Meningiomas are considered to be the most common primary extra-axial brain tumors that mostly develop as benign slowly growing lesions classified by the WHO as grade I, with a lower incidence of more aggressive types classified as grades II and III. Despite their benign nature, meningiomas can cause significant morbidity and mortality, particularly when they are located near critical neurovascular structures (1–3). Its incidence increases with advancing age, peaking around the sixth decade (1, 2, 4). Epidemiological studies consistently report a higher prevalence in females, with a risk that is twice that of males or higher, depending on the age group. Meningiomas also occur at a younger age in females than in males, around middle age (1, 2, 5). Since most lesions are benign and grow slowly, patients can be asymptomatic and discovered incidentally or with insidious and slow progression of neurological symptoms depending on the affected location (3, 5–7).

Considering that meningiomas are more frequent in females than males, hormonal factors such as progesterone are hypothesized to be involved (8). This raises the following question: are meningiomas more common in pregnant females? The overall incidence of meningiomas during pregnancy is lower than that in the general female population because meningiomas typically present in older age groups (9, 10). However, this does not negate the faster growth of meningiomas during pregnancy induced by hormones, which makes it even more challenging than the normal population owing to a harder diagnosis, since the symptoms may mimic other obstetric conditions, such as preeclampsia, eclampsia and hyperemesis gravidarum, a higher rate of complications and a higher risk of mortality if not promptly diagnosed and treated (10–12).

Boŝnjak et al. presented two cases in which unsuspected meningioma hemorrhaged, and they reviewed the literature for 145 similar cases dating from the pre-CT era until the date of publication of the study, stating that the risk of bleeding is only up to 2.4%, which clearly outlines the rarity of the event occurrence (13). Magnetic resonance imaging (MRI) has been proven to have excellent performance in diagnosing meningiomas and even predicting their WHO grade (14); however, in the setting of overlying hemorrhage, a sufficient amount of blood can mask the presence of the meningioma on imaging, leading to its discovery intraoperatively or even postoperatively with the recurrence of bleeding (15, 16).

In this study, we report a unique case of a middle-aged pregnant woman who presented with an extradural hematoma (EDH) on preoperative MRI and who was discovered intraoperatively to have a subdural hematoma (SDH) overlying a meningioma. To the best of our knowledge, this is the first reported case of a hemorrhagic convexity meningioma presenting as a presumed hematoma in a pregnant patient.

Case presentation:

A forty-four-year-old pregnant female patient presented to the emergency department at Mansoura University hospitals (MUH) after referral from her obstetrician presented with headache for 5 days and blurring of vision, vomiting and drowsiness on the day of presentation. The patient is pregnant in her second trimester, and as this is an old-age pregnancy, the obstetrician she is following with prescribed her low-dose aspirin as an antiplatelet since the first day of pregnancy. The patient had no history of trauma or previous operations. On examination, her GCS score was 14, and was drowsy, her pupils were round, regular and reactive to light; otherwise, the results of the other neurological examinations were normal, with intact motor and sensory examinations. A series of investigations done were as follows: blood grouping (AB + ve); complete blood count revealing mild neutrophilic leukocytosis (WBCs 11.93*10³/mL, neutrophil number 9.82*10³/mL), normal red blood cell indices for pregnancy (HGB 11.7 g/dL, MCV 86.0 fL, MCH 31.0 pg, MCHC 36.0 g/dL) and normal platelet count (347 k/µl); blood gases and electrolytes that revealed respiratory alkalosis (pH 7.506, PCO2 29.1 mmHg, HCO3- 22.5 mmol/L) and mild hypokalemia (2.94 mmol/L); prothrombin time and INR which were normal (11.6 seconds and 1.0, respectively); liver enzymes which were elevated (SGPT 161 U/L, SGOT 117 U/L); and serum total bilirubin, serum albumin, serum creatinine and random blood glucose which were all normal. After neurology consultation, the neurologist suspected dural sinus thrombosis and ordered MRI. Additionally, obstetric consultation was done to exclude any obstetric-related emergency. Non-contrast MRI of the brain revealed a well-defined extra axial space-occupying lesion measuring 6*3.5*5 cm, seen in the left parietal region displaying low signal intensity (SI) on T1 and areas of high SI denoting blood component, mixed SI on T2, and a blooming effect on SWIs. It exerts a mass effect in the form of compression upon the related cortical sulci, compression of the left lateral ventricle and minimal rightward deviation of midline structures. All these signs are coping with left parietal EDH (Fig. 1).

