Clinical Investigative Study Posttraumatic Carotid Artery Dissection in Children: Not to be missed! Gunes Orman, MD, Aylin Tekes, MD, Andrea Poretti, MD, Courtney Robertson, MD, Thierry A. G. M. Huisman, MD From the Section of Pediatric Neuroradiology, Division of Pediatric Radiology, Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD (GO, AT, AP, TAGMH); Pediatric Intensive Care Unit, Department of Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD (CR)
ABSTRACT BACKGROUND
Post-traumatic carotid artery dissection (PTCAD) may result in acute arterial ischemic stroke (AIS). Pediatric PTCAD is rarely diagnosed prior to onset of neurological symptoms. We report on neuroimaging findings in a series of children with PTCAD. METHODS
Five children with head or neck trauma were included in this study. Clinical histories were reviewed for mechanism of trauma, symptoms, complications, therapy, and outcome. Computed tomography (CT), magnetic resonance imaging (MRI), and CT/MR angiography (CTA, MRA) studies were retrospectively evaluated for signs and complications of PTCAD and presence and extent of skull base fractures. RESULTS
PTCAD was located at the level of the skull base in all children and was associated with a skull base fracture in two. The diagnosis was made in five children by combined MRI/MRA and in two by CTA. Air in the carotid canal suggested skull base injury with PTCAD in two children. PTCAD was complicated by AIS in three children. CONCLUSION
PTCAD may result from neck and head trauma. To avoid secondary AIS, radiologists should be familiar with neuroimaging findings in children, especially as acute PTCAD may initially be clinically silent. Consequently, pediatric neuroradiologists should actively exclude PTCAD in children with head and neck trauma.
Introduction Post-traumatic carotid artery dissection (PTCAD) in children like in adults, represent a mechanical breach in the carotid artery wall integrity with formation of a subintimal hematoma.1 The true lumen may be narrowed by the false lumen, resulting in a hemodynamically significant stenosis. In addition, thrombi originating from the false lumen may result in intracranial embolic infarction. In both children and adults, the morbidity from arterial ischemic stroke (AIS) can be significant.2 Early recognition and adequate therapy are important to prevent or limit brain ischemia. Although there are currently no evidence-based guidelines for treatment of pediatric CAD,3 it is critical for the intensive care specialist to know presence of CAD, since it has an impact on the management of the child. Pediatric and adult CAD differs in various terms including their pathomechanism, location and most importantly clinical presentation. In adults, preexisting atherosclerotic changes increase the risk of spontaneous CAD as well as the chances for PTCAD because of the higher vulnerability of the atherosclerotic neck vasculature for minor neck injuries.1, 4 The majority of pediatric PTCADs result from a direct blunt or penetrat-
Keywords: Children, head trauma, neck trauma, carotid artery, dissection, neuroimaging. Acceptance: Received March 14, 2013, and in revised form July 1, 2013. Accepted for publication July 3, 2013. Correspondence: Address correspondence to Thierry A.G.M. Huisman, MD, EQNR, FICIS, Professor of Radiology Pediatrics, and Neurology, Director of Pediatric Radiology and Pediatric Neuroradiology, Russell H. Morgan Department of Radiology and Radiological Science, Charlotte R. Bloomberg Children’s Center, Sheikh Zayed Tower, Room 4174, 1800 Orleans Street, Baltimore, MD 21287-0842. E-mail: [email protected]. J Neuroimaging 2013;00:1-6. DOI: 10.1111/jon.12071
ing injury to the internal carotid artery (ICA) or secondary to an (over-) stretching of the vessel due to acute hyperextension or excessive rotation of the neck. Subtle insults, including external manipulation, physical exertion, or contact sports have also been identified as cause of pediatric PTCAD.5, 6 Children have a higher risk of PTCAD compared to adults because of their lower cranio-cervical stability resulting from the weaker neck musculature, higher dependency on ligamentous rather than bony structures, large head to neck proportion and less well developed protective reflexes.6, 7 In children PTCAD typically occurs in the distal cervical segment of the ICA before entering the carotid canal at the skull base (exocranial orifice of the petrous carotid canal) where the vessel mobility abruptly changes.6 During injuries with rapid deceleration and resultant hyperextension and rotation of the neck, the ICA is stretched over the upper cervical vertebrae producing an intimal tear.6 Finally, in contrast to adult patients in which prodromal signs of upcoming AIS are frequently noted (transient ischemic attacks, amaurosis fugax, or local symptoms) children rarely present with these warning signs.8 AIS may occur “out of the blue” indicating ICA injury.
Copyright
◦ 2013 by the American Society of Neuroimaging C
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M 1 5
F 1.9 4
ICA = internal carotid artery; MCA = middle cerebral artery; ACA = anterior cerebral artery; R = right; L = left; MVA = motor vehicle accident; N/A = not applicable; F = female; M = male; TV = television.
