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Traumatic bilateral vertebral artery dissection
Forensic Science International 214 (2012) e12–e15
Contents lists available at ScienceDirect
Forensic Science International journal homepage: www.elsevier.com/locate/forsciint
Case report
Traumatic bilateral vertebral artery dissection Ignasi Galte´s a,*, Juan Carlos Borondo b, Mo`nica Cos c, Merce` Subirana a, Carles Martı´n a, Josep Castella` a, Jordi Medallo a a
Institut de Medicina Legal de Catalunya, Ciutat de la Justı´cia n8 111, Edifici G, Gran Via de les Corts Catalanes, 08075 Barcelona, Catalonia, Spain Instituto Nacional de Toxicologı´a Barcelona, Departamento de Anatomı´a Patolo´gica, C/Merce` n8 1, 08014 Barcelona, Catalonia, Spain c Institut de Diagno`stic per la Imatge (IDI), Hospital Universitari de Bellvitge, 08907 L’Hospitalet de Llobregat, Barcelona, Catalonia, Spain b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 July 2010 Received in revised form 29 March 2011 Accepted 1 July 2011 Available online 27 July 2011
Traumatic vertebral artery dissection is not often seen by forensic pathologists, and cases investigated are scarce in the forensic literature. We present the case of a 40-year-old woman cyclist who was struck by a car while wearing a helmet, and was neurologically near normal immediately thereafter at Emergency. She presented 48 h later with acute right hemiparesis, decreasing level of consciousness, and unsteadiness. CT revealed massive cerebellar infarction. CT angiography was normal. The patient died in coma 7 days after injury and autopsy revealed bilateral edematous cerebellar infarction and bilateral vertebral artery dissection. Rotational neck injury and mural tear in the wall of the Atlantic parts of both vertebral arteries is suggested as the possible mechanism of the arterial injury. Head and neck injuries are reported as a precipitating cause of vertebral artery injury. The possible influence of trauma may be further underestimated if longer intervals between vessel dissection and ischemia occur. The current case illustrates that ‘‘talk-and-die’’ syndrome may be due to occult vertebral artery dissection, possibly bilateral. In forensic cases of delayed death after mild trauma to the head and neck, the vertebral arteries should be examined for the cause of death. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Forensic pathology Cervical spine Neck injuries Neuropathology Vertebral artery injury
1. Introduction Traumatic vertebral artery dissection is not often seen by forensic pathologists, and cases investigated are scarce in the forensic literature. The infrequent diagnosis of this injury may be due to the fact that it is indeed rare, or due to the fact that vertebral artery dissection is rarely carried out at autopsy. Alternatively, such injury may be considered rare because its manifestations are unclear or mainly attributed to primary brain damage and therefore is only infrequently suspected and diagnosed. Forensic autopsy examination should consider vertebral artery dissection as a cause of delayed death in cases of ‘‘talk and die syndrome’’. Thus, vertebral artery dissection can occur after relatively minor head and neck injuries producing no initial coma [1]. Precipitating events are mainly associated with minor indirect mechanisms causing hyperextension or sudden rotation of the neck such as motor vehicle accidents [2], surgical and anaesthesia procedures [3,4], chiropractic manipulation [5], or sports activities [6]. To illustrate the importance of recognizing rotational neck injury after a relatively minor helmeted head trauma, we report a
* Corresponding author at: Servei de Patologia Forense Zona Nord- Collserola, Institut de Medicina Legal de Catalunya, Ctra. Nacional 150, Km. 1,5- Montcada i Reixac, Spain. Tel.: +34 93 575 42 24; fax: +34 93 575 05 65. E-mail address: [email protected] (I. Galte´s). 0379-0738/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2011.07.005
fatal case of a young woman who developed bilateral vertebral artery dissection following cranio-cervical trauma secondary to a bicycle accident. 2. Case report A 40-yeard-old Caucasian woman was involved in a frontal collision between a car and her bicycle. The victim wore a helmet, and she was thrown on to the bonnet of the car and rolled up to the windscreen, causing head trauma with brief loss of consciousness. On arrival at hospital emergency department, neurological examination revealed almost normal findings. Computed Tomography (CT) scan of the brain was normal. CT at the C7 level revealed soft-tissue swelling of the neck and spinous process fracture. She was transferred to the observation unit. At 48 h post injury, she presented with acute right hemiparesis, decreasing level of consciousness, unsteadiness, and difficulty swallowing. CT revealed massive cerebellar infarction. CT angiography (CTA) depicted no radiological abnormality (Fig. 1). The patient was transferred to the critical care unit. In spite of medical treatment, increasing intracranial pressure led to tonsillar herniation, and the patient died 7 days after injury in an irreversible comatose state. At medico-legal autopsy, external examination showed multiple areas of bruising on the face and upper limbs. Internal examination revealed no skull fracture, nor injuries of the
I. Galte´s et al. / Forensic Science International 214 (2012) e12–e15
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Fig. 1. Computed tomography image reveals large area of cerebellar hypodensity (A, arrowheads). CT angiography depicted no radiological abnormality (B).
