Skip to main content
AAN.com
Articles
March 23, 2011
Letter to the Editor

The outer arterial wall layers are primarily affected in spontaneous cervical artery dissection

April 26, 2011 issue
76 (17) 1463-1471

Abstract

Objective:

To evaluate the macroscopic and microscopic phenotype of the distal superficial temporal artery (STA) in patients with spontaneous cervical artery dissection (sCAD, n = 14). Arteries of accident victims, free of clinically apparent vascular disease, served as reference samples (n = 9).

Methods:

Specimens of distal STA branches were obtained by biopsy or at autopsy. Their fine and ultrafine structure was documented by close-up photography of native STA branches, light microscopy, and electron microscopy in a case-control study.

Results:

STA specimens from patients with sCAD revealed pathologic changes mainly in the adventitial and medial layers. In these areas, vacuolar degeneration and fissuring were associated with neoangiogenesis of capillaries and microscopic erythrocyte extravasation into the connective tissue. In addition, some specimens showed overt microhematomas close to the medial/adventitial border visible at low magnification. The reference arteries showed virtually no pathologic changes in the outer arterial layers.

Conclusion:

Bearing in mind that the STA is only a surrogate for the cervical arteries affected by sCAD, we propose the following pathogenetic model. We hypothesize that sCAD affects primarily the outer arterial layers. The process starts with degenerative changes at the medial-adventitial border associated with neoangiogenesis of capillary vessels branching from vasa vasorum in the adventitia. Leakage of neoangiogenetic capillaries releases blood cells into the connective tissue and leads to formation of microhematomas along the medial/adventitial border, as well as disintegration of the medial and adventitial texture. Microhematomas might then cause successive rupture of multiple neoangiogenetic capillaries and vasa vasorum, ultimately resulting in dissection.

Get full access to this article

View all available purchase options and get full access to this article.

Supplementary Material

File (voker.pdf)

REFERENCES

1.
Bachmann R, Nassenstein I, Kooijman H, et al. Spontaneous acute dissection of the internal carotid artery: high-resolution magnetic resonance imaging at 3.0 Tesla with a dedicated surface coil. Invest Radiol 2006;41:105–111.
2.
Schievink WI. Spontaneous dissection of the carotid and vertebral arteries. N Engl J Med 2001;344:898–906.
3.
Biousse V, D'Anglejan-Chatillon J, Touboul PJ, Amarenco P, Bousser MG. Time course of symptoms in extracranial carotid artery dissections: a series of 80 patients. Stroke 1995;26:235–239.
4.
Dziewas R, Konrad C, Drager B, et al. Cervical artery dissection: clinical features, risk factors, therapy and outcome in 126 patients. J Neurol 2003;250:1179–1184.
5.
Arnold M, Kappeler L, Georgiadis D, et al. Gender differences in spontaneous cervical artery dissection. Neurology 2006;67:1050–1052.
6.
Dittrich R, Nassenstein I, Bachmann R, et al. Polyarterial clustered recurrence of cervical artery dissection seems to be the rule. Neurology 2007;69:180–186.
7.
Völker W, Besselmann M, Dittrich R, et al. Generalized arteriopathy in patients with cervical artery dissection. Neurology 2005;64:1508–1513.
8.
Volker W, Kuhlenbaumer G, Dittrich R, et al. Two sets of identical twins with cervical artery dissection concordant for temporal artery pathology. Neurology 2008;71:1035–1037.
9.
El-Hamamsy I, Yacoub MH. Cellular and molecular mechanisms of thoracic aortic aneurysms. Nat Rev Cardiol 2009;6:771–786.
10.
Boor PJ, Yang Y, Gong B. Role of the media in vascular injury: atherosclerosis and dissection. Toxicol Pathol 2006;34:33–38.
11.
Maiellaro K, Taylor WR. The role of the adventitia in vascular inflammation. Cardiovasc Res 2007;75:640–648.
12.
Arnold M, De Marchis GM, Stapf C, et al. Triple and quadruple spontaneous cervical artery dissection: presenting characteristics and long-term outcome. J Neurol Neurosurg Psychiatry 2009;80:171–174.
13.
Debette S, Leys D. Cervical-artery dissections: predisposing factors, diagnosis, and outcome. Lancet Neurol 2009;8:668–678.
14.
Grau AJ, Brandt T, Buggle F, et al. Association of cervical artery dissection with recent infection. Arch Neurol 1999;56:851–856.
15.
Bachmann R, Nassenstein I, Kooijman H, et al. High-resolution magnetic resonance imaging (MRI) at 3.0 Tesla in the short-term follow-up of patients with proven cervical artery dissection. Invest Radiol 2007;42:460–466.
16.
Vertinsky AT, Schwartz NE, Fischbein NJ, Rosenberg J, Albers GW, Zaharchuk G. Comparison of multidetector CT angiography and MR imaging of cervical artery dissection. AJNR Am J Neuroradiol 2008;29:1753–1760.
17.
Dittrich R, Rohsbach D, Heidbreder A, et al. Mild mechanical traumas are possible risk factors for cervical artery dissection. Cerebrovasc Dis 2007;23:275–281.
18.
Grond-Ginsbach C, Pjontek R, Aksay SS, Hyhlik-Durr A, Bockler D, Gross-Weissmann ML. Spontaneous arterial dissection: phenotype and molecular pathogenesis. Cell Mol Life Sci 2010;67:1799–1815.
19.
Nesi G, Anichini C, Tozzini S, Boddi V, Calamai G, Gori F. Pathology of the thoracic aorta: a morphologic review of 338 surgical specimens over a 7-year period. Cardiovasc Pathol 2009;18:134–139.
20.
Kamineni R, Sadhu A, Alpert JS. Spontaneous coronary artery dissection: report of two cases and a 50-year review of the literature. Cardiol Rev 2002;10:279–284.
21.
Evangelista A, Mukherjee D, Mehta RH, et al. Acute intramural hematoma of the aorta: a mystery in evolution. Circulation 2005;111:1063–1070.
22.
He R, Guo DC, Estrera AL, et al. Characterization of the inflammatory and apoptotic cells in the aortas of patients with ascending thoracic aortic aneurysms and dissections. J Thorac Cardiovasc Surg 2006;131:671–678.
Letters to the Editor
8 August 2011
The outer arterial wall layers are primarily affected in spontaneous cervical artery dissection
Joshua Z Willey