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(b)

Decision for surgical evacuation was made, and during preoperative preparation of the patient, her GCS score dropped to 9, and her pupils became unequal. Surgery started by shaving a wide area of the head to explore and evacuate the EDH; a question mark incision was made to the skin and subcutaneous tissue; the temporalis muscle was dissected toward the skull base; and the frontotemporoparietal flap of bone was elevated starting from the superior temporal line. After elevation of the flap, no EDH was found, but the dura was bluish, and the brain was very tense, suggesting the bleeding was subdural instead. A C-shaped incision of the dura was made, followed by evacuation of the subdural hematoma, which was found to be overlying a bluish grayish soft dural base mass (Fig. 2). The tumor was successfully excised and sent for histopathological examination, and the total time of surgery was 3 hours. Histopathological examination revealed a meningiothelial meningioma (WHO grade I) with no evidence of malignancy. The sections revealed prominent lobules, whorls, and collagenized blood vessels. Thorough examination revealed few mitotic figures and no detected necrosis, but wide areas of hemorrhage with excess hemosiderin deposition were detected. After surgery, the patient stayed in the ICU for 2 days, then in the ward for 4 days and was finally discharged without any complications during her hospital stay.

Owing to the rarity of this condition, hemorrhagic meningiomas appear to be only described in the literature as case reports. Hence, the risk factors and mechanisms of bleeding have yet to be confirmed and are still unclear. In a systematic review published in 2020, they attempted to outline the natural history of bleeding meningiomas through the available literature of 190 cases, 109 of which were females. They reported that among the different types of intracranial bleeding associated with the condition, SDH represented the second most common type to occur after intracerebral hemorrhage (17) despite the previous literature stating otherwise (18). The proposed risk factors for hemorrhage are age greater than 70 years or less than 30 years; location within the ventricle or on the convexity; malignant, fibrous, or angioblastic histopathology; and the presence of hypertension; anticoagulation therapy; and traumatic brain injury (13). It is already well established that female sex hormones increase the growth rate of meningiomas not only through hormonal pathways but also through increased blood volume and vascularization (10). Recently, it was proposed to also be considered as a risk factor for hemorrhagic meningiomas in a case report done on a patient who did not have any of the risk factors associated with this condition other than taking hormone replacement therapy together with serotonin-modulating therapy (19), which leads us to consider the possibility of pregnancy as not only a factor for faster growth of the tumor but also for hemorrhagic meningioma presentation just like with, similar to our case.

Literature was searched for cases of pregnant females with a convexity tumor presenting for the first time with hemorrhage, but to the best of our knowledge ours is the first to be reported. We found only four research papers discussing hemorrhagic meningiomas, two of which were during pregnancy and two were in early postpartum period, with multiple differences from our study. Table 1 summarizes those differences between the four case reports and ours, highlighting the rarity of our case. In all four cases, the tumor was discovered preoperatively either before pregnancy as for the first patient or in the acute event of hemorrhage when imaging was performed, whether during pregnancy like in the second or postpartum as for the other two patients. This is unlike our case, where the tumor was discovered only intraoperatively. The first two cases were pregnant patients but did not have convexity tumors, so the bleeding was not subdural and the occurrence of acute hemorrhage was not the first presentation for either patient. Although the second two had convexity tumors with subdural hemorrhages, which is the common type for this position, they occurred in the postpartum setting.

