A case series of atraumatic nonaneurysmal perimesencephalic subarachnoid hemorrhages triggered during exertion at altitude

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J Neurocrit Care. 2024;17(2):57-61

Publication date (electronic) : 2024 September 3

doi : https://doi.org/10.18700/jnc.240012

Austin T Smith, MD

Department of Emergency Medicine, Intermountain Health, Park City, UT, USA

Corresponding Author: Austin T Smith, MD Department of Emergency Medicine, Intermountain Health, 900 Round Valley Drive, Park City, UT 84060, USA Tel: +1-43-5658-6705 Fax: +1-43-5658-6739 E-mail: Austin.Smith@imail.org

Received 2024 April 25; Revised 2024 June 22; Accepted 2024 July 3.

Abstract

INTRODUCTION

Nonaneurysmal perimesencephalic subarachnoid hemorrhage (NAPH) is a form of subarachnoid hemorrhage (SAH) which develops predominantly in the perimesencephalic region in the absence of an aneurysm or any other sources of bleeding on diagnostic angiography [1]. The term was first described by van Gijn [1] in 1985. These hemorrhages represent approximately 10%–15% of all spontaneous SAH cases [1,2]. The clinical presentation of patients with NAPH is similar to aneurysmal SAH, and includes sudden onset headache, meningismus, photophobia, and nausea. In one study, headaches were more gradual [1,3]; however, this result remains unvalidated.

Fortunately, NAPH has a much better prognosis than aneurysmal SAH [3]. However, the underlying cause of NAPH remains unclear. This case series describes three patients who developed NAPH during strenuous activity after traveling to an altitude of approximately 7,500 feet. Although several theories regarding disease pathogenesis exist, this case series demonstrates that hypoxia and vigorous exercise may be risk factors for NAPH.

CASE REPORTS

Case 1

A 49-year-old female with a medical history of chronic neck pain presented to the emergency department with the chief complaint of neck pain. The patient was visiting from the Atlanta, Georgia area for a music festival and had further taken a cross-country ski lesson. After enjoying the initial lessons, she returned to the cross-country course. While exerting herself, she reported sudden onset of severe pain on the right side of her neck which worsened when she flexed her neck. She further experienced an episode of emesis, but pain persisted. Other than a mild fall earlier in the day during which she did not hit her head, she denied any trauma.

In the emergency department, the patient was uncomfortable but nontoxic. She was afebrile with a heart rate of 94 beats per minute (bpm), blood pressure of 144/91 mm Hg, and oxygen saturation of 99% on room air. Neurological examination revealed no deficits. Given the severity of her neck stiffness, computed tomography (CT) of the brain (Fig. 1) and neck was performed, revealing acute SAHs in the basal and prepontine cisterns, without evidence of hydrocephalus. A CT angiogram was further obtained, revealing patent cervical and intracranial arterial vasculatures without any evidence of dissection or aneurysm. She did not require antihypertensives in the emergency department, but received levetiracetam for seizure prophylaxis. These findings were consistent with Hunt and Hess grade 2 of SAH [4].

Fig. 1.

(A) A noncontrast computed tomography (CT) scan showing a subarachnoid hemorrhage in the basal and prepontine cisterns without evidence of hydrocephalus. (B) A CT angiogram of the brain revealing no evidence of aneurysm. (C) A diagnostic angiogram of the brain revealing no evidence of aneurysm.

The patient was transferred to a tertiary care facility where she underwent catheter angiography on hospitalization day 1, which revealed no evidence of an intracranial aneurysm or vascular malformation. On hospital day 3, magnetic resonance imaging (MRI) and magnetic resonance angiography of the neck and brain revealed a small amount of subarachnoid blood within the sulci of the occipital convexities, without any significant vascular abnormalities. Daily transcranial Doppler examinations did not show any evidence of vasospasm, except for an episode on hospital day 5, which normalized by hospital day 6. A repeat catheter angiography was performed and revealed mild narrowing of the distal basilar artery compared to prior. No flow restrictions or vasospasms involving other vascular distributions were observed. Her examination remained non-focal throughout the hospital course, and she was eventually discharged on hospital day 10 with a prescription for 2 days of dexamethasone.

Case 2

A 57-year-old male with no medical history presented to the emergency department with the chief complaints of headache and neck pain. The patient was from the Los Angeles area, and was visiting Park City, UT, for vacation, and stated that he had gone on a hike in the morning and then went on to wake surfing. While wake surfing, he developed neck stiffness that progressed to more severe upper neck pain radiating throughout his head over several hours. He denied any trauma.

In the emergency department, the patient was uncomfortable, but nontoxic. He was afebrile, with a heart rate of 55 bpm, blood pressure of 171/95 mm Hg, and oxygen saturation of 96% on room air. Neurological examinations revealed no deficits. Given the severity of his symptoms, a CT scan of the brain (Fig. 2) was performed, revealing a moderate-to-large SAH in the prepontine cistern and ambient cisterns extending to the foramen magnum. There was no evidence of hydrocephalus. CT angiography revealed no evidence of intracranial stenosis, emboli, or angiogram. Nicardipine infusion was initiated, and levetiracetam was administered. These findings were consistent with Hunt and Hess grade 2 of SAH [4].

Fig. 2.

