Pathomorphometry of ruptured intracranial vertebral arterial dissection: adventitial rupture, dilated lesion, intimal tear, and medial defect

Laboratory investigation

Restricted access

Object

Subarachnoid hemorrhage (SAH) due to ruptured intracranial vertebral artery (VA) dissection is a life-threatening disease. Angiographic and symptomatic prognostic factors for rupture and rerupture have been investigated, but the pathological characteristics have not been fully investigated. The authors aimed to investigate these features by performing a pathomorphometic study of ruptured intracranial VA dissections.

Methods

This study included 50 administrative autopsy cases of fatal SAH due to ruptured intracranial VA dissection among 517 fatal nontraumatic cases of SAH occurring between March 2003 and May 2011.

Pathomorphometry was performed using serial 5-μm histological cross-sections with elastica van Gieson staining from each 0.2-mm segment around the ruptured intracranial VA. The longitudinal lengths of 4 types of vascular lesions—adventitial ruptures, dilated lesions where the internal elastic lamina (IEL) was ruptured with adventitial extension, intimal tears where the IEL was ruptured, and medial defects—were calculated based on the numbers of the slides in which these lesions were continuously detected (minimum 2 adjoining slides). The distance from the vertebrobasilar junction to the center of adventitial rupture was also calculated in 37 cases.

Results

All cases showed one adventitial rupture with a mean length of about 1.9 ± 1.1 mm. The center of the adventitial rupture was located 5.0–26.8 mm (mean 14.6 ± 5.5 mm) from the intracranial VA bifurcation. Adventitial ruptures existed in the centers of dilated lesions, where the adventitia was highly extended. Other vascular lesions were serially observed surrounding the adventitial rupture. The mean lengths of dilated lesions, intimal tears, and medial defects were 9.4 ± 4.8 mm, 13.2 ± 6.3 mm, and 15.6 ± 7.2 mm, respectively. The lengths between proximal lesions and distal lesions from the center of the adventitial rupture for both medial defects and intimal tears were significantly longer at proximal lesions than at distal ones (chi-square test, p < 0.01).

Conclusions

Every ruptured intracranial VA dissection has a single point of adventitial rupture where the adventitia was maximally extended, so dilation appears to be a valuable predictive factor for hemorrhagic intracranial VA dissections. The adventitial ruptures were as small as 2 mm in length, and clinically detectable dilated lesions were about 9 mm in length. However, vascular vulnerability caused by IEL ruptures and medial defects existed more widely across a length of VA of 1.3–1.5 cm. Comparatively broader protection of the intracranial VA than the clinically detected area of dissection might be desirable to prevent rebleeding. Broader protection of proximal lesions than distal lesions might be effective from the viewpoint of site distribution of vascular lesions and blood flow alteration to the pseudolumen caused by the dissecting hematoma. Medial defects are the most widely seen lesions among the 4 types of vascular lesions studied. Medial degenerative disease, known as segmental arterial mediolysis, is suspected in the pathogenesis of intracranial VA dissections.

Abbreviations used in this paper:IEL = internal elastic lamina; SAH = subarachnoid hemorrhage; VA = vertebral artery.

Article Information

Address correspondence to: Ayako Ro, M.D., Ph.D., Department of Legal Medicine, Tokyo Women's Medical University, 8-1 Kawada-cho, Shinjuku-ku, Tokyo 162-8666, Japan. email: chaeja@nifty.com.

Please include this information when citing this paper: published online April 12, 2013; DOI: 10.3171/2013.2.JNS121586.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    A representative case of ruptured intracranial VA dissection. A: Macroscopic appearance and schematic of each vascular lesion measured by pathomorphometry. L indicates the distance from the vertebrobasilar junction (VBJ) to the center of the adventitial rupture; R, adventitial rupture; D, intimal tear with adventitial extension (dilated lesion); I, intimal tear; Id, distal lesion of intimal tear; Ip, proximal lesion of intimal tear; M, medial defect; Md, distal lesion medial defect; and Mp, proximal lesion of medial defect. B–D: Representative photomicrographs of the 4 types of vascular lesion shown in A. B: Adventitial rupture. C: Dilated lesion where the IEL is ruptured with adventitial extension. D: Intimal tear without adventitial extension. E: Medial defect. Elastica van Gieson staining, original magnification ×2.

  • View in gallery

    3D segmentation model and longitudinal reconstruction of the ruptured intracranial VA using Avizo 6.1 software (posterior view of the same representative case as that shown in Fig. 1). A: 3D segmentation model around the rupture point, exterior appearance. B: Longitudinal sectional view of A. The adventitia is colored green, the media is colored orange, and the intima is colored yellow. C: Longitudinal reconstruction of serial digital photographs of histological cross-sections around the rupture; same lesion as shown in A and B. Elastica van Gieson, original magnification ×2.