meninges. No injuries in the intracranial vessels were observed. The brain weighed 1420 g. Gross evaluation after fixation revealed softening and swelling of both cerebellar hemispheres, with massive haemorrhagic/ischemic lesions involving both cortex and white matter. The cerebral hemispheres showed marked signs of increased intracranial pressure with flattened gyri, left uncal herniation, and dilatation of the supratentorial ventricular system. Tonsillar herniation and central pontine haemorrhage with medullary compression were also present. Autopsy evidence of neck trauma was revealed by dissection of the posterior aspect of the inferior neck which showed intramuscular haemorrhage and examination of the lower cervical spine, which confirmed the fracture of the spinous process of C7. Bilateral haemorrhage in the adventitia of both vertebral arteries was observed at the atlantooccipital (V3) segment. Both vessels were removed and fixed in formaldehyde (10% final concentration) prior to serial transverse section study, which showed bilateral circumferential dissection resulting in severe luminal stenosis (Fig. 2). Neuropathological examination confirmed the macroscopic data, particularly the extent of recent infarction of the cerebellum, with neuronal necrosis, edema and vascular congestion, infiltrate of neutrophil polymorphs and macrophages with early tissue removal in the haemorrhagic/ischemic area noted grossly. General signs of cerebral death were also found on microscopic exam.
Histological study of the vertebral arteries was performed using hematoxylin–eosin stain, Perls’ stain, Movat’s pentachrome, and immunostaining for factor VIII-related antigen, vimentin and CD68+ macrophages using the Envision + system (Dako Cytomation, Glostrup, Denmark). The results showed partial splitting of the wall at the atlanto-occipital (V3) segment of the vertebral arteries, with tearing of the intima and media, and concentric haemorrhagic dissection within the outer layers of the tunica media, resulting in stenosis of the arterial lumen. The dissection tract contained early fibrovascular granulation tissue, with collections of red cells, fibrin, proliferating fibroblasts, early neovascularization changes, and haemosiderin-containing macrophages. No evidence of underlying vasculopathy was observed in either vertebral artery (Fig. 3). 3. Discussion The patient presented cerebellar ischemic symptoms 48 h after sustaining minor head trauma due to frontal collision between a car and her bicycle, dying 7 days later in an irreversible comatose state. The delayed death was due to bilateral traumatic vertebral artery dissection, subsequent massive cerebellar infarction, edema and brainstem compression. Head and neck injuries are reported as a precipitating cause of vertebral artery injury [1]. Application of
Fig. 2. Transverse section of the right (A) and left (B) vertebral arteries at the atlanto-occipital (V3) segment shows circumferential dissection of the wall, resulting in severe luminal stenosis.
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I. Galte´s et al. / Forensic Science International 214 (2012) e12–e15
Fig. 3. Microscopic findings in vertebral arteries. (A) Dissection within the outer layers of the tunica media. The intramural hematoma (H) extends almost entirely around the artery resulting in stenosis of the arterial lumen (L) (HE). (B) Immunostaining of factor VIII reveals the splitting of the wall, with tearing of the intima and media (asterisk). (C) Subadventitial intramural hematoma contained early fibrovascular granulation tissue (HE).