Left hemiparesis 8 Distal cervical RICA Hyposensitivity on the left side
RMCA and RACA stroke
Acutely antiggregation (aspirin), then anticoagulation
Complete recovery 1 No No Proximal petrous LICA
LMCA stroke No Distal cervical LICA Vertical petrous LICA 7.6 3.1 2 3
M M
Head trauma MVA with polytrauma and left skull fracture TV fell on the head > left skull fracture Fall from grandma’s arms, landed on his head
Altered mental state
N/A Complete recovery N/A 8
Right hemiplegia 19
Antiaggregation (aspirin) N/A Antiaggregation (aspirin) LMCA stroke Supraclinoid LICA
Right hemiplegia, aphasia N/A Focal seizure
Outcome Follow-Up (Months) Therapy Complications Location of Dissection Clinical Presentation Mechanism of Injury
Fall out of stroller F 3.6 1
Five patients (3 males and 2 females), 1-7.6 years of age (median age, 4.2 years) were included in the study. The mechanism of trauma, clinical presentation, location of PTCAD, complications, therapy, and outcome of the patients are summarized in Table 1. The mechanism of injury was variable: in one child, head and neck trauma occurred in the context of a polytrauma due to MVA; the remainder of the children had mild to moderate head
Gender
Results
Age (Years)
This study was approved by the Johns Hopkins Medicine Institutional Review Board. Five children with confirmed PTCAD by computed tomography (CT), magnetic resonance imaging (MRI) and/or CT/MR angiography (CTA, MRA) were included in the study. All children had experienced minor or major head or neck trauma. The clinical histories were reviewed for: (1) age and gender of the children, (2) the mechanism of trauma (eg, fall, motor vehicle accident [MVA]), (3) symptoms and neurological findings related to PTCAD (eg, hemiplegia, seizures), (4) complications of PTCAD (eg, stroke), (5) therapy performed for PTCAD (eg, anticoagulation), and (6) outcome of PTCAD. CT, MRI, CTA, and/or MRA were performed by using standard departmental protocols. All available images were retrospectively and qualitatively evaluated by a pediatric neuroradiologist and a pediatric radiologist with experience in pediatric neuroimaging in consensus. First, all the images were systematically re-evaluated for signs of PTCAD. CT images were searched for crescentic hemorrhage in the vessel wall and partial contrast enhancement/flow related enhancement on CTA/MRA or tapering of the ICA. Axial, non-contrast T1weighted images with fat suppression were evaluated for the presence of a hyperintense crescentic rim in the vessel wall. Additionally, MRI and MRA were evaluated for other signs of PTCAD including the presence of an intimal flap, double lumen, aneurysmal dilatation (pseudoaneurysm), segmental narrowing or occlusion of ICA, and flow restriction. Each PTCAD was characterized in terms of affected vessel and location. Second, all images were evaluated for complications of PTCAD, namely acute/subacute intracranial ischemic lesions. Ischemic strokes were characterized for distribution, laterality, and number. Additionally, hemorrhagic conversion and the presence of a thrombus were assessed. All images were evaluated for direct (fracture lines) and indirect (eg, intracranial free air or air within/along the carotid canal) signs of skull base injury. Finally, the presence of cervical spine fractures and the seat belt sign, which are other predictors of PTCAD, was evaluated.
Patient
Methods
Table 1. Mechanism of Trauma, Clinical Presentation, Location of Dissection, Complications, Therapy and Outcome in 5 Children with Post-Traumatic Carotid Artery Dissection
Goal of our study is to report on the neuroimaging findings in five children with PTCAD. Awareness of the pertinent neuroimaging findings should increase the detection rate of these potentially devastating vascular complications in pediatric head and neck trauma. In this article, we use the term CAD as a general term defining carotid artery dissection independently on its etiology, while PTCAD refers only to CAD that occurred after minor or major head trauma.
Table 2. CT and CTA Findings in 5 Children with Post-Traumatic Carotid Artery Dissection Carotid Artery Dissection
Patients
Skull Fractures
Complications
Hemorrhage in the carotid wall
Poor opacification/ tapering of ICA
Isolated fracture lines
Multiple fracture lines
Air within the carotid canal
Thrombus
Stroke
− − − − −
+ + − − −
− N/A − − −
− N/A + + −
− N/A + + −
+ N/A − − +
+ N/A − − +
1 2 3 4 5
N/A = not applicable (no CT was performed for this patient); ICA = internal carotid artery.
Table 3. MRI and MRA Findings in 5 Children with Post-Traumatic Carotid Artery Dissection Complications Carotid Artery Dissection
Patients
1 2 3 4 5
Early
Delayed
Hyperintense Crescentic Rim
Intimal Flap
Double Lumen
PseudoAneursym
Narrowing/ Occlusion of ICA
Thrombus within ICA
Segmental stroke
Multifocal stroke
Hemorrhagic conversion
Recurrent stroke
+ − − + −
− − + − −
− − − − −
− − − − −
+ + + + +
+ + − − +
+ + − − +
− − + − −
+ − − − −
− − − − +
ICA = internal carotid artery.