  • View in gallery

    Schema of the suspected pathophysiology of intracranial VA dissections. A: Medial defect occurs for unknown reasons. B: Internal elastic lamina is ruptured and blood pours into the pseudolumen. C: A hematoma grows inwardly into the pseudolumen forming a so-called lesion of “string” or “stenosis.” D: The adventitia gradually becomes dilated from the distal side of the pseudolumen. E: The blood preferentially flows into the dilated pseudolumen. F: The adventitia is ruptured at the most dilated site, resulting in a hemorrhagic intracranial vertebral arterial dissection.

References

1

Kai YHamada JMorioka MOhmori YWatanabe MHirano T: Dissecting aneurysms of the vertebral artery— angiographic patterns at the dissecting site on balloon test occlusion. Neuroradiology 54:8578622012

2

Kai YNishi TWatanabe MMorioka MHirano TYano S: Strategy for treating unruptured vertebral artery dissecting aneurysms. Neurosurgery 69:108510922011

3

Manz HJLuessenhop AJ: Dissecting aneurysm of intracranial vertebral artery: case report and review of literature. J Neurol 230:25351983

4

Matsuda RHironaka YTakeshima YPark YSNakase H: Subarachnoid hemorrhage in a case of segmental arterial mediolysis with coexisting intracranial and intraabdominal aneurysms. Case report. J Neurosurg 116:9489512012

5

Matsukawa HFujii MShinoda MTakahashi OYamamoto DMurakata A: Comparison of clinical characteristics and MR angiography appearance in patients with spontaneous intradural vertebral artery dissection with or without subarachnoid hemorrhage. Clinical article. J Neurosurg 115:1081122011

6

Mizutani T: Natural course of intracranial arterial dissections. Clinical article. J Neurosurg 114:103710442011

7

Mizutani TAruga TKirino TMiki YSaito ITsuchida T: Recurrent subarachnoid hemorrhage from untreated ruptured vertebrobasilar dissecting aneurysms. Neurosurgery 36:9059131995

8

Mizutani TKojima HAsamoto SMiki Y: Pathological mechanism and three-dimensional structure of cerebral dissecting aneurysms. J Neurosurg 94:7127172001

9

Murai TBaba MRo AMurai NMatsuo YTakada A: Sudden death due to cardiovascular disorders: a review of the studies on the medico-legal cases in Tokyo. Keio J Med 50:1751812001

10

Ro AKageyama NAbe NTakatsu AFukunaga T: Intracranial vertebral artery dissection resulting in fatal subarachnoid hemorrhage: clinical and histopathological investigations from a medicolegal perspective. Clinical article. J Neurosurg 110:9489542009

11

Ro AKageyama NHayashi KShigeta AFukunaga T: Nontraumatic rupture of the intracranial vertebral artery of a man found dead in a severe car accident—histopathological differentiation by step-serial sections. Leg Med (Tokyo) 10:1011062008

12

Ro AKageyama NTakatsu AFukunaga T: Segmental arterial mediolysis of varying phases affecting both the intraabdominal and intracranial vertebral arteries: an autopsy case report. Cardiovasc Pathol 19:2482512010

13

Sakata NTakebayashi SShimizu KKojima MMasawa NSuzuki K: A case of segmental mediolytic arteriopathy involving both intracranial and intraabdominal arteries. Pathol Res Pract 198:4934972002

14

Slavin REInada K: Segmental arterial mediolysis with accompanying venous angiopathy: a clinical pathologic review, report of 3 new cases, and comments on the role of endothelin-1 in its pathogenesis. Int J Surg Pathol 15:1211342007

15

Slavin REYaeger MJ: Segmental arterial mediolysis—an iatrogenic vascular disorder induced by ractopamine. Cardiovasc Pathol 21:3343382012

16

Takagi TTakayasu MSuzuki YYoshida J: Prediction of rebleeding from angiographic features in vertebral artery dissecting aneurysms. Neurosurg Rev 30:32392007

17

Yamada MKitahara TKurata AFujii KMiyasaka Y: Intracranial vertebral artery dissection with subarachnoid hemorrhage: clinical characteristics and outcomes in conservatively treated patients. J Neurosurg 101:25302004

18

Yamakawa HKaku YYoshimura SOhkuma ASakai N: Two cases of dissecting aneurysm of the distal posterior inferior cerebellar artery: possible involvement of segmental mediolytic arteriopathy in the pathogenesis. Clin Neurol Neurosurg 107:1171222005

19

Yamaura AOno JHirai S: Clinical picture of intracranial non-traumatic dissecting aneurysm. Neuropathology 20:85902000

20

Yonas HAgamanolis DTakaoka YWhite RJ: Dissecting intracranial aneurysms. Surg Neurol 8:4074151977

TrendMD

Cited By

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 51 51 23
Full Text Views 135 135 20
PDF Downloads 137 137 16
EPUB Downloads 0 0 0

PubMed

Google Scholar