vascular noninvasive radiological techniques in patients with traumatic preceding events, has unmasked a higher incidence of vertebral artery injury than previously thought, suggesting that vertebral artery dissection may be occult. Two recently published series using digital subtraction arteriography as part of an established screening protocol describe the incidence of vertebral artery injury in 0.73 and 0.71% of all blunt traumatic admissions. In total, 605 (4.8%) and 216 (3.5%) patients admitted to their respective centres underwent digital subtraction arteriography, detecting vertebral artery injury in 15 and 20% of cases [7,8]. In the case presented, the mode of injury suggests that the arterial damage may be related to hyperextension and/or neck rotation. Johnson et al. [9] demonstrate a distinct susceptibility of the vertebral artery to longitudinal stretch that may explain why it is injured during these sudden neck movements. Nevertheless,
Auer et al. [2] highlight the importance of the neck rotation in the frontal car–bicycle collision, since this neck movement likely occurs as the victim rolled up the hood of the vehicle after impact. Biomechanical flow experiments show that neck rotation may kink the vertebral artery causing its compression and occlusion [2,10,11]. According to Farag et al. [12], the reversed blood flow induced by sudden vertebral artery occlusion stresses the arterial wall, with subsequent dissection of the artery. As in the present case, kinking and occluding the vertebral artery is more usual at the atlantic parts (segment V3). The vulnerability of this segment has been related to its high mobility, as the artery leaves the transverse foramen of the axis vertebra and changes its direction from vertical to horizontal, after which the artery becomes fixed, being thus very susceptible to strain [1,2,9]. Vertebral artery dissection usually arises from an intimal tear. The tear allows blood under arterial pressure to enter between the layers of the wall of the artery, forming an intramural hematoma, the so-called false lumen [13,14]. The intramural hematoma is usually located within the layers of the tunica media, but it may be eccentric, either toward the intima or toward the adventitia [14]. Moreover, as another suggested mechanism, intramural hematoma forms through ruptures of the vasa vasorum [15,16] without intimal tear, especially if the wall is arteriopathic [17]. In the present case, histological results of the vertebral arteries lead us to suggest an intimal tear as a primary event to form the intramural hematoma. Furthermore, early fibrovascular granulation tissue in the dissection tract allows us to relate vertebral artery dissection with preceding traumatic history. Focal manifestations of vertebral artery dissection include neck pain and occipitocervical headache, while intrinsic brainstem symptoms are suggested by vertigo, nausea and vomiting, unilateral facial numbness or unsteadiness [18]. As in the present case, however, many patients are asymptomatic or had delayed presentations, following after a variable interval by ischemic symptoms [2,19,20]. Thus, the longest case is reported by Devereaux et al. [21], where the patient died after vertebral dissection 8 years following a road traffic accident. Lateral medullary syndrome and cerebellar infarcts are the most common types of strokes. Occasionally, spinal cord infarcts occur because of the involvement of branches of the extracranial vertebral artery that supply the cervical spinal cord [22]. Moreover, more than 50% of intracranial vertebral artery dissections are associated with subarachnoid haemorrhage [23]. Intracranial arteries have fewer elastic fibers in the media, thinner adventitia, and no external elastic membrane, explaining the predisposition to bleed through the rupture of the adventitia [24]. In the case presented, cerebellar infarction was preceded by minor head trauma and C7 spinous process fracture. In the series studied by Miller et al. [7] and Cothren et al. [8], cervical spine fractures were present in more than 70% of patients. The diagnosis of vertebral artery dissection is based on direct visualization of the intramural hematoma and narrowing or occlusion of the arterial lumen. Digital subtraction arteriography