Advertisement
Mayo Clinic Proceedings Home

Origin of Pretruncal Nonaneurysmal Subarachnoid Hemorrhage: Ruptured Vein, Perforating Artery, or Intramural Hematoma?

      Pretruqeal (perimesencephalic) nonaneurysmal subarachnoid hemorrhage (SAH) is a benign variant of SAH. Although angiography fails to show a source of the hemorrhage, mild basilar artery narrowing may be observed. The cause of pretruncal nonaneurysmal SAH has not been established. Recent imaging studies have demonstrated that the center of this type of SAH is not around the mesencephalon but is in the prepontine or interpeduncular cistern with the hemorrhage closely associated with the basilar artery. We review the possible sources of hemorrhage in these cisterns and hypothesize that pretruncal nonaneurysmal SAH is caused by a primary intramural hematoma of the basilar artery. Such an intramural hematoma would explain bleeding under low pressure, the location of the hemorrhage anterior to the brainstem, and the typical findings of hemorrhage adjacent to the basilar artery lumen on magnetic resonance imaging and mild basilar artery narrowing on angiography. Although an intramural hematoma of the basilar artery would be easily identified at surgical exploration, such surgeries have never included the extensive base-of-the-skull approaches the-skull approaches that are necessary to visualize the artery in the prepontine cistern.
      CT (computed tomography), MRI (magnetic resonance imaging), SAH (subarachnoid hemorrhage)
      Among patients with a subarachnoid hemorrhage (SAH) and normal findings on an angiogram, 50% to 75% have a computed tomographic (CT) scan showing a specific pattern of hemorrhage, the so-called pretruncal (perimesencephalic) nonaneurysmal SAH (Figure 1). This type of hemorrhage has become well established as a benign variant of SAH.
      • van Gijn J
      • van Dongen J
      • Vermeulen M
      • Hijdra A
      Perimesen-cephalic hemorrhage: a nonaneurysmal and benign fonn of sub-arachnoid hemorrhage.
      • Rinkel GJE
      • Wijdicks EFM
      • Vermeulen M
      • et al.
      Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from ancurysmal ruplure.
      • Rinkel GJE
      • Wijdicks EFM
      • Hasan D
      • et al.
      Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography.
      • Van Calenbergh F
      • Plets C
      • Goffin J
      • Velghe L
      Nonancurysmal subarachnoid hemorrhage: prevalence of perimesencephalic hemorrhage in a consecutive series.
      • Schievink WI
      • Wijdicks EFM
      • Piepgras DG
      • Nichols DA
      • Ebersold MJ
      Perimesencephalic subarachnoid hemorrhage: additional perspectives from four cases.
      • Canhao P
      • Ferro JM
      • Pinto AN
      • Melo TP
      • Campos JG
      Perimesencephalic and nonperimesencephalic subarachnoid haemorrhages with negative angiograms.
      • Schievink WI
      • Wijdicks EFM
      Pretruncal subarachnoid hemorrhage: an anatomically correct description of the perimesencephalic subarachnoid hemorrhage [letter].
      • Wijdicks EFM
      • Shievink WI
      • Miller GM
      Pretruncal nonancurysmal subarachnoid hemorrhage.
      • Schievink WI
      • Wijdicks EFM
      • Spetzler RF
      Diffuse vasospasm after pretruncal nonaneurysmal subarachnoid hemorrhage.
      Despite clinical observations in a large number of patients worldwide, extensive radiographic investigations, and surgical exploration in a few patients, the cause of pretruncal nonaneurysmal SAH has remained a mystery. Because of the invariably excellent prognosis, no postmortem studies are available. Recent imaging studies have demonstrated that the center of this type of SAH is not around the mesencephalon but rather is anterior to the brainstem, most commonly in the prepontine cistern with the hemorrhage intimately associated with the basilar artery.