Reviews on the topic gathered the possible pathophysiologic mechanisms behind acute peritumoral hemorrhagic onset with meningiomas: rupture from excessive or unusual blood vessels; direct vascular invasion by tumor cells; extensive tumor infarction; stretching and rupture of subdural veins; fragility of arterial and venous walls due to rapid tumor growth; and progressive vessel parietal weakening due to variation in tumoral stromal support (13, 17, 24). In alignment with our case, Lefranc et al. presented four patients without a history of trauma who developed subdural hemorrhage on top of meningeal tumor, and after histopathological examination of the specimens they proved that the bleeding started intratumorally where the specimens contained blood clots with hemosiderin deposition, concluding that the tumor had to be excised in the same setting as the evacuation since it was the source (15). This may explain the misdiagnosis of our patient pre-operatively, suggesting that the EDH observed was only the intratumoral hemorrhage (ITH) masking the presence of the tumor with mixed areas of high and low signal intensities and its extension subdurally. In a study looking further into ITH, Kuzeyli et al. reported that ITH is a rare event in meningiomas with a mortality risk of 40–55%, and that the bleeding is usually found extratumorally, according to the location of the tumor, mostly in the subarachnoid space. When both types of bleeding occur together, it is possibly related to a large amount of bleeding that is located in the peripheries of the tumor, leading to capsular rupture and a subsequent SDH or subarachnoid hemorrhage (25). The proposed mechanisms of ITH include erosion or disruption of the blood vessels by the tumor, distortion of the vessels by the tumor, venous hypertension, endothelial proliferation with secondary vascular occlusion and necrosis, and foci of abnormal blood vessels in a number of non-angioblastic meningiomas (25).

The only risk factor for our patient that could lead to hemorrhagic meningioma other than the fact that she was pregnant was her intake of prophylactic low-dose aspirin. A case report presented a 66-year-old female patient with hemorrhagic meningioma after intake of low-dose aspirin. They explained that since aspirin is known to increase the risk of hematoma enlargement and postoperative hemorrhage, it could be a potential risk factor for hemorrhagic meningioma; however, the patient’s prothrombin time and partial thromboplastin time were within normal ranges (26). This finding is similar to that of our patient, whose platelet count, prothrombin time and INR were normal. In contrast, studies assessing the risk of intracranial hemorrhage in patients with primary or metastatic brain tumors who are using antiplatelets concluded that there was no association (27, 28).

Our case highlights a very critical aspect of hemorrhagic meningiomas which is misdiagnosis pre-operatively which may lead to fatal consequences. MRI has very characteristic signs for accurately diagnosing typical meningiomas; additionally, atypical diagnostic features are also known (29). Unfortunately, owing to the rarity and misdiagnosis of hemorrhagic meningiomas, even with MRI, we still do not fully understand or have enough data on the radiographic features of this condition. A study on this issue revealed that no specific pattern of features could be expected in case of hemorrhagic meningiomas since the imaging shows absent dural tail and mixed signal intensities on both T1 and T2 of MRI, aligning with what happened with our case (30).

To conclude, this is a very unique case that sheds light on the importance of considering intracranial hemorrhage as a differential diagnosis for pregnant patients presenting with neurological symptoms such as headache and blurred vision, among other obstetric differentials like pre-eclampsia and eclampsia, making the diagnosis more challenging. Additionally, the findings highlight the importance of considering meningioma as a differential diagnosis for unexplained intracranial hemorrhage since it can be masked on imaging. Taking that into account will allow better surgical planning and technique to be used in the setting there is a tumor so that the treatment could effectively remove the source of hemorrhage to prevent the recurrence of bleeding if not removed. This case also prompts further research on risk factors for bleeding from meningiomas focusing on the risk of pregnancy and the use of prophylactic low-dose aspirin.