellut et al. noted that 68 hemorrhages associated with meningiomas were described in the available references. Subsequent epidemiological data on such cases remain unclear.
| > Case Reports|| |
Three patients with meningioma-associated hemorrhages were treated neurosurgically in Bydgoszcz, Poland, at the Department of Neurosurgery and Neurotraumatology and Pediatric Neurosurgery of Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Toruń, from 2006 to 2020. These cases constituted 2.2% of the 136 meningiomas treated in our department during this time period. This study was approved by the Bioethics Committee of the Ludwik Rydygier Collegium Medicum in Bydgoszcz, the Nicolaus Copernicus University in Toruń (document no. KB 35/2020). The preparation of this manuscript consisted of a retrospective analysis of medical documentation, and analysis of CT and MRI images. There was no direct contact with patients in this study. No patient personal data was taken into account, retrospective documentation analysis was anonymous.
The first patient was a 38-year-old male in good general condition, complaining of a headache, with consciousness state at 15 GCS. Focal symptoms were found on neurological examination, including motor aphasia, slight right-sided hemiparesis and headache. The patient had no history of chronic diseases and did not take any medication regularly. Urgent admission to the hospital was decided due to sudden occurrence of these symptoms. A CT scan revealed hemorrhage in the left frontal region, corresponding to tumor bleeding [Figure 1], with thin SDH located below the tumor, in the pterional region [Figure 2]. Due to the patient's good neurological status, there was no indication for urgent neurosurgery and the diagnostic procedures were extended to MRI. A bleeding tumor was revealed on MRI images, and its morphology was suggestive of a meningioma. CT images of the tumor hemorrhage in this patient are shown in [Figure 1] and [Figure 2].
|Figure 1: Computed tomography image with hemorrhage in the left frontal region associated with brain tumor|
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|Figure 2: Computed tomography image with marked by author thin subdural hematoma located below the tumor|
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On expressing informed consent for the procedure and anesthesiologic preparation, the patient underwent surgery. Craniotomy was performed and the tumor was excised with Simpson I radicality. However, due to severe intraoperative cerebral edema, the bone flap was not restored during closure and a decompressive craniectomy was performed. Histopathological evaluation confirmed transitional (mixed) meningioma with I grade of malignancy according to the World Health Organization (WHO I).
Following the surgery, the patient's neurological state remained good, at 15 GCS, and the focal signs gradually decreased. Physical rehabilitation was applied, anti-edema drugs were administered until the 7th day after surgery. Cranioplasty was performed 8 weeks after the first surgery. The patient's recovery was very good. As the tumor was WHO I degree, no additional oncological treatment was needed. Postoperative MRI confirmed no tumor recurrence [Figure 3].
|Figure 3: Postoperative magnetic resonance imaging with no tumor recurrence (magnetic resonance imaging T1)|
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The second patient was a 57-year-old female, who underwent an urgent operation due to her severe neurological state. The patient's condition was 10 GCS, with focal symptoms presenting as paresis. The patient's history of chronic diseases and medication was unknown. Later, it was found that she was being treated for mild hypertension, controlled correctly, with no disturbing blood pressure values. Surgical treatment was life-saving and urgent. No consent was obtained due to disturbed consciousness. The patient's general condition indicated high intracranial pressure. CT revealed massive hemorrhage associated with right parietal region tumor with SDH [Figure 4].
|Figure 4: Computed tomography coronal view with tumor hemorrhage with subdural hematoma above tumor (a), computed tomography axial view with tumor hemorrhage with subdural hematoma forward from the tumor (b)|
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Operative treatment was planned on the basis of CT. Radical resection of the tumor (Simpson I) was performed, following parietal craniotomy, with the bone flap restored afterwards. There was no brain edema that would necessitate decompressive craniectomy. Histopathological evaluation confirmed WHO I meningothelial meningioma. Following the surgery, the patient's neurological state improved, and the focal signs also gradually receded. Physical rehabilitation was applied. The patient's recovery was excellent. Due to the tumor's classification as WHO I, no additional oncological treatment was required, as in Case 1 described in the present manuscript.