is accepted as the gold standard for the diagnosis of vertebral artery dissection during life. CTA and magnetic resonance angiography (MRA) are accepted as the more practical screening methods [1,19]. Intramural hematoma can be directly identified with MRA [25]. In this case, however, CTA was normal and unfortunately MRA was not feasible due to the patient’s clinical condition. In summary, the current case illustrates that delayed death can occur due to occult vertebral artery dissection at the time of a minor head trauma due to frontal car-bicycle collision. Rotational neck injury and mural tear in the wall of the atlantic parts of both vertebral arteries is suggested as the possible mechanism of the arterial injury. Emergency physicians should keep in mind that the internal injury may take hours to appear, and that the patient may
I. Galte´s et al. / Forensic Science International 214 (2012) e12–e15
be at risk of delayed death. Although vertebral artery injury is a rare cause of death in forensic activity, we must always be aware of this diagnosis in the cases of traumatic head and neck injuries, especially if the autopsy reveals an infarction of the cerebellum or lateral medulla, or a predominantly basal subarachnoid haemorrhage. Vertebral artery dissection as a cause of death cannot be ruled out by lucid intervals of time between trauma and death. Vertebral dissection can be bilateral, and can occur after relatively minor craniocervical trauma that produces no initial coma. Examination of the vertebral arteries in traumatic head and neck injuries is an essential component of determination of precise cause of death and to assess the true incidence of this injury, which is likely higher than commonly believed. Acknowledgements The authors are grateful to the anonymous reviewers for their comments and suggestions on the manuscript. Thanks are due to Eduard Aizpun de la Escosura for his help in the revision of English manuscript. References [1] Y.K. Kim, S. Schulman, Cervical artery dissection: pathology, epidemiology and management, Thromb. Res. 123 (2009) 810–821. [2] R.N. Auer, J. Krcek, J.C. Butt, Delayed symptoms and death after minor head trauma with occult vertebral artery injury, J. Neurol. Neurosurg. Psychiat. 57 (1994) 500–502. [3] V. Caso, M. Paciaroni, J. Bogousslavsky, Environmental factors and cervical artery dissection, Front. Neurol. Neurosci. 20 (2005) 44–53. [4] R.D. Dickerman, J.E. Zigler, Atraumatic vertebral artery dissection after cervical corpectomy: a traction injury? Spine 30 (2005) E658–E661. [5] E. Ernst, Deaths after chiropractic: a review of published cases, Int. J. Clin. Pract. 64 (2010) 1162–1165. [6] J.C. Maroon, P. Gardner, A.A. Abla, H. El-Kadi, J. Bost, Golfer’s stroke’’: golf-induced stroke from vertebral artery dissection, Surg. Neurol. 67 (2007) 163–168. [7] P.R. Miller, T.C. Fabian, M.A. Croce, C. Cagiannos, J.S. Williams, M. Vang, W.G. Qaisi, R.E. Felker, S.D. Timmons, Prospective screening for blunt cerebrovascular injuries: analysis of diagnostic modalities and outcomes, Ann. Surg. 236 (2002) 386– 393.
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[8] C.C. Cothren, E.E. Moore, W.L. Biffi, D.J. Ciesla, C.E. Johnson Jr., J.B. Moore, J.M. Burch, Cervical spine fracture patterns predictive of blunt vertebral artery injury, J. Trauma 55 (2003) 811–813. [9] C.P. Johnson, T. How, M. Scraggs, C.R. West, J. Burns, A biomechanical study of the human vertebral artery with implications for fatal arterial injury, Forensic Sci. Int. 109 (2000) 169–182. [10] J.F. Toole, S.H. Tucker, Influence of head position upon cerebral circulation. Studies on blood flow in cadavers, Arch. Neurol. 2 (1960) 616–623. [11] J.W. Barton, M.T. Margolis, Rotational obstructions of the vertebral artery at the atlantoaxial joint, Neuroradiology 9 (1975) 117–120. [12] A.M. Farag, A. Franks, D.J. Gee, Simple laboratory experiments to replicate some of the stresses on vertebro-basilar arterial walls—an investigation of possible mechanisms of traumatic subarachnoid haemorrhage, Forensic Sci. Int. 38 (1988) 275– 284. [13] C.K. Lee, L. Gray, J. Maguire, Traumatic vertebral artery injury. Detailed clinicopathologic and morphometric analysis of 6 cases, Am. J. Forensic Med. Pathol. 