and neck injuries. Three out of five children developed MCA strokes, and one out the three had additional ACA stroke. Of these three children two had persisting hemi-syndrome. Two children that did not have arterial stroke completely recovered. Patient two was lost to follow up. A latent period between trauma and onset of PTCADsymptoms was seen in two patients: patient 3 had seizure several hours after trauma, patient five became hemiparetic after 1 day. Patients 1 and 5 already had neurological symptoms at the time of initial presentation to our emergency department at 25 and 1 days after trauma, respectively. No information about the period between trauma and onset of symptoms was available for the other patients. Acute CAD treatment included antiaggregation in three patients. In patient 4, neither antiaggregation, nor anticoagulation were started because of simultaneous subarachnoid and intraventricular hemorrhages secondary to the head trauma (Table 1). CT was performed in 4/5 patients, CTA in 2/5 patients, MRI in 5/5 patients, and MRA in 5/5 patients. The neuroimaging findings on CT, CTA, MRI, and MRA are summarized in Tables 2 and 3 and shown in Figures 1 and 2, respectively. Two children had skull-base fractures. Patient 3 had a sagittal-oblique fracture of the left mastoid extending across the external auditory canal, a fracture of the left occipital bone with diastasis of the lamboid suture, and a fracture of the sphenoid bone. Patient 4 had a fracture of the left occipital bone extending into the lambdoid suture, right lateral orbital roof, and left mastoid bone. Additionally, in patient 4 head trauma caused subarachnoid and intraventricular hemorrhages. One day after trauma, she developed a post-hemorrhagic hydrocephalus that required a ventriculo-peritoneal shunt. Diagnosis of PTCAD was possi-
ble by combined MRI/MRA in all patients. CTA allowed to make the diagnosis in 2/5 patients, CT suggested PTCAD in 2/4 patients. Air was seen within the carotid canal in 2/4 patients indicating skull base fracture extending along the carotid canal. None of the patients had cervical spine fractures or the seat belt sign.
Discussion Dissection of arteries of the brain and neck is a leading cause of cerebrovascular injuries in children and accounts for about 20% of pediatric AIS.9 The long-term outcome of CAD in children is variable. Depending on the presence and extent of AIS, the outcome ranges from complete recovery or only mild remaining neurological deficits to severe hemiparesis or hemiplegia, aphasia, and epileptic seizures as shown in our patients.10, 11 In pediatric CAD, the dissecting event is usually followed by a latent period which typically ranges from minutes to days as in our patients, but which on occasion may last weeks or even longer.12, 13 In addition, in pediatric CAD, rarely prodromal symptoms predict upcoming AIS. Ideally, the diagnosis of CAD and the onset of therapy should occur during this latent period to prevent ischemic lesions, and, subsequently, improve the long-term outcome. Multiple genetic and environmental factors have been reported in children with CAD: infections, acute and chronic inflammation, several forms of congenital heart diseases, connective tissue disorders, homocystinuria, and head and neck trauma.14 Severe head and neck trauma such as in MVA, but also any history of injury to the head or neck, intraoral injuries, and non-accidental injury have been associated with
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Fig 1. Selection of the most relevant CT and CTA findings in children with PTCAD. (A) Left coronal CT image of the temporal bone and (B) axial CT image (bone window) of patient 1 show hypodense air inclusions in the left carotid canal (arrows in A and B) secondary to a left sided skull base fracture; (C) Axial CT image of patient 3 shows a dense M2 segment of the right MCA representing a thrombus (arrow in C); (D) Coronal, arterial-phase, 3D reconstruction of a contrast-enhanced CT image of patient 2 reveals tapering of the left distal cervical ICA (arrow) without contrast enhancement of the distal cavernous and supraclinoid ICA; (E) Coronal, arterial-phase, 3D reconstruction of a contrast-enhanced CT image of patient 4 reveals tapering of the left distal cervical ICA (arrow); (F) Axial neck CTA of patient 4 demonstrates a hypodense crescent filling defect (arrow) in the left ICA. CAD.1, 15–19 Spontaneous CAD has been found to occur most likely intracranially, while CAD after trauma are more likely extracranial.12 The distal segment of the ICA before entering the carotid canal at the skull base is the most vulnerable arterial segment in PTCAD.20 During injuries with rapid deceleration and resultant hyperextension and rotation of the neck, the ICA is stretched over the upper cervical vertebrae causing intimal tears.6 In children with major or minor head or neck trauma, neuroradiologists have to carefully evaluate this anatomical region for findings suggestive of PTCAD to be able to diagnose PTCAD prior to onset of focal neurological symptoms. Neuroimaging plays an essential role in establishing the diagnosis of PTCAD and its complications.2, 20 Non-contrast enhanced CT was shown to be insensitive for PTCAD. CT is however able to show skull base fracture, which is commonly associated with PTCAD in children and adults.3 In adults, air extending along the carotid canal was shown to predict injury of the ICA with a sensitivity of 60% and specificity of 67%.21 Although sensitivity and specificity are rather low, in 2 of our patients, air inclusions extending along the carotid canal in combination with skull base fractures alerted the radiologist to examine the ICA region carefully to rule out PTCAD. A missed CAD may have deleterious neurological sequelae as discussed above. Although experience is still limited, CTA was reported to be as sensitive as MRA in detecting CAD.2, 22 CAD findings in CTA include eccentric mural thickening in stenotic regions and a narrowed central or eccentric enhancement from a residual lumen surrounded by hypodensity secondary to a mural
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hematoma.2, 22 A major limitation of using CTA in children is the deleterious effect of ionizing radiation on the developing brain and radiosensitive structures like the eye lens. Children are at a greater risk than adults to suffer from radiation-induced side effects both because they are inherently more radiosensitive and because they have more expected years of life during which a radiation-induced cancer might develop.23 Conventional angiography is helpful in defining vascular changes in CAD and has been considered the diagnostic goldstandard for CAD.20 Specific angiographic findings in CAD include identification of intimal flaps, double lumen, and aneurysmal pouch formation, but also stenosis (irregular, elongated, tapered) and occlusion (often tapering with a flame-shape appearance).2 Compared to adults, conventional angiography has some disadvantages in children: difficulty and morbidity associated with obtaining arterial vascular access, the need for general anesthesia and again the limiting use of ionizing radiation, and the greater costs compared to MRI/MRA. Therefore, conventional angiography is increasingly being replaced by newer, non-invasive techniques.9, 20, 24–27 MRI and MRA have been shown to be as sensitive and specific as conventional angiography.2 Subsequently, combined MRI and MRA are now considered the neuroimaging diagnostic tool of choice in CAD.28 Our results confirm the high sensitivity of combined MRI and MRA in diagnosing PTCAD. As shown in our patients, MRI findings of PTCAD include absence of the normal flow void or altered luminal signal intensity in and narrowing of the arterial lumen with hematoma within the arterial wall.2 Fat saturated, non-contrast T1-weighted MRI
Fig 2. Selection of the most relevant MRI and MRA findings in children with PTCAD. (A) Axial T2-weighted image of patient 2 shows a hyperintense signal abnormality within the left cervical ICA indicating a thrombus (arrow); (B) Axial T1-weighted MR image of patient 3 shows a hyperintense thrombus within the right ICA (arrow); (C) Contrast enhanced 3D TOF MRA of patient 4 demonstrates a near complete occlusion of left ICA (arrow) and partial occlusion of left MCA; (D) ADC map of patient 3 demonstrates an area of restricted diffusion (ADC-hypointense) within the right MCA territory compatible with AIS; (E) Axial cerebral blood flow (CBF) arterial spin labeling (ASL) image of patient 3 shows a matching area of hypoperfusion; (F) Axial minIP-susceptibility weighted imaging (SWI) of patient 3 shows a hypointense signal in the expected course of the M1 segment of the right MCA indicating a thrombus and prominently hypointense sulcal veins in the ischemic area.