      • Schievink WI
      • Wijdicks EFM
      Pretruncal subarachnoid hemorrhage: an anatomically correct description of the perimesencephalic subarachnoid hemorrhage [letter].
      • Wijdicks EFM
      • Shievink WI
      • Miller GM
      Pretruncal nonancurysmal subarachnoid hemorrhage.
      Based on this knowledge, we review the possible sources of bleeding in pretruncal nonaneurysmal SAH and propose that this benign variant of SAH may be caused by a primary intramural hematoma of the basilar artery.
      Figure thumbnail gr1
      Figure 1Computed tomograms of patients with pretruncal nonaneurysmal subarachnoid hemorrhage showing localized hemorrhage in the prepontine (left) and interpeduncular (right) cisterns.
      An SAH caused by rupture of a cerebral aneurysm is a devastating event, associated with a 50% early mortality rate.
      • Schievink WI
      Intracranialaneurysms.
      In contrast, patients with a pretruncal nonaneurysmal SAH rarely lose consciousness at the time of the hemorrhage, are in good condition on admission to the hospital, have an excellent prognosis, and have a corresponding CT scan with no pronounced intraventricular hemorrhage or intracerebral hematoma.
      • van Gijn J
      • van Dongen J
      • Vermeulen M
      • Hijdra A
      Perimesen-cephalic hemorrhage: a nonaneurysmal and benign fonn of sub-arachnoid hemorrhage.
      • Rinkel GJE
      • Wijdicks EFM
      • Vermeulen M
      • et al.
      Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from ancurysmal ruplure.
      • Rinkel GJE
      • Wijdicks EFM
      • Hasan D
      • et al.
      Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography.
      • Van Calenbergh F
      • Plets C
      • Goffin J
      • Velghe L
      Nonancurysmal subarachnoid hemorrhage: prevalence of perimesencephalic hemorrhage in a consecutive series.
      • Schievink WI
      • Wijdicks EFM
      • Piepgras DG
      • Nichols DA
      • Ebersold MJ
      Perimesencephalic subarachnoid hemorrhage: additional perspectives from four cases.
      • Canhao P
      • Ferro JM
      • Pinto AN
      • Melo TP
      • Campos JG
      Perimesencephalic and nonperimesencephalic subarachnoid haemorrhages with negative angiograms.
      • Schievink WI
      • Wijdicks EFM
      Pretruncal subarachnoid hemorrhage: an anatomically correct description of the perimesencephalic subarachnoid hemorrhage [letter].
      • Wijdicks EFM
      • Shievink WI
      • Miller GM
      Pretruncal nonancurysmal subarachnoid hemorrhage.
      • Schievink WI
      • Wijdicks EFM
      • Spetzler RF
      Diffuse vasospasm after pretruncal nonaneurysmal subarachnoid hemorrhage.
      Because of the benign clinical presentation and findings on imaging studies, the source of a pretruncal nonaneurysmal SAH must be under relatively low pressure. The typical distribution of blood in this type of hemorrhage is best explained by a source in the prepontine or interpeduncular cistern, such as the anterior pontomesencephalic vein, perforating arteries arising from the basilar artery or its main branches, or the basilar artery itself (Figure 2).
      Figure thumbnail gr2
      Figure 2Intraoperative photograph (left) and corresponding line drawing (right) of the prepontine and interpeduncular cisterns in a patient who underwent an orbitozygomatic craniotomy. Note the proximity of the possible sources of pretruncal nonaneurysmal subarachnoid hemorrhage.