30 (2009) 134–136. [14] W.I. Schievink, Spontaneous dissection of the carotid and vertebral arteries, N. Engl. J. Med. 344 (2001) 898–906. [15] R.G. Hart, J.D. Easton, Dissections of cervical and cerebral arteries, Neurol. Clin. 1 (1983) 155–182. [16] W.K. Ehrenfeld, E.J. Wylie, Spontaneous dissection of the internal carotid artery, Arch. Surg. 111 (1976) 1294–1301. [17] W. Vo¨lker, M. Besselmann, R. Dittrich, D. Nabavi, C. Konrad, R. Dziewas, S. Evers, S. Grewe, S.C. Kra¨mer, R. Bachmann, F. Sto¨gbauer, E.B. Ringelstein, G. Kuhlenba¨umer, Generalized arteriopathy in patients with cervical artery dissection, Neurology 64 (2005) 1508–1513. [18] A.B. Saeed, A. Shuaib, G. Al-Sulaiti, D. Emery, Vertebral artery dissection: warning symptoms, clinical features and prognosis in 26 patients, Can. J. Neurol. Sci. 27 (2000) 292–296. [19] M.T. McCormick, H.K. Robinson, I. Bone, A.N. McLean, D.B. Allan, Blunt cervical spine trauma as a cause of spinal cord injury and delayed cortical blindness, Spinal Cord 45 (2007) 687–689. [20] F.S. Nazir, K.W. Muir, Prolonged interval between vertebral artery dissection and ischemic stroke, Neurology 62 (2004) 1646–1647. [21] M.W. Devereaux, J.R. Keane, R.L. Davis, Automatic respiratory failure associated with infarction of the medulla. Report of two cases with pathologic study of one, Arch. Neurol. 29 (1973) 46–52. [22] K.W. Park, J.S. Park, S.Ch. Hwang, S.B. Im, W.H. Shin, B.T. Kim, Vertebral artery dissection: natural history, clinical features and therapeutic considerations, J. Korean Neurosurg. Soc. 44 (2008) 109–115. [23] B. Thanvi, S.K. Munshi, S.L. Dawson, T.G. Robinson, Carotid and vertebral artery dissection sindromes, Postgrad. Med. J. 81 (2005) 383–388. [24] O. Pelkonen, T. Tikkakoski, J. Pyhtinen, K. Sotaniemi, Cerebral CT and MRI findings in cervicocephalic artery dissection, Acta Radiol. 45 (2004) 259–265. [25] A. Auer, S. Felber, C. Schmidauer, P. Waldenberger, F. Aichner, Magnetic resonance angiographic and clinical features of extracranial vertebral artery dissection, J. Neurol. Neurosurg. Psychiatry 64 (1998) 474–481.
Contents lists available at ScienceDirect
Forensic Science International journal homepage: www.elsevier.com/locate/forsciint
Case report
Traumatic bilateral vertebral artery dissection Ignasi Galte´s a,*, Juan Carlos Borondo b, Mo`nica Cos c, Merce` Subirana a, Carles Martı´n a, Josep Castella` a, Jordi Medallo a a
Institut de Medicina Legal de Catalunya, Ciutat de la Justı´cia n8 111, Edifici G, Gran Via de les Corts Catalanes, 08075 Barcelona, Catalonia, Spain Instituto Nacional de Toxicologı´a Barcelona, Departamento de Anatomı´a Patolo´gica, C/Merce` n8 1, 08014 Barcelona, Catalonia, Spain c Institut de Diagno`stic per la Imatge (IDI), Hospital Universitari de Bellvitge, 08907 L’Hospitalet de Llobregat, Barcelona, Catalonia, Spain b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 July 2010 Received in revised form 29 March 2011 Accepted 1 July 2011 Available online 27 July 2011
Traumatic vertebral artery dissection is not often seen by forensic pathologists, and cases investigated are scarce in the forensic literature. We present the case of a 40-year-old woman cyclist who was struck by a car while wearing a helmet, and was neurologically near normal immediately thereafter at Emergency. She presented 48 h later with acute right hemiparesis, decreasing level of consciousness, and unsteadiness. CT revealed massive cerebellar infarction. CT angiography was normal. The patient died in coma 7 days after injury and autopsy revealed bilateral edematous cerebellar infarction and bilateral vertebral artery dissection. Rotational neck injury and mural tear in the wall of the Atlantic parts of both vertebral arteries is suggested as the possible mechanism of the arterial injury. Head and neck injuries are reported as a precipitating cause of vertebral artery injury. The possible influence of trauma may be further underestimated if longer intervals between vessel dissection and ischemia occur. The current case illustrates that ‘‘talk-and-die’’ syndrome may be due to occult vertebral artery dissection, possibly bilateral. In forensic cases of delayed death after mild trauma to the head and neck, the vertebral arteries should be examined for the cause of death. ß 2011 Elsevier Ireland Ltd. All rights reserved.