of both head and neck best visualized the diagnostic intramural hematoma. MRA may show a tapered narrowing or occlusion of the dissected vessel.2 Another advantage of MRI compared to conventional angiography is the possibility to time the thrombosis related to CAD.25 This additional information may be helpful in the decision to start anticoagulation treatment or not. Moreover, MRI allows to simultaneously rule out or detect complicating AIS. MRI and MRA, however, have some limitations compared to conventional angiography: the degree of stenosis and the extent of longitudinal extension may be overestimated, hemodynamic parameters cannot be obtained, and, particularly for intracranial dissection and posterior circulation stroke, MRI/MRA may be limited.2 Therefore, MRI/MRA and conventional angiography are complementary and should be selected depending on the individual findings. Differences in neuroimaging findings between pediatric and adult CAD are shown in the literature and by our study.2, 9, 12, 20 In children, CAD typically occurs in the distal cervical segment of the ICA before entering the carotid canal at the skull base. This is due to the immature cranio-cervical stability resulting from the weak neck musculature, high dependency on more lax pediatric ligaments rather than bony structures, large head to neck proportion and underdeveloped protective reflexes.6, 7 In adults, however, CAD occurs more frequently at the level of the carotid bifurcation, where atheromatous plaques are typically located and may increase the risk for posttraumatic dissections.
In children, however, carotid arteries are usually healthy without degenerative pathology. We are aware of some limitations in our study: The small sample size and the lack of some clinical data as well as unavailability of comparison between the different imaging techniques in all patients due to the retrospective character of this study.
Conclusion PTCAD is one of the most common causes of pediatric AIS and may be associated with high morbidity and long-term neurological sequelae. Usually, PTCAD is diagnosed after onset of focal neurological symptoms due to AIS. Neuroradiologists should be aware of the increased risk for PTCAD in children with head and neck trauma due to the unique biomechanical properties of the pediatric cranio-cervical junction and mobility of the neck. Consequently, if there is a blunt or penetrating injury of the pediatric head and neck region with history of acute acceleration/deceleration or rotational forces, a PTCAD should actively be ruled out. In addition, if air inclusions extending along the course of the carotid canal are noted secondary to a skull base fracture, PTCAD may be present. An early diagnosis of PTCAD with immediate start of an appropriate therapy prior to the onset of neurological symptoms is important in terms of long-term outcome.
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References 1. Camacho A, Villarejo A, De Aragon ´ AM, et al. Spontaneous carotid and vertebral artery dissection in children. Pediatr Neurol 2001;25:250-253. 2. Chamoun RB, Mawad ME, Whitehead WE, et al. Extracranial traumatic carotid artery dissections in children: a review of current diagnosis and treatment options. J Neurosurg Pediatr 2008;2:101108. 3. Kopelman TR, Berardoni NE, O’Neill PJ, et al. Risk factors for blunt cerebrovascular injury in children: do they mimic those seen in adults? J Trauma 2011;71:559-564. 4. Lew SM, Frumiento C, Wald SL. Pediatric blunt carotid injury: a review of the National Pediatric Trauma Registry. Pediatr Neurosurg 1999;30:239-244. 5. De Borst GJ, Slieker MG, Monteiro LM, et al. Bilateral traumatic carotid artery dissection in a child. Pediatr Neurol 2006;34:408411. 6. Pinto PS, Meoded A, Poretti A, et al. The unique features of traumatic brain injury in children. Review of the characteristics of the pediatric skull and brain, mechanisms of trauma, patterns of injury, complications, and their imaging findings-part 2. J Neuroimaging 2012;22:e18-41. 7. Pinto PS, Poretti A, Meoded A, et al. The unique features of traumatic brain injury in children. Review of the characteristics of the pediatric skull and brain, mechanisms of trauma, patterns of injury, complications and their imaging findings-part 1. J Neuroimaging 2012;22:e1-17. 8. Giroud M, Lemesle M, Madinier G, et al. Stroke in children under 16 years of age. Clinical and etiological difference with adults. Acta Neurol Scand 1997;96:401-406. 9. Chabrier S, Lasjaunias P, Husson B, et al. Ischaemic stroke from dissection of the craniocervical arteries in childhood: report of 12 patients. Eur J Paediatr Neurol 2003;7:39-42. 10. Tabarki B, EI Madani A, Alvarez H, et al. Accident vasculaire cerebral ischemique par dissection arterielle vertebrale. Arch Pediatr 1997;4:763-766. 11. Patel H, Smith RR, Garg BP. Spontaneous extracranial carotid artery dissection in children. Pediatr Neurol 1995;13:55-60. 12. Fullerton HJ, Johnston SC, Smith WS. Arterial dissection and stroke in children. Neurology 2001;57:1155-1160. 13. Silverboard G, Tart R. Cerebrovascular arterial dissection in children and young adults. Semin Pediatr Neurol 2000;7:289300.