I read the article by Volker et al. who provided interesting evidence of a pathological process affecting the tunica media and adventitia as the nidus for cervical artery dissection. [1]

Their work appears to be consistent with coronary artery and thoracic aortic dissection. However, the authors do not discuss dissection of the intracranial arteries, where a different vascular layer may be affected depending on the nature of the presentation. These arteries are histologically different from extracranial arteries where the media is thinner and there is no external elastic lamina. [2]

Patients with subarachnoid hemorrhage due to intracranial dissection may present with subarachnoid hemorrhage, where the plane of dissection is considered subadventitial; patients with ischemic stroke present with subintimal dissection. [3] It has been shown that patients with subintimal dissection and ischemia do not progress to hemorrhage even if treated with anticoagulation. [4] It would be interesting to know if the authors believe that their proposed pathogenic pathway would be applicable in intracranial dissection, whether presenting with ischemia or hemorrhage.

Due to the different morphology of the arteries, it is possible that a different pathogenic process is occurring in intracranial artery dissection.

References

1 Volker W, Dittrich R, Grewe S, et al. The outer arterial wall layers are primarily affected in spontaneous cervical artery dissection. Neurology 2011;76: 1463-1471.

2. Li S, Yan B, Kaye A, et al. Prognosis of intracranial dissection relates to site and presenting features. J Clin Neurosci 2011 Apr 18. [Epub ahead of print]

3 Ohkuma H, Suzuki S, Ogane K; Study Group of the Association of Cerebrovascular Disease in Tohoku, Japan. Dissecting aneurysms of intracranial carotid circulation. Stroke 2002;33:941-947.

4. Metso TM, Metso AJ, Helenius J, et al. Prognosis and safety of anticoagulation in intracranial artery dissections in adults. Stroke 2007;38:1837-1842.

Disclosure: Dr. Willey received financial compensation from the American College of Physicians and has received research support from the NINDS and NIH.

8 August 2011
Reply from the authors
Ralf Dittrich
Gregor Kuhlenbaeumer ([email protected]) and E. Bernd Ringelstein ([email protected])

We thank Dr. Willey for his comments. We did not mention intracranial dissections because we did not examine superficial temporal artery biopsies of patients with intracranial dissection. However, we think that the pathophysiological mechanisms of dissection may be different.