Keywords: Forensic pathology Cervical spine Neck injuries Neuropathology Vertebral artery injury
1. Introduction Traumatic vertebral artery dissection is not often seen by forensic pathologists, and cases investigated are scarce in the forensic literature. The infrequent diagnosis of this injury may be due to the fact that it is indeed rare, or due to the fact that vertebral artery dissection is rarely carried out at autopsy. Alternatively, such injury may be considered rare because its manifestations are unclear or mainly attributed to primary brain damage and therefore is only infrequently suspected and diagnosed. Forensic autopsy examination should consider vertebral artery dissection as a cause of delayed death in cases of ‘‘talk and die syndrome’’. Thus, vertebral artery dissection can occur after relatively minor head and neck injuries producing no initial coma [1]. Precipitating events are mainly associated with minor indirect mechanisms causing hyperextension or sudden rotation of the neck such as motor vehicle accidents [2], surgical and anaesthesia procedures [3,4], chiropractic manipulation [5], or sports activities [6]. To illustrate the importance of recognizing rotational neck injury after a relatively minor helmeted head trauma, we report a
* Corresponding author at: Servei de Patologia Forense Zona Nord- Collserola, Institut de Medicina Legal de Catalunya, Ctra. Nacional 150, Km. 1,5- Montcada i Reixac, Spain. Tel.: +34 93 575 42 24; fax: +34 93 575 05 65. E-mail address: [email protected] (I. Galte´s). 0379-0738/$ – see front matter ß 2011 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2011.07.005
fatal case of a young woman who developed bilateral vertebral artery dissection following cranio-cervical trauma secondary to a bicycle accident. 2. Case report A 40-yeard-old Caucasian woman was involved in a frontal collision between a car and her bicycle. The victim wore a helmet, and she was thrown on to the bonnet of the car and rolled up to the windscreen, causing head trauma with brief loss of consciousness. On arrival at hospital emergency department, neurological examination revealed almost normal findings. Computed Tomography (CT) scan of the brain was normal. CT at the C7 level revealed soft-tissue swelling of the neck and spinous process fracture. She was transferred to the observation unit. At 48 h post injury, she presented with acute right hemiparesis, decreasing level of consciousness, unsteadiness, and difficulty swallowing. CT revealed massive cerebellar infarction. CT angiography (CTA) depicted no radiological abnormality (Fig. 1). The patient was transferred to the critical care unit. In spite of medical treatment, increasing intracranial pressure led to tonsillar herniation, and the patient died 7 days after injury in an irreversible comatose state. At medico-legal autopsy, external examination showed multiple areas of bruising on the face and upper limbs. Internal examination revealed no skull fracture, nor injuries of the
I. Galte´s et al. / Forensic Science International 214 (2012) e12–e15
e13
Fig. 1. Computed tomography image reveals large area of cerebellar hypodensity (A, arrowheads). CT angiography depicted no radiological abnormality (B).
meninges. No injuries in the intracranial vessels were observed. The brain weighed 1420 g. Gross evaluation after fixation revealed softening and swelling of both cerebellar hemispheres, with massive haemorrhagic/ischemic lesions involving both cortex and white matter. The cerebral hemispheres showed marked signs of increased intracranial pressure with flattened gyri, left uncal herniation, and dilatation of the supratentorial ventricular system. Tonsillar herniation and central pontine haemorrhage with medullary compression were also present. Autopsy evidence of neck trauma was revealed by dissection of the posterior aspect of the inferior neck which showed intramuscular haemorrhage and examination of the lower cervical spine, which confirmed the fracture of the spinous process of C7. Bilateral haemorrhage in the adventitia of both vertebral arteries was observed at the atlantooccipital (V3) segment. Both vessels were removed and fixed in formaldehyde (10% final concentration) prior to serial transverse section study, which showed bilateral circumferential dissection resulting in severe luminal stenosis (Fig. 2). Neuropathological examination confirmed the macroscopic data, particularly the extent of recent infarction of the cerebellum, with neuronal necrosis, edema and vascular congestion, infiltrate of neutrophil polymorphs and macrophages with early tissue removal in the haemorrhagic/ischemic area noted grossly. General signs of cerebral death were also found on microscopic exam.