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14. Ganesan V, Cox TC, Gunny R. Abnormalities of cervical arteries in children with arterial ischemic stroke. Neurology 2011;76:166-171. 15. Moriarty JM, Lukas C, Rossler L, et al. Carotid artery dissection following a minor household accident in a 10-month-old child. Ir J Med Sci 2009;178:535-539. 16. Pierrot S, Bernardeschi D, Morrisseau-Durand MP, et al. Dissection of the internal carotid artery following trauma of the soft palate in children. Ann Otol Rhinol Laryngol 2006;115:323-329. 17. Agner C. Arterial dissection and stroke following child abuse: case report and review of the literature. Childs Nerv Syst 2005;21:416420. 18. Levack MM, Pettitt BJ, Winston AD. Carotid artery thrombosis and delayed stroke associated with the use of a shoulder belt in a teenager. J Pediatr Surg 2009;44:E29-33. 19. Lequin MH, Peeters EAJ, Holscher HC. Arterial infarction caused by carotid artery dissection in the neonate. Eur J Paediatr Neurol 2004;8:155-160. 20. Rafay MF, Armstrong D, Domi T, et al. Craniocervical arterial dissection in children: clinical and radiographic presentation. J Child Neurol 2006;21:8-16. 21. York G, Barboriak D, Petrella J, et al. Association of internal carotid artery injury with carotid canal fractures in patients with head trauma. AJR Am J Roentgenol 2005;184:1672-1678. 22. Robertson William C Jr, Given CA. Spontaneous intracranial arterial dissection in the young: diagnosis by CT angiography. BMC Neurol 2006;6:16-21. 23. Brenner DJ, Hall EJ. Computed tomography—an increasing source of radiation exposure. N Engl J Med 2007;357:2277-2284. 24. Mortazavi MM, Verma K, Tubbs RS, et al. Pediatric traumatic carotid, vertebral and cerebral artery dissections: a review. Childs Nerv Syst 2011;27:2045-2056. 25. Oelerich M, Stogbauer F, Kurlemann G, et al. Craniocervical artery ¨ dissection: MR imaging and MR angiographic findings. Eur Radiol 1999;9:1385-1391. 26. Levy C, Laissy JP, Raveau V, et al. Carotid and vertebral ´ artery dissections: three-dimensional time-of-flight MR angiography and MR imaging versus conventional angiography. Radiology 1994;190:97-103. 27. Rommel O, Niedeggen A, Tegenthoff M, et al. Carotid and vertebral artery injury following severe head or cervical spine trauma. Cerebrovasc Dis 1999;9:202-209. 28. Jones TS, Burlew CC, Kornblith LZ, et al. Blunt cerebrovascular injuries in the child. Am J Surg 2012;204:7-10.
ABSTRACT BACKGROUND
Post-traumatic carotid artery dissection (PTCAD) may result in acute arterial ischemic stroke (AIS). Pediatric PTCAD is rarely diagnosed prior to onset of neurological symptoms. We report on neuroimaging findings in a series of children with PTCAD. METHODS
Five children with head or neck trauma were included in this study. Clinical histories were reviewed for mechanism of trauma, symptoms, complications, therapy, and outcome. Computed tomography (CT), magnetic resonance imaging (MRI), and CT/MR angiography (CTA, MRA) studies were retrospectively evaluated for signs and complications of PTCAD and presence and extent of skull base fractures. RESULTS
PTCAD was located at the level of the skull base in all children and was associated with a skull base fracture in two. The diagnosis was made in five children by combined MRI/MRA and in two by CTA. Air in the carotid canal suggested skull base injury with PTCAD in two children. PTCAD was complicated by AIS in three children. CONCLUSION
PTCAD may result from neck and head trauma. To avoid secondary AIS, radiologists should be familiar with neuroimaging findings in children, especially as acute PTCAD may initially be clinically silent. Consequently, pediatric neuroradiologists should actively exclude PTCAD in children with head and neck trauma.