The third case was an 82-year-old female, admitted to the hospital due to right-sided hemiparesis and memory impairment. Initially, muscle weakness affected the upper limb, then paresis of the lower limb also appeared. Despite the patient's advanced age, she had no history of chronic diseases, nor did she take any medication on a regular basis. CT showed a polycyclic partially calcified tumor, which showed features of bleeding into its mass [Figure 5].
|Figure 5: Computed tomography image of a brain tumor with signs of bleeding inside (marked by the author)|
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Due to the patient's relatively good neurological condition and absence of any symptoms of high intracranial pressure, the diagnosis was extended to MRI. MRI confirmed a tumor suggestive of meningioma [Figure 6], although earlier CT also showed morphology rather similar to meningioma.
|Figure 6: Magnetic resonance imaging with tumor suggestive of meningioma|
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Initially, the patient did not want to give her informed consent for the surgery, but after the physician (the author of this manuscript) provided her with further explanation, she decided to undergo the surgery. Following anesthetic preparation, partial tumor resection was performed. The part of the meningioma which contained the bleeding was removed. However, the calcified tumor fraction, which appeared clinically silent, was not removed, as the author believed its removal posed too high a risk of perioperative complications in view of the patient's advanced age. The patient endured the surgery well. Histopathological examination confirmed a WHO I meningothelial meningioma. Following the operation, the patient was admitted to the Rehabilitation Department to improve the paresis, which nonetheless persisted throughout the 6 months of follow-up. The patient's functional state remained the same as before the surgery, defined as 50 points on the Karnofsky Scale. She was assisted by permanent social care adequate to her functional state and age.
| > Discussion|| |
Hemorrhages associated with meningiomas are rare and seem to be the subject of case reports of many authors practicing in neurosurgical departments worldwide. The authors reviewed previous literature and found references published in the last 82 years (1938–2020). References reviewed in this manuscript were cases reports and literature reviews. The summary of 24 cases descriptions is presented in [Table 1]. Summary of meningioma-associated hemorrhages from review articles is presented in [Table 2]. The authors cited the selected cases descriptions in chronological order.
Historically, the first case description of hemorrhage– SAH associated with posterior fossa fibrous meningioma was prepared by Cushing and Eisenhardt.
Modesti et al. reported four cases of spontaneous intracranial hematomas caused by unsuspected meningiomas. He claimed at the time of publication of his work that nine previous cases were found in the literature and the entire series of 13 cases was reviewed in 1976. Modesti et al. emphasized that these cases had not been diagnosed correctly prior to radiological studies because of their unusual clinical presentation.
Lazaro et al. reported meningioma-associated hemorrhages in two patients with meningioma without risk factors predisposing toward hemorrhage. Bleeding was reported to be associated with meningiomas regardless of the sex or age of the patient or the location or histological nature of the tumor. This is similar to our study. The age of the patients described in our manuscript was 38–82, two patients (Cases 1, 3) had no risk factors, while Case 2 had only properly controlled hypertension. According to Lazaro et al. the mechanism of hemorrhage is not clear.
Review articles about meningiomas hemorrhages from the 20th century put attention on differences in diagnosis and outcome before CT era and after the widespread use of CT. Cheng et al. based on 20 reviewed cases found that death occurred in 55% of patients. He emphasized that in CT era, 58% of patients had recovered, while in the pre-CT era 78% died and none had a good recovery. Cheng et al. concluded that early diagnosis is crucial for favorable outcome.
Agazzi et al. described the case of a 72-year-old patient with meningioma-associated hemorrhage and reported that 44 cases of meningioma-associated hemorrhages had been described in English and Japanese literature. According to Agazzi et al. these 44 cases showed 23 cases of SAH, 20 cases of ICH/ITH and 13 cases of SHD, mixed patterns of hemorrhage were not infrequent. The author emphasized that of the 44 cases described, only eight manifested in a coma and severe clinical condition and immediate surgical treatment based on CT was indicated. In this manuscript one patient (Case 2) was in severe neurological condition and was treated urgently. The patient described by Agazzi et al. fully recovered. Clinical examination and a follow-up CT scan after 3 months were considered normal, which is similar to the outcome of the patient described in this study (Case 2). The outcome seems to be improved with rapid brain decompression and tumor removal.
Kuzeyli et al. reported 11 cases of meningiomas manifested by hemorrhage among all 126 meningiomas operated in his center during 12 years (1990–2001). He classified hemorrhages in two groups: macroscopic and microscopic. With regard to the hemorrhages described in this manuscript, only these macroscopic according to Kuzeyli et al. have been used for comparative analysis. All were convexity meningiomas, which was consistent to our study. Kuzeyli et al. reported that described patients presented progressive neurological deficits, and emergency operations were performed.