      RUPTURED VEIN

      A ruptured vein has long been suspected to be the cause of pretruncal nonaneurysmal SAH.
      • van Gijn J
      • van Dongen J
      • Vermeulen M
      • Hijdra A
      Perimesen-cephalic hemorrhage: a nonaneurysmal and benign fonn of sub-arachnoid hemorrhage.
      Not only would a venous source account for bleeding under low pressure but also a history of a Valsalva maneuver immediately before the onset of headache is often elicited in this patient population. A Valsalva maneuver may result in an abrupt increase in cerebral venous pressure by retrograde transmission of increased intrathoracic pressure. However, Valsalva maneuvers also frequently precipitate SAH from an arterial source, possibly because of the associated changes in arterial blood pressure, intracranial pressure, and transmural pressure.
      • Schievink WI
      • Karemaker JM
      • Hageman LM
      • van der Werf DJ
      Circumstances surrounding ancurysmal subarachnoid hemorrhage.
      In an early angiographic study, when the center of this type of SAH was believed to be in the perimesencephalic cisterns, particular attention was paid to the basal vein of Rosenthal, and. no abnormalities were reported.
      • van Gijn J
      • van Dongen J
      • Vermeulen M
      • Hijdra A
      Perimesen-cephalic hemorrhage: a nonaneurysmal and benign fonn of sub-arachnoid hemorrhage.
      This vein courses through the crural, ambient, and quadrigeminal cisterns but not through the interpeduncular or prepontine cisterns. Subsequent detailed angiographic investigations of the venous structures in the interpeduncular and prepontine cisterns also detected no abnormalities (W.I.S. and E.F.M.W., unpublished data, 2000). On surgical exploration of the prepontine and interpeduncular cisterns for unrelated vascular or neoplastic disease, we have occasionally noted an engorged anterior pontomesencephalic vein (Figure 2). This vein, also known as the prepontine vein, courses along the anterior surface of the pons near the basilar artery (Figure 2). Once ruptured, this vein is a likely candidate for the source of pretruncal nonaneurysmal SAH.
      Because of venous collapse and the variability of venous anatomy in the posterior fossa, it is unlikely that a ruptured vein would be an easily identified source of SAH at autopsy or surgical exploration.

      PERFORATING ARTERY

      Alexander et al
      • Alexander MS
      • Dias PS
      • Uttley D
      Spontaneous subarach noid hem -orrhage and negative cerebral panangiography: review of 140 cases.
      were the first to suggest a perforating artery as the cause of pretruncal nonaneurysrnal SAH. Numerous perforating arteries arising from the basilar artery, the superior cerebellar arteries, and the posterior cerebral arteries course through the prepontine and interpeduncular cisterns (Figure 2). Often, perforating arteries are tethered to the surrounding arachnoid trabeculae, perhaps predisposing them to tearing and bleeding after minor trauma.
      In the pre-CT era, Hochberg et al
      • Hochberg FH
      • Fisher CM
      • Roberson GH
      Subarachnoid hemorrhage caused by rupture of a small superficial artery.
      described a patient with an SAH and normal findings on an angiogram in whom a ruptured pontine perforating artery was found at postmortem examination. Some patients with a pretruncal nonaneurysmal SAH develop acute lacunar infarcts, and investigators have suggested that this favors a perforating artery as the source of the hemorrhage.
      • Tatter SB
      • Buonanno FS
      • Ogilvy CS
      Acute lacunar stroke in association with angiogram-negative subarachnoid hemorrhage: mechanistic implications of two cases.
      • Rogg JM
      • Smcaton S
      • Doberstein C
      • Goldstein JH
      • Tung GA
      • Haas RA
      Assessment of the value of MR imaging for examining patients with angiographically negative subarachnoid hemorrhage.
      However, these infarcts generally are found inthe putamen or caudate, and magnetic resonance images (MRIs) have shown that infarcts in the distribution of perforating arteries coursing through the prepontine or interpeduncular cistern are very rare.
      • Rogg JM
      • Smcaton S
      • Doberstein C
      • Goldstein JH
      • Tung GA
      • Haas RA
      Assessment of the value of MR imaging for examining patients with angiographically negative subarachnoid hemorrhage.
      • Wijdicks EFM
      • Schievink WI
      • Miller GM
      MR imaging in pretruncal nonaneurysmal subarachnoid hemorrhage: is it worthwhile?.
      Because of the large number and variability of perforating vessels anterior to the brains term, it is also unlikely that a ruptured perforating artery would be an easily identified source of SAH at autopsy or surgical exploration, unless associated with thrombosis of the vessel.