Introduction Post-traumatic carotid artery dissection (PTCAD) in children like in adults, represent a mechanical breach in the carotid artery wall integrity with formation of a subintimal hematoma.1 The true lumen may be narrowed by the false lumen, resulting in a hemodynamically significant stenosis. In addition, thrombi originating from the false lumen may result in intracranial embolic infarction. In both children and adults, the morbidity from arterial ischemic stroke (AIS) can be significant.2 Early recognition and adequate therapy are important to prevent or limit brain ischemia. Although there are currently no evidence-based guidelines for treatment of pediatric CAD,3 it is critical for the intensive care specialist to know presence of CAD, since it has an impact on the management of the child. Pediatric and adult CAD differs in various terms including their pathomechanism, location and most importantly clinical presentation. In adults, preexisting atherosclerotic changes increase the risk of spontaneous CAD as well as the chances for PTCAD because of the higher vulnerability of the atherosclerotic neck vasculature for minor neck injuries.1, 4 The majority of pediatric PTCADs result from a direct blunt or penetrat-
Keywords: Children, head trauma, neck trauma, carotid artery, dissection, neuroimaging. Acceptance: Received March 14, 2013, and in revised form July 1, 2013. Accepted for publication July 3, 2013. Correspondence: Address correspondence to Thierry A.G.M. Huisman, MD, EQNR, FICIS, Professor of Radiology Pediatrics, and Neurology, Director of Pediatric Radiology and Pediatric Neuroradiology, Russell H. Morgan Department of Radiology and Radiological Science, Charlotte R. Bloomberg Children’s Center, Sheikh Zayed Tower, Room 4174, 1800 Orleans Street, Baltimore, MD 21287-0842. E-mail: [email protected]. J Neuroimaging 2013;00:1-6. DOI: 10.1111/jon.12071
ing injury to the internal carotid artery (ICA) or secondary to an (over-) stretching of the vessel due to acute hyperextension or excessive rotation of the neck. Subtle insults, including external manipulation, physical exertion, or contact sports have also been identified as cause of pediatric PTCAD.5, 6 Children have a higher risk of PTCAD compared to adults because of their lower cranio-cervical stability resulting from the weaker neck musculature, higher dependency on ligamentous rather than bony structures, large head to neck proportion and less well developed protective reflexes.6, 7 In children PTCAD typically occurs in the distal cervical segment of the ICA before entering the carotid canal at the skull base (exocranial orifice of the petrous carotid canal) where the vessel mobility abruptly changes.6 During injuries with rapid deceleration and resultant hyperextension and rotation of the neck, the ICA is stretched over the upper cervical vertebrae producing an intimal tear.6 Finally, in contrast to adult patients in which prodromal signs of upcoming AIS are frequently noted (transient ischemic attacks, amaurosis fugax, or local symptoms) children rarely present with these warning signs.8 AIS may occur “out of the blue” indicating ICA injury.
Copyright
◦ 2013 by the American Society of Neuroimaging C
1
2
Journal of Neuroimaging Vol 00 No 0 xxxx 2013
M 1 5
F 1.9 4
ICA = internal carotid artery; MCA = middle cerebral artery; ACA = anterior cerebral artery; R = right; L = left; MVA = motor vehicle accident; N/A = not applicable; F = female; M = male; TV = television.
Left hemiparesis 8 Distal cervical RICA Hyposensitivity on the left side
RMCA and RACA stroke
Acutely antiggregation (aspirin), then anticoagulation
Complete recovery 1 No No Proximal petrous LICA
LMCA stroke No Distal cervical LICA Vertical petrous LICA 7.6 3.1 2 3
M M
Head trauma MVA with polytrauma and left skull fracture TV fell on the head > left skull fracture Fall from grandma’s arms, landed on his head
Altered mental state
N/A Complete recovery N/A 8
Right hemiplegia 19
Antiaggregation (aspirin) N/A Antiaggregation (aspirin) LMCA stroke Supraclinoid LICA
Right hemiplegia, aphasia N/A Focal seizure
Outcome Follow-Up (Months) Therapy Complications Location of Dissection Clinical Presentation Mechanism of Injury
Fall out of stroller F 3.6 1
Five patients (3 males and 2 females), 1-7.6 years of age (median age, 4.2 years) were included in the study. The mechanism of trauma, clinical presentation, location of PTCAD, complications, therapy, and outcome of the patients are summarized in Table 1. The mechanism of injury was variable: in one child, head and neck trauma occurred in the context of a polytrauma due to MVA; the remainder of the children had mild to moderate head
Gender
Results
Age (Years)
This study was approved by the Johns Hopkins Medicine Institutional Review Board. Five children with confirmed PTCAD by computed tomography (CT), magnetic resonance imaging (MRI) and/or CT/MR angiography (CTA, MRA) were included in the study. All children had experienced minor or major head or neck trauma. The clinical histories were reviewed for: (1) age and gender of the children, (2) the mechanism of trauma (eg, fall, motor vehicle accident [MVA]), (3) symptoms and neurological findings related to PTCAD (eg, hemiplegia, seizures), (4) complications of PTCAD (eg, stroke), (5) therapy performed for PTCAD (eg, anticoagulation), and (6) outcome of PTCAD. CT, MRI, CTA, and/or MRA were performed by using standard departmental protocols. All available images were retrospectively and qualitatively evaluated by a pediatric neuroradiologist and a pediatric radiologist with experience in pediatric neuroimaging in consensus. First, all the images were systematically re-evaluated for signs of PTCAD. CT images were searched for crescentic hemorrhage in the vessel wall and partial contrast enhancement/flow related enhancement on CTA/MRA or tapering of the ICA. Axial, non-contrast T1weighted images with fat suppression were evaluated for the presence of a hyperintense crescentic rim in the vessel wall. Additionally, MRI and MRA were evaluated for other signs of PTCAD including the presence of an intimal flap, double lumen, aneurysmal dilatation (pseudoaneurysm), segmental narrowing or occlusion of ICA, and flow restriction. Each PTCAD was characterized in terms of affected vessel and location. Second, all images were evaluated for complications of PTCAD, namely acute/subacute intracranial ischemic lesions. Ischemic strokes were characterized for distribution, laterality, and number. Additionally, hemorrhagic conversion and the presence of a thrombus were assessed. All images were evaluated for direct (fracture lines) and indirect (eg, intracranial free air or air within/along the carotid canal) signs of skull base injury. Finally, the presence of cervical spine fractures and the seat belt sign, which are other predictors of PTCAD, was evaluated.