(A) A noncontrast computed tomography (CT) scan showing a moderate subarachnoid hemorrhage in the prepontine cistern. (B) A CT angiogram of the brain showing no evidence of aneurysm.

He was transferred to a tertiary care facility, where he underwent repeat head CT on hospital day 1, along with a diagnostic angiogram that did not reveal any vascular source of bleeding. MRI performed on hospital day 2 of which did not reveal any acute changes or aneurysms. The patient underwent a repeat diagnostic angiography on hospital day 10, which did not reveal any vascular source of bleeding. The patient’s hospital course was complicated by hyponatremia and he was successfully treated with salt tablets. The patient was discharged on day 12 of hospitalization.

Case 3

A 50-year-old male with a medical history of coronary artery disease presented to the emergency department with the chief complaint of headache. The patient was from Orlando, Florida, and had visited Park City, UT, for vacation. Four days prior to presentation, he had gone downhill skiing after a day of cross-country skiing. While skiing, the patient experienced an immediate onset of severe headache. The headache seemed to improve after ibuprofen administration; however, over the next several days, it relapsed. The patient subsequently presented to his primary care physician who sent him directly to the emergency department.

Upon arrival at the emergency department, he appeared diaphoretic and ill. He was afebrile, with a heart rate of 47 bpm, blood pressure of 155/90 mm Hg, and oxygen saturation of 97% on room air. Neurological examinations revealed no deficits. Given the severity of his symptoms, CT of the brain was performed (Fig. 3), which revealed a hemorrhage within the subarachnoid space anterior to the pons, extending into the interpeduncular and suprasellar cistern. There was no evidence of hydrocephalus. CT angiogram revealed no evidence of vascular abnormalities. His blood pressure increased slightly, and he was started on nicardipine infusion and was administered levetiracetam. These findings were consistent with Hunt and Hess grade 2 of SAH [4].

Fig. 3.

(A) A noncontrast head computed tomography (CT) showing a subarachnoid hemorrhage within the subarachnoid space anterior to the pons extending into the interpeduncular cistern. (B) A CT angiogram of the brain revealing no evidence of aneurysm. (C) A diagnostic angiogram of the brain revealing no evidence of aneurysm.

He was transferred to a tertiary care facility, where he underwent diagnostic angiography on hospitalization day 0 that did not reveal any vascular source of bleeding. MRI performed on hospitalization day 1 did not reveal any acute changes or aneurysms. A repeat diagnostic angiogram on hospitalization day 4 did not reveal any changes, and the patient was discharged on the same day.

DISCUSSION

The underlying cause of bleeding in patients with non-aneurysmal perimesencephalic SAH remains unclear. Several theories regarding its causes exist, including primitive drainage of the basal vein of Rosenthal [2], microaneurysm or microangioma, rupture of the pontine perforating arteries, bleeding from the perimesencephalic or deep internal veins, or hemorrhage from basilar trunk dissections and intramural hematoma [2,3,5,6].

Although venous abnormalities, specifically within the basal vein of Rosenthal, were postulated as a cause in the original article introducing NAPH, careful examination of venograms was not consistent with this [1,3]. A more recent systematic review and meta-analysis revealed that patients with NAPH have a higher prevalence of the primitive basal vein of Rosenthal [2], although other mechanisms may also play a role.

Several authors have reported that physical exertion, resulting in cerebral venous hypertension or mechanical swelling of the intracranial veins, can lead to venous damage and NAPH [6-9]. Because the venous pressure in this small-volume area is low, there is generally a tamponade effect, resulting in a self-limited hemorrhage. This is thought to contribute to a better prognosis than aneurysmal SAH [9].

Supporting the theory that intracranial hypertension contributes to hemorrhage, there have been several case reports of scuba divers developing SAH and other intracranial hemorrhages following rapid ascent secondary to increased intracranial pressure [10-12]. Altitude and barometric pressure changes associated with SAH have also been reported. For example, Litch et al. [13] described the case of a Swedish climber who developed an aneurysmal SAH while climbing Mount Everest, and further highlighted an article by Jehle et al. [14] that linked spontaneous SAH to decreased barometric pressures.

Hypoxia has also been associated with NAPH. Blandford and Chalela [15] previously described a case of NAPH in a patient who underwent hypoxia training while swimming. The authors [15] hypothesized that breath-holding leads to cerebral vasodilatation, resulting in venous congestion and impaired cerebral venous return from the brain to systemic circulation. Therefore, bilateral jugular venous occlusion may be a contributing factor, as could the Valsalva maneuver.

Physiologically, the cerebral vasculature undergoes vasodilation in response to hypoxia. It is plausible that relative hypoxemia at high altitude, in combination with vigorous activity, led to the patient’s NAPH. Patients traveling to high altitudes should be counseled regarding the importance of gradually increasing exercise intensity. Additionally, clinicians practicing at high altitudes should be aware of this condition to facilitate diagnosis and treatment, along with help with prognostication.

In the present study, we presented a case series of three patients traveling to an altitude who engaged in vigorous exercise and had NAPH. All three patients had similar presentations, courses, and outcomes. The combination of venous congestion from strenuous exercise and hypoxia was thought to cause NAPH. Patients should be cautioned about gradually increasing their exercise intensity when traveling to high altitudes.

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