      INTRAMURAL HEMATOMA

      Magnetic resonance images in patients with pretruncal nonaneurysmal SAH· often demonstrate a localized hemorrhage closely associated with the lumen of the basilar artery (Figure 3).
      • Rogg JM
      • Smcaton S
      • Doberstein C
      • Goldstein JH
      • Tung GA
      • Haas RA
      Assessment of the value of MR imaging for examining patients with angiographically negative subarachnoid hemorrhage.
      • Wijdicks EFM
      • Schievink WI
      • Miller GM
      MR imaging in pretruncal nonaneurysmal subarachnoid hemorrhage: is it worthwhile?.
      • Kuker W
      • Thiex R
      • Block F
      Hyperacute perimesencephalic subarachnoid hemorrhage: demonstration of blood extravasation with MRI.V.
      Rather than a layering of blood along the basilar artery, this may represent a primary hematoma within the wall of the artery itself. Luminal narrowing of the basilar artery is common in pretruncal nonaneurysmal SAH and may be seen in up to 25% of patients.
      • Wijdicks EFM
      • Shievink WI
      • Miller GM
      Pretruncal nonancurysmal subarachnoid hemorrhage.
      This nonspecific narrowing is mild and generally interpreted as vasospasm but also is compatible with basilar artery dissection (Figure 4). It may seem counterintuitive to suggest arterial dissection as the cause of a type of SAH that is associated with completely normal findings on an angiogram in at least 75% of patients. Although sporadic MRI-diagnosed cases of carotid artery dissection with normal angiographic findings have been reported, a wide majority of cases of cervicocephalic arterial dissections are characterized angiographically by areas of stenosis, wall irregularities, aneurysmal dilatation, or a double lumen.
      • Mokri B
      Dissections of cervical and cephalic arteries.
      However, a substantial majority of cervicocephalic arterial dissections are associated with an intimal tear, allowing circulating blood to penetrate into the vessel wall.
      • Mokri B
      Dissections of cervical and cephalic arteries.
      Under such circumstances, the hemorrhage is under frank arterial pressure, and a resultant SAH has a correspondingly poor prognosis. Alternatively, however, an intramural hematoma may be the primary event in arterial dissection. In the aorta, such a primary intramural hematoma is known as aortic dissection without intimal rupture and is believed to be caused by rupture of vasa vasorum.
      • Yamada T
      • Tada S
      • Harada J
      Aortic dissection without intimai rupture: diagnosis with MR imaging and CT.
      • Coady MA
      • Rizzo JA
      • Elefteriades JA
      Pathologic variants of thoracic aortic dissections: penetrating atherosclerotic ulcers and intramural hematomas.
      Vasa vasorum are also present in human vertebrobasilar arteries.
      • Atkinson JLD
      • Okazaki H
      • Sundt Jr, TM
      • Nichols DA
      • Rufcnacht DA
      Intracranial cerebrovascular vasa vasorum associated with atherosclerosis and large thick-walled aneurysms.
      • Takaba M
      • Endo S
      • Kurimoto M
      • Kuwayama N
      • Nishijima M
      • Takaku A
      Vasa vasorum of the intracranial arteries.