Patient
Methods
Table 1. Mechanism of Trauma, Clinical Presentation, Location of Dissection, Complications, Therapy and Outcome in 5 Children with Post-Traumatic Carotid Artery Dissection
Goal of our study is to report on the neuroimaging findings in five children with PTCAD. Awareness of the pertinent neuroimaging findings should increase the detection rate of these potentially devastating vascular complications in pediatric head and neck trauma. In this article, we use the term CAD as a general term defining carotid artery dissection independently on its etiology, while PTCAD refers only to CAD that occurred after minor or major head trauma.
Table 2. CT and CTA Findings in 5 Children with Post-Traumatic Carotid Artery Dissection Carotid Artery Dissection
Patients
Skull Fractures
Complications
Hemorrhage in the carotid wall
Poor opacification/ tapering of ICA
Isolated fracture lines
Multiple fracture lines
Air within the carotid canal
Thrombus
Stroke
− − − − −
+ + − − −
− N/A − − −
− N/A + + −
− N/A + + −
+ N/A − − +
+ N/A − − +
1 2 3 4 5
N/A = not applicable (no CT was performed for this patient); ICA = internal carotid artery.
Table 3. MRI and MRA Findings in 5 Children with Post-Traumatic Carotid Artery Dissection Complications Carotid Artery Dissection
Patients
1 2 3 4 5
Early
Delayed
Hyperintense Crescentic Rim
Intimal Flap
Double Lumen
PseudoAneursym
Narrowing/ Occlusion of ICA
Thrombus within ICA
Segmental stroke
Multifocal stroke
Hemorrhagic conversion
Recurrent stroke
+ − − + −
− − + − −
− − − − −
− − − − −
+ + + + +
+ + − − +
+ + − − +
− − + − −
+ − − − −
− − − − +
ICA = internal carotid artery.
and neck injuries. Three out of five children developed MCA strokes, and one out the three had additional ACA stroke. Of these three children two had persisting hemi-syndrome. Two children that did not have arterial stroke completely recovered. Patient two was lost to follow up. A latent period between trauma and onset of PTCADsymptoms was seen in two patients: patient 3 had seizure several hours after trauma, patient five became hemiparetic after 1 day. Patients 1 and 5 already had neurological symptoms at the time of initial presentation to our emergency department at 25 and 1 days after trauma, respectively. No information about the period between trauma and onset of symptoms was available for the other patients. Acute CAD treatment included antiaggregation in three patients. In patient 4, neither antiaggregation, nor anticoagulation were started because of simultaneous subarachnoid and intraventricular hemorrhages secondary to the head trauma (Table 1). CT was performed in 4/5 patients, CTA in 2/5 patients, MRI in 5/5 patients, and MRA in 5/5 patients. The neuroimaging findings on CT, CTA, MRI, and MRA are summarized in Tables 2 and 3 and shown in Figures 1 and 2, respectively. Two children had skull-base fractures. Patient 3 had a sagittal-oblique fracture of the left mastoid extending across the external auditory canal, a fracture of the left occipital bone with diastasis of the lamboid suture, and a fracture of the sphenoid bone. Patient 4 had a fracture of the left occipital bone extending into the lambdoid suture, right lateral orbital roof, and left mastoid bone. Additionally, in patient 4 head trauma caused subarachnoid and intraventricular hemorrhages. One day after trauma, she developed a post-hemorrhagic hydrocephalus that required a ventriculo-peritoneal shunt. Diagnosis of PTCAD was possi-
ble by combined MRI/MRA in all patients. CTA allowed to make the diagnosis in 2/5 patients, CT suggested PTCAD in 2/4 patients. Air was seen within the carotid canal in 2/4 patients indicating skull base fracture extending along the carotid canal. None of the patients had cervical spine fractures or the seat belt sign.