Histological study of the vertebral arteries was performed using hematoxylin–eosin stain, Perls’ stain, Movat’s pentachrome, and immunostaining for factor VIII-related antigen, vimentin and CD68+ macrophages using the Envision + system (Dako Cytomation, Glostrup, Denmark). The results showed partial splitting of the wall at the atlanto-occipital (V3) segment of the vertebral arteries, with tearing of the intima and media, and concentric haemorrhagic dissection within the outer layers of the tunica media, resulting in stenosis of the arterial lumen. The dissection tract contained early fibrovascular granulation tissue, with collections of red cells, fibrin, proliferating fibroblasts, early neovascularization changes, and haemosiderin-containing macrophages. No evidence of underlying vasculopathy was observed in either vertebral artery (Fig. 3). 3. Discussion The patient presented cerebellar ischemic symptoms 48 h after sustaining minor head trauma due to frontal collision between a car and her bicycle, dying 7 days later in an irreversible comatose state. The delayed death was due to bilateral traumatic vertebral artery dissection, subsequent massive cerebellar infarction, edema and brainstem compression. Head and neck injuries are reported as a precipitating cause of vertebral artery injury [1]. Application of
Fig. 2. Transverse section of the right (A) and left (B) vertebral arteries at the atlanto-occipital (V3) segment shows circumferential dissection of the wall, resulting in severe luminal stenosis.
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Fig. 3. Microscopic findings in vertebral arteries. (A) Dissection within the outer layers of the tunica media. The intramural hematoma (H) extends almost entirely around the artery resulting in stenosis of the arterial lumen (L) (HE). (B) Immunostaining of factor VIII reveals the splitting of the wall, with tearing of the intima and media (asterisk). (C) Subadventitial intramural hematoma contained early fibrovascular granulation tissue (HE).
vascular noninvasive radiological techniques in patients with traumatic preceding events, has unmasked a higher incidence of vertebral artery injury than previously thought, suggesting that vertebral artery dissection may be occult. Two recently published series using digital subtraction arteriography as part of an established screening protocol describe the incidence of vertebral artery injury in 0.73 and 0.71% of all blunt traumatic admissions. In total, 605 (4.8%) and 216 (3.5%) patients admitted to their respective centres underwent digital subtraction arteriography, detecting vertebral artery injury in 15 and 20% of cases [7,8]. In the case presented, the mode of injury suggests that the arterial damage may be related to hyperextension and/or neck rotation. Johnson et al. [9] demonstrate a distinct susceptibility of the vertebral artery to longitudinal stretch that may explain why it is injured during these sudden neck movements. Nevertheless,
Auer et al. [2] highlight the importance of the neck rotation in the frontal car–bicycle collision, since this neck movement likely occurs as the victim rolled up the hood of the vehicle after impact. Biomechanical flow experiments show that neck rotation may kink the vertebral artery causing its compression and occlusion [2,10,11]. According to Farag et al. [12], the reversed blood flow induced by sudden vertebral artery occlusion stresses the arterial wall, with subsequent dissection of the artery. As in the present case, kinking and occluding the vertebral artery is more usual at the atlantic parts (segment V3). The vulnerability of this segment has been related to its high mobility, as the artery leaves the transverse foramen of the axis vertebra and changes its direction from vertical to horizontal, after which the artery becomes fixed, being thus very susceptible to strain [1,2,9]. Vertebral artery dissection usually arises from an intimal tear. The tear allows blood under arterial pressure to enter between the layers of the wall of the artery, forming an intramural hematoma, the so-called false lumen [13,14]. The intramural hematoma is usually located within the layers of the tunica media, but it may be eccentric, either toward the intima or toward the adventitia [14]. Moreover, as another suggested mechanism, intramural hematoma forms through ruptures of the vasa vasorum [15,16] without intimal tear, especially if the wall is arteriopathic [17]. In the present case, histological results of the vertebral arteries lead us to suggest an intimal tear as a primary event to form the intramural hematoma. Furthermore, early fibrovascular granulation tissue in the dissection tract allows us to relate vertebral artery