      The walls of intracranial arteries are very attenuated compared to their extracranial counterparts of the same diameter and lack an external elastic membrane. Therefore, a primary intramural hematoma would be expected to break through into the subarachnoid space easily before building up a high intramural pressure, without causing any, or only mild, luminal compromise (Figure 5). The absence of communication between the basilar artery lumen and the dissection would also explain the lack of wall irregularity, aneurysmal dilatation, or double lumen.
      Figure thumbnail gr3
      Figure 3Magnetic resonance images (left and right) of patients with pretruncal nonaneurysmal subarachnoid hemorrhage. Note the proximity of the hematomato the basilar artery lumen.
      Figure thumbnail gr4
      Figure 4Frontal vertebral angiogram of a patient with a pretruncal nonaneurysmal subarachnoid hemorrhage. Note the smooth mild stenosis of the basilar artery as it traverses the prepontine cistern (arrowheads).
      Figure thumbnail gr5
      Figure 5A primary intramural hematoma of the basilar artery.
      Unlike a ruptured vein or perforating artery, an intramural hematoma of the basilar artery may be expected to be identified easily at the time of surgery. However, explorative craniotomies have been performed in patients with pretruncal nonaneurysmal SAH and no source of the hemorrhage was found.
      • Schievink WI
      • Wijdicks EFM
      • Piepgras DG
      • Nichols DA
      • Ebersold MJ
      Perimesencephalic subarachnoid hemorrhage: additional perspectives from four cases.
      • Rinkel GJE
      • Jafar JJ
      • Weiner HL
      Surgery for angiographically occult cerebral aneurysms.
      • Tatter SB
      • Crowell RM
      • Ogilvy CS
      Ancurysmal and micro-aneurysm'al “angiogram-negative” subarachnoid hemorrhage.
      Details of the extent of surgical exploration are scant in these reports, but having participated in 2 of the 4 reported cases, we know that the center of attention was the perimesencephalic cisterns, not the prepontine cistern. No skull-base approaches were used in these cases, and most of the basilar trunk, certainly the infraclinoid portion, was not visualized. Thus, an intramural hematoma of the basilar artery trunk could have easily escaped detection. In addition, the appearance of arterial dissections may change rapidly over a very short period; intramural hematomas of the aorta have been reported to resolve completely within 24 hours.
      • Ohmi M
      • Tabayashi K
      • Moizumi Y
      • Komatsu T
      • Sekino Y
      • Goko C
      Extremely rapid regression of aortic intramural hemaloma.
      There are no other types of SAH limited to a specific location that have the same benign clinical and radiographic characteristics as a pretruncal nonaneurysmal SAH which suggests that the source of pretruncal nonaneurysmal SAH must be unique to its location anterior to the brainstem. The only vascular structure anatomically unique to the prepontine and interpeduncular cisterns is the basilar artery, not small to medium-sized veins or perforating arteries, which are found throughout the major intracranial subarachnoid cisterns.
      It is unlikely that useful autopsy results will become available in a large group of patients with pretruncal nonaneurysmal SAH Further refinements in imaging techniques, particularly more powerful MRI scanners, will allow direct visualization of the contents of the pretruncal cisterns· in great detail and will test the hypothesis that a primary intramural hematoma of the basilar artery is the source of pretruncal nonaneurysmal SAH