The key point is the different anatomy of intradural arteries so it may be preferable to differentiate between extra- and intradural dissections instead of extra- and intracranial dissections. Dr. Willey mentioned that these arteries have an up to 30% thinner Tunica muscularis and Tunica adventitia and a missing Lamina elastica externa. [5] In autopsy studies, both mechanisms of subintimal dissection and subadventitial dissection have been described. [6,7]

The clinical consequences of an arterial occlusion in case of a subintimal dissection and arterial rupture in case of a subadventitial dissection correspond to these different pathophysiological mechanisms. [8] However, we think that no firm conclusions can be drawn from these findings in a small patient series.

References

5. Yonas H, Agamonolis D, Takaoka Y, White RJ. Dissecting intracranial aneurysms. Surg Neurol 1977;8:407-415.

6. Yamaura A, Ono J. Current diagnosis and treatment of intracranial dissecting aneurysms. Neurosurg Q 1994;4:67-81.

7. Yamaura A, Ono J, Hirai S. Clinical picture of intracranial non- traumatic dissecting aneurysm. Neuropathology 2000;20:85-90.

8. Sasaki O, Ogawa H, Koike T, Koizumi T, Tanaka R. A clinicopathological study of dissecting aneurysms of the intracranial vertebral artery. J Neurosurg 1999;75:874-882.

Disclosures: See original article for full disclosure list.

Information & Authors

Information

Published In

Neurology®
Volume 76Number 17April 26, 2011
Pages: 1463-1471
PubMed: 21430296

Publication History

Received: July 21, 2010
Accepted: January 11, 2011
Published online: March 23, 2011
Published in print: April 26, 2011

Permissions

Request permissions for this article.

Disclosure

Dr. Völker, Dr. Dittrich, Dr. Grewe, and Dr. Nassenstein report no disclosures. Prof. Csiba has served on scientific advisory boards for Rocket AF and the Stroke Prevention in Atrial Fibrillation Alliance; serves on editorial advisory boards for International Journal of Stoke, Frontiers in Stroke, and Stroke (through June 2010); and has received research support from the Hungarian Ministry of Health and OTKA (Hungarian Research Fund). Dr. Herczeg, Dr. Borsay, and Prof. Robenek report no disclosures. Prof. Kuhlenbäumer receives research support from the Deutsche Forschungsgemeinschaft (DFG) and is a member of the DFG Cluster of Excellence. Prof. Ringelstein has served on scientific advisory boards for Deutsche Schlaganfall-Gesellschaft (DSG), Boehringer Ingelheim, Bayer Schering Pharma, and sanofi-aventis; serves on the editorial advisory board of Klinische Neurophysiologie; has served as a consultant for Boehringer Ingelheim, Sygnis, Neurobiological Technologies, Novartis, Novo Nordisk, sanofi-aventis, Solvay Pharmaceuticals, Inc., Bayer Schering Pharma, M's Science, SERVIER, UCB, and Trommsdorf; and has received speaker honoraria from Boehringer Ingelheim, sanofi-aventis, and Bayer Schering Pharma.

Authors

Affiliations & Disclosures

W. Völker, PhD*
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
R. Dittrich, MD*
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
S. Grewe, MD
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
I. Nassenstein, MD
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
L. Csiba, MD
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
L. Herczeg, MD
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
B.A. Borsay, MD
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
H. Robenek, PhD
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
G. Kuhlenbäumer, MD, PhD*
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.
E.B. Ringelstein, MD*
From the Departments of Neurology (W.V., R.D., E.B.R.), Ophthalmology (S.G.), and Clinical Radiology (I.N.), University of Münster; Department of Cell Biology and Ultrastructure Research (W.V., H.R.), Leibniz Institute for Arteriosclerosis Research at the University of Münster, Germany; Departments of Neurology (L.C.) and Forensic Medicine (L.H., B.A.B.), Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Hungary; and Institute of Experimental Medicine (G.K.), University of Kiel, Germany.