dissection with preceding traumatic history. Focal manifestations of vertebral artery dissection include neck pain and occipitocervical headache, while intrinsic brainstem symptoms are suggested by vertigo, nausea and vomiting, unilateral facial numbness or unsteadiness [18]. As in the present case, however, many patients are asymptomatic or had delayed presentations, following after a variable interval by ischemic symptoms [2,19,20]. Thus, the longest case is reported by Devereaux et al. [21], where the patient died after vertebral dissection 8 years following a road traffic accident. Lateral medullary syndrome and cerebellar infarcts are the most common types of strokes. Occasionally, spinal cord infarcts occur because of the involvement of branches of the extracranial vertebral artery that supply the cervical spinal cord [22]. Moreover, more than 50% of intracranial vertebral artery dissections are associated with subarachnoid haemorrhage [23]. Intracranial arteries have fewer elastic fibers in the media, thinner adventitia, and no external elastic membrane, explaining the predisposition to bleed through the rupture of the adventitia [24]. In the case presented, cerebellar infarction was preceded by minor head trauma and C7 spinous process fracture. In the series studied by Miller et al. [7] and Cothren et al. [8], cervical spine fractures were present in more than 70% of patients. The diagnosis of vertebral artery dissection is based on direct visualization of the intramural hematoma and narrowing or occlusion of the arterial lumen. Digital subtraction arteriography is accepted as the gold standard for the diagnosis of vertebral artery dissection during life. CTA and magnetic resonance angiography (MRA) are accepted as the more practical screening methods [1,19]. Intramural hematoma can be directly identified with MRA [25]. In this case, however, CTA was normal and unfortunately MRA was not feasible due to the patient’s clinical condition. In summary, the current case illustrates that delayed death can occur due to occult vertebral artery dissection at the time of a minor head trauma due to frontal car-bicycle collision. Rotational neck injury and mural tear in the wall of the atlantic parts of both vertebral arteries is suggested as the possible mechanism of the arterial injury. Emergency physicians should keep in mind that the internal injury may take hours to appear, and that the patient may
I. Galte´s et al. / Forensic Science International 214 (2012) e12–e15
be at risk of delayed death. Although vertebral artery injury is a rare cause of death in forensic activity, we must always be aware of this diagnosis in the cases of traumatic head and neck injuries, especially if the autopsy reveals an infarction of the cerebellum or lateral medulla, or a predominantly basal subarachnoid haemorrhage. Vertebral artery dissection as a cause of death cannot be ruled out by lucid intervals of time between trauma and death. Vertebral dissection can be bilateral, and can occur after relatively minor craniocervical trauma that produces no initial coma. Examination of the vertebral arteries in traumatic head and neck injuries is an essential component of determination of precise cause of death and to assess the true incidence of this injury, which is likely higher than commonly believed. Acknowledgements The authors are grateful to the anonymous reviewers for their comments and suggestions on the manuscript. Thanks are due to Eduard Aizpun de la Escosura for his help in the revision of English manuscript. References [1] Y.K. Kim, S. Schulman, Cervical artery dissection: pathology, epidemiology and management, Thromb. Res. 123 (2009) 810–821. [2] R.N. Auer, J. Krcek, J.C. Butt, Delayed symptoms and death after minor head trauma with occult vertebral artery injury, J. Neurol. Neurosurg. Psychiat. 57 (1994) 500–502. [3] V. Caso, M. Paciaroni, J. Bogousslavsky, Environmental factors and cervical artery dissection, Front. Neurol. Neurosci. 20 (2005) 44–53. [4] R.D. Dickerman, J.E. Zigler, Atraumatic vertebral artery dissection after cervical corpectomy: a traction injury? Spine 30 (2005) E658–E661. [5] E. Ernst, Deaths after chiropractic: a review of published cases, Int. J. Clin. Pract. 64 (2010) 1162–1165. [6] J.C. Maroon, P. Gardner, A.A. Abla, H. El-Kadi, J. Bost, Golfer’s stroke’’: golf-induced stroke from vertebral artery dissection, Surg. Neurol. 67 (2007) 163–168. [7] P.R. Miller, T.C. Fabian, M.A. Croce, C. Cagiannos, J.S. Williams, M. Vang, W.G. Qaisi, R.E. Felker, S.D. Timmons, Prospective screening for blunt cerebrovascular injuries: analysis of diagnostic modalities and outcomes, Ann. Surg. 236 (2002) 386– 393.
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