      Acknowledgments

      We are grateful to Peggy Firth for the drawing in Figure 2 and to Mark Schornak for the drawing in Figure 5.

      REFERENCES

        • van Gijn J
        • van Dongen J
        • Vermeulen M
        • Hijdra A
        Perimesen-cephalic hemorrhage: a nonaneurysmal and benign fonn of sub-arachnoid hemorrhage.
        Neurology. 1985; 35: 493-497
        • Rinkel GJE
        • Wijdicks EFM
        • Vermeulen M
        • et al.
        Nonaneurysmal perimesencephalic subarachnoid hemorrhage: CT and MR patterns that differ from ancurysmal ruplure.
        AJNR Am J Neuroradiol. 1991; 12: 829-834
        • Rinkel GJE
        • Wijdicks EFM
        • Hasan D
        • et al.
        Outcome in patients with subarachnoid haemorrhage and negative angiography according to pattern of haemorrhage on computed tomography.
        Lancet. 1991; 338: 964-968
        • Van Calenbergh F
        • Plets C
        • Goffin J
        • Velghe L
        Nonancurysmal subarachnoid hemorrhage: prevalence of perimesencephalic hemorrhage in a consecutive series.
        Surg Neurol. 1993; 39: 320-323
        • Schievink WI
        • Wijdicks EFM
        • Piepgras DG
        • Nichols DA
        • Ebersold MJ
        Perimesencephalic subarachnoid hemorrhage: additional perspectives from four cases.
        Stroke. 1994; 25: 1507-1511
        • Canhao P
        • Ferro JM
        • Pinto AN
        • Melo TP
        • Campos JG
        Perimesencephalic and nonperimesencephalic subarachnoid haemorrhages with negative angiograms.
        Ada Neurochir (Wien). 1995; 132: 14-19
        • Schievink WI
        • Wijdicks EFM
        Pretruncal subarachnoid hemorrhage: an anatomically correct description of the perimesencephalic subarachnoid hemorrhage [letter].
        Stroke. 1997; 28: 2572
        • Wijdicks EFM
        • Shievink WI
        • Miller GM
        Pretruncal nonancurysmal subarachnoid hemorrhage.
        Mayo Clin froc. 1998; 73: 745-752
        • Schievink WI
        • Wijdicks EFM
        • Spetzler RF
        Diffuse vasospasm after pretruncal nonaneurysmal subarachnoid hemorrhage.
        AJNR Am J Neuroradiol. 2000; 21: 521-523
        • Schievink WI
        Intracranialaneurysms.
        New Engl J Med. 1997; 336: 28-40
        • Schievink WI
        • Karemaker JM
        • Hageman LM
        • van der Werf DJ
        Circumstances surrounding ancurysmal subarachnoid hemorrhage.
        Surg Neurol. 1989; 32: 266-272
        • Alexander MS
        • Dias PS
        • Uttley D
        Spontaneous subarach noid hem -orrhage and negative cerebral panangiography: review of 140 cases.
        J Neurosurg. 1986; 64: 537-542
        • Hochberg FH
        • Fisher CM
        • Roberson GH
        Subarachnoid hemorrhage caused by rupture of a small superficial artery.
        Neurology. 1974; 24: 319-321
        • Tatter SB
        • Buonanno FS
        • Ogilvy CS
        Acute lacunar stroke in association with angiogram-negative subarachnoid hemorrhage: mechanistic implications of two cases.
        Stroke. 1995; 26: 891-895
        • Rogg JM
        • Smcaton S
        • Doberstein C
        • Goldstein JH
        • Tung GA
        • Haas RA
        Assessment of the value of MR imaging for examining patients with angiographically negative subarachnoid hemorrhage.
        AJR Am JRoentgenol. 1999; 172: 201-206
        • Wijdicks EFM
        • Schievink WI
        • Miller GM
        MR imaging in pretruncal nonaneurysmal subarachnoid hemorrhage: is it worthwhile?.
        Stroke. 1998; 29: 2514-2516
        • Kuker W
        • Thiex R
        • Block F
        Hyperacute perimesencephalic subarachnoid hemorrhage: demonstration of blood extravasation with MRI.V.
        Comput Assist Tomogr. 1999; 23: 521-523
        • Mokri B
        Dissections of cervical and cephalic arteries.
        in: Meyer FB Sundt's Occlusive CerebrovascularDisease. 2nd ed. WB Saunders Co, Philadelphia, Pa1994: 45-70
        • Yamada T
        • Tada S
        • Harada J
        Aortic dissection without intimai rupture: diagnosis with MR imaging and CT.
        Radiology. 1988; 168: 347-352
        • Coady MA
        • Rizzo JA
        • Elefteriades JA
        Pathologic variants of thoracic aortic dissections: penetrating atherosclerotic ulcers and intramural hematomas.
        Cardiol Clin. 1999; 17: 637-657
        • Atkinson JLD
        • Okazaki H
        • Sundt Jr, TM
        • Nichols DA
        • Rufcnacht DA
        Intracranial cerebrovascular vasa vasorum associated with atherosclerosis and large thick-walled aneurysms.
        Surg Neurol. 1991; 36: 365-369
        • Takaba M
        • Endo S
        • Kurimoto M
        • Kuwayama N
        • Nishijima M
        • Takaku A
        Vasa vasorum of the intracranial arteries.
        Ada Neurochir (Wien). 1998; 140: 411-416
        • Rinkel GJE
        Perimesencephalic Nonancurysmal Hemorrhage [thesis]. University of Utrecht, Utrecht, the Netherlands1991
        • Jafar JJ
        • Weiner HL
        Surgery for angiographically occult cerebral aneurysms.
        J Neurosurg. 1993; 79: 674-679
        • Tatter SB
        • Crowell RM
        • Ogilvy CS
        Ancurysmal and micro-aneurysm'al “angiogram-negative” subarachnoid hemorrhage.
        Neurosurgery. 1995; 37: 48-55
        • Ohmi M
        • Tabayashi K
        • Moizumi Y
        • Komatsu T
        • Sekino Y
        • Goko C
        Extremely rapid regression of aortic intramural hemaloma.
        J Thorac Cardiovasc Surg. 1999; 118: 968-969