It is thought that the largest review about hemorrhagic meningiomas was performed by Boŝnjak et al. He described 145 cases of spontaneously bleeding meningiomas. Boŝnjak et al. noted that the risk factors for meningiomas hemorrhage are age older than 70 and younger than 30 years, location in the convexity, and hypertension. This was also consistent with the observations in the present study-all the three meningiomas described (Cases 1-3) were located in the convexity, and in one case (Case 2) hypertension was also documented. Boŝnjak et al. revealed that the mortality rate in preoperatively conscious patients was similar to that documented in cases in which the meningioma did not bleed. In contrast, the associated morbidity rates were much higher. According to Boŝnjak et al., one-stage total removal of the hemorrhagic meningioma and hematoma is the treatment of choice in such patients. Boŝnjak's conclusions are consistent with the treatment described in our manuscript, because in all patients (Cases 1-3) one-stage total removal of the hemorrhagic meningioma was done.
Ziyal et al. reported a 57-year-old male with hemorrhage associated with right tentorial meningioma in severe neurological state, with focal signs. MRI scans demonstrated intra-and peritumoral hemorrhage. This is similar to the patient described in our study (Case 2) regarding the clinical condition. Also in our manuscript, two patients (Cases 1-2) both had intra- and peri-tumoral hemorrhage, as in the case described by Ziyal et al.
Mangubat et al. reported a patient with a history of a subtotal resection of a petroclival meningioma, followed by gamma knife radiosurgery. The patient presented with sudden neurological deterioration following ITH after four asymptomatic years. In this case report, the patient underwent early resection of this atypical meningioma and evacuation of the hematoma through a retrosigmoid transpetrosal approach. The patient's neurological condition improved rapidly. In contrast to patients described in our study, the meningioma in Mangubat's report was atypical, and the previous radiosurgery of the tumor draws attention as a potential risk factor, which is consistent with the conclusions drawn by Vij et al.
A particular case of meningioma-related hemorrhage was reported by Bellut et al. As in our study, the described patient was treated urgently and the prognosis was good. In his case, two hemorrhages were observed: primary and recurrent. Initially neurological condition was good and CT showed partially hemorrhagic tumor, then patient suddenly became comatose and CT revealed massive ICH and intraventricular hemorrhage surrounding the lesion which resulted in immediate surgery. The case described by Bellut et al. was a WHO I meningioma with the same degree of malignancy as in all cases described in this manuscript. Bellut et al. claimed that at the time of publishing his work (2011) 68 cases of ICHs associated with meningiomas had been reported.
Vij et al., in turn, noted that hemorrhage is a rare complication of meningiomas that can occur spontaneously, after embolization, stereotactic radiation and perioperatively. He reported that meningiomas with hemorrhagic onset remain rare, and pathophysiology is still incompletely understood. Prevention and outcome of ITH highly depends on early diagnosis and adequate treatment. In his study, Vij et al. described one case of hemorrhage associated with meningioma: a 45-year-old female with a WHO I meningothelial meningioma of the parasagittal area, treated by left frontal craniotomy with tumor decompression. The WHO malignancy grade described by Vij et al. is the same as in the patients described in our study.
In the second decade of the 21st century, case reports of meningioma-related hemorrhages were also prepared by Chonan et al., Frič et al., Lin et al., and Masoudi et al. These four descriptions presented hemorrhagic convexity and sphenoid wing meningiomas.,,,
Pressman et al. described a 56-year-old female with spontaneous SAH, in a coma from a petroclival meningioma. The patient was taking escitalopram and was undergoing high-dose estrogen therapy. Histopathological examination confirmed a WHO I meningioma. The case described by Pressman is similar to our Case 2 in terms of gender, age, neurological state and malignancy grade (WHO I). Pressman proposed two new risk factors to be considered that may predispose toward hemorrhage in a meningioma: serotonin-modulating therapy and high-dose estrogen-replacement. No such drugs were taken by the patients described in our study.
Sato et al.(2020) described a falx meningioma presenting with ITH in the right occipital lobe and an interhemispheric acute SDH in a 68-year-old male with a sudden headache. The presence of hemorrhagic meningioma was suspected initially on the basis of CT, then was confirmed by MRI.
| > Conclusion|| |
On the basis of the cases described and the data in the source literature, it is evident that meningioma-related hemorrhages are rare, and they are each time described by neurosurgeons listed in the references. Such risk factors as age and gender dependence are ambiguous and difficult to determine. Neurological states at the onset of hemorrhage may also vary widely, depending on each case individually. One-stage total removal of the hemorrhagic meningioma and hematoma is the treatment of choice. Based on our own observations and references, such meningiomas have often low degree of malignancy.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2]