Notes

*
These authors contributed equally to this work.
Study funding: Supported by Competence Net Stroke, Germany (BMBF), the “Innovative Medizinische Forschung” (IMF) of the Medical Faculty of the University of Münster, and the Neuromedical Foundation, Münster. G.K. is a member of the DFG Cluster of Excellence “Inflammation at Interfaces.”
Address correspondence and reprint requests to Dr. Ralf Dittrich, Department of Neurology, University Hospital of Münster, Albert-Schweitzer-Strasse 33, 48129 Münster, Germany [email protected]

Author Contributions

W. Völker and H. Robenek: Investigation of the superficial temporal artery biopsy specimens by macroscopic, microscopic, and electron microscopic techniques and writing the manuscript. R. Dittrich and I. Nassenstein: Clinical and radiological investigation of the patients with cervical artery dissection, treatment of the patients, and writing the manuscript. S. Grewe: Performing the biopsies in patients with cervical artery dissection. L. Csiba, L. Herczeg, V. Szilvia, B.A. Borsay: Autopsy of the accident victims and performance of the biopsies in these persons and writing parts of the manuscript. G. Kuhlenbäumer, E.B. Ringelstein: Idea for the study, writing and correction of the manuscript. The study design, collection, analysis, and interpretation of the data, as well as writing the manuscript, were exclusive responsibilities of the authors. In particular, the funding sources—the Competence Net Stroke, Germany (BMBF); the “Innovative Medizinische Forschung” (IMF) of the Medical Faculty of the University of Münster; the Neuromedical Foundation, Münster; and the DFG Cluster of Excellence “Inflammation at Interfaces”—had neither influence on the preparation of this manuscript nor the decision to submit it for publication. All authors have access to all data in the study and held final responsibility for the decision to submit for publication.

Metrics & Citations

Metrics

Citations

Download Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Select your manager software from the list below and click Download.

Cited By
  1. Stylohyoid Chain Syndrome (Eagle Syndrome) in Conjunction with Carotid Artery Dissection: A Case Report of Surgical Treatment, Diseases, 12, 1, (24), (2024).https://doi.org/10.3390/diseases12010024
    Crossref
  2. High risk and low prevalence diseases: Spontaneous cervical artery dissection, The American Journal of Emergency Medicine, 76, (55-62), (2024).https://doi.org/10.1016/j.ajem.2023.11.011
    Crossref
  3. Unraveling the Links between Chronic Inflammation, Autoimmunity, and Spontaneous Cervicocranial Arterial Dissection, Journal of Clinical Medicine, 12, 15, (5132), (2023).https://doi.org/10.3390/jcm12155132
    Crossref
  4. Traumatic dissection of the anterior cerebral artery secondary to a rugby related impact: A case report with emphasis on the usefulness of T1-VISTA, Surgical Neurology International, 14, (43), (2023).https://doi.org/10.25259/SNI_1082_2022
    Crossref
  5. Cervical Artery Dissection, CONTINUUM: Lifelong Learning in Neurology, 29, 2, (540-565), (2023).https://doi.org/10.1212/CON.0000000000001233
    Crossref
  6. Clinical characteristics and outcome in expansive compared with steno-occlusive mural hematoma in spontaneous cervical artery dissection, International Journal of Stroke, 18, 10, (1186-1192), (2023).https://doi.org/10.1177/17474930231185032
    Crossref
  7. Intimal Injury Potentially Plays a Key Role in the Formation of Carotid Artery Dissection: A Novel Animal Model Establishing, Cerebrovascular Diseases, (1-9), (2023).https://doi.org/10.1159/000531657
    Crossref
  8. Imaging of Vertebral Artery Dissection in Children: An Underrecognized Condition with High Risk of Recurrent Stroke, RadioGraphics, 43, 12, (2023).https://doi.org/10.1148/rg.230107
    Crossref
  9. Progress in the treatment of chronic intracranial large artery occlusion: Time for large, randomized trials?, Brain Hemorrhages, 4, 4, (204-209), (2023).https://doi.org/10.1016/j.hest.2022.10.009
    Crossref
  10. Belastendes Beweismaterial für die Rolle der Mikrozirkulation bei der Atherosklerose, Atherosklerose-Pathogenese und mikrovaskuläre Dysfunktion, (59-79), (2023).https://doi.org/10.1007/978-3-031-31766-8_4
    Crossref
  11. See more
Loading...

View Options

Get Access

Login options

Check if you have access through your login credentials or your institution to get full access on this article.

Personal login Institutional Login
Purchase Options

Purchase this article to get full access to it.

Purchase Access, $39 for 24hr of access

View options

Full Text

View Full Text

Full Text HTML

View Full Text HTML

Media

Figures

Other

Tables

Share

Share

Share article link

Share