Discussion Dissection of arteries of the brain and neck is a leading cause of cerebrovascular injuries in children and accounts for about 20% of pediatric AIS.9 The long-term outcome of CAD in children is variable. Depending on the presence and extent of AIS, the outcome ranges from complete recovery or only mild remaining neurological deficits to severe hemiparesis or hemiplegia, aphasia, and epileptic seizures as shown in our patients.10, 11 In pediatric CAD, the dissecting event is usually followed by a latent period which typically ranges from minutes to days as in our patients, but which on occasion may last weeks or even longer.12, 13 In addition, in pediatric CAD, rarely prodromal symptoms predict upcoming AIS. Ideally, the diagnosis of CAD and the onset of therapy should occur during this latent period to prevent ischemic lesions, and, subsequently, improve the long-term outcome. Multiple genetic and environmental factors have been reported in children with CAD: infections, acute and chronic inflammation, several forms of congenital heart diseases, connective tissue disorders, homocystinuria, and head and neck trauma.14 Severe head and neck trauma such as in MVA, but also any history of injury to the head or neck, intraoral injuries, and non-accidental injury have been associated with
Orman et al: Posttraumatic Carotid Artery Dissection in Children
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Fig 1. Selection of the most relevant CT and CTA findings in children with PTCAD. (A) Left coronal CT image of the temporal bone and (B) axial CT image (bone window) of patient 1 show hypodense air inclusions in the left carotid canal (arrows in A and B) secondary to a left sided skull base fracture; (C) Axial CT image of patient 3 shows a dense M2 segment of the right MCA representing a thrombus (arrow in C); (D) Coronal, arterial-phase, 3D reconstruction of a contrast-enhanced CT image of patient 2 reveals tapering of the left distal cervical ICA (arrow) without contrast enhancement of the distal cavernous and supraclinoid ICA; (E) Coronal, arterial-phase, 3D reconstruction of a contrast-enhanced CT image of patient 4 reveals tapering of the left distal cervical ICA (arrow); (F) Axial neck CTA of patient 4 demonstrates a hypodense crescent filling defect (arrow) in the left ICA. CAD.1, 15–19 Spontaneous CAD has been found to occur most likely intracranially, while CAD after trauma are more likely extracranial.12 The distal segment of the ICA before entering the carotid canal at the skull base is the most vulnerable arterial segment in PTCAD.20 During injuries with rapid deceleration and resultant hyperextension and rotation of the neck, the ICA is stretched over the upper cervical vertebrae causing intimal tears.6 In children with major or minor head or neck trauma, neuroradiologists have to carefully evaluate this anatomical region for findings suggestive of PTCAD to be able to diagnose PTCAD prior to onset of focal neurological symptoms. Neuroimaging plays an essential role in establishing the diagnosis of PTCAD and its complications.2, 20 Non-contrast enhanced CT was shown to be insensitive for PTCAD. CT is however able to show skull base fracture, which is commonly associated with PTCAD in children and adults.3 In adults, air extending along the carotid canal was shown to predict injury of the ICA with a sensitivity of 60% and specificity of 67%.21 Although sensitivity and specificity are rather low, in 2 of our patients, air inclusions extending along the carotid canal in combination with skull base fractures alerted the radiologist to examine the ICA region carefully to rule out PTCAD. A missed CAD may have deleterious neurological sequelae as discussed above. Although experience is still limited, CTA was reported to be as sensitive as MRA in detecting CAD.2, 22 CAD findings in CTA include eccentric mural thickening in stenotic regions and a narrowed central or eccentric enhancement from a residual lumen surrounded by hypodensity secondary to a mural
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hematoma.2, 22 A major limitation of using CTA in children is the deleterious effect of ionizing radiation on the developing brain and radiosensitive structures like the eye lens. Children are at a greater risk than adults to suffer from radiation-induced side effects both because they are inherently more radiosensitive and because they have more expected years of life during which a radiation-induced cancer might develop.23 Conventional angiography is helpful in defining vascular changes in CAD and has been considered the diagnostic goldstandard for CAD.20 Specific angiographic findings in CAD include identification of intimal flaps, double lumen, and aneurysmal pouch formation, but also stenosis (irregular, elongated, tapered) and occlusion (often tapering with a flame-shape appearance).2 Compared to adults, conventional angiography has some disadvantages in children: difficulty and morbidity associated with obtaining arterial vascular access, the need for general anesthesia and again the limiting use of ionizing radiation, and the greater costs compared to MRI/MRA. Therefore, conventional angiography is increasingly being replaced by newer, non-invasive techniques.9, 20, 24–27 MRI and MRA have been shown to be as sensitive and specific as conventional angiography.2 Subsequently, combined MRI and MRA are now considered the neuroimaging diagnostic tool of choice in CAD.28 Our results confirm the high sensitivity of combined MRI and MRA in diagnosing PTCAD. As shown in our patients, MRI findings of PTCAD include absence of the normal flow void or altered luminal signal intensity in and narrowing of the arterial lumen with hematoma within the arterial wall.2 Fat saturated, non-contrast T1-weighted MRI
Fig 2. Selection of the most relevant MRI and MRA findings in children with PTCAD. (A) Axial T2-weighted image of patient 2 shows a hyperintense signal abnormality within the left cervical ICA indicating a thrombus (arrow); (B) Axial T1-weighted MR image of patient 3 shows a hyperintense thrombus within the right ICA (arrow); (C) Contrast enhanced 3D TOF MRA of patient 4 demonstrates a near complete occlusion of left ICA (arrow) and partial occlusion of left MCA; (D) ADC map of patient 3 demonstrates an area of restricted diffusion (ADC-hypointense) within the right MCA territory compatible with AIS; (E) Axial cerebral blood flow (CBF) arterial spin labeling (ASL) image of patient 3 shows a matching area of hypoperfusion; (F) Axial minIP-susceptibility weighted imaging (SWI) of patient 3 shows a hypointense signal in the expected course of the M1 segment of the right MCA indicating a thrombus and prominently hypointense sulcal veins in the ischemic area.
of both head and neck best visualized the diagnostic intramural hematoma. MRA may show a tapered narrowing or occlusion of the dissected vessel.2 Another advantage of MRI compared to conventional angiography is the possibility to time the thrombosis related to CAD.25 This additional information may be helpful in the decision to start anticoagulation treatment or not. Moreover, MRI allows to simultaneously rule out or detect complicating AIS. MRI and MRA, however, have some limitations compared to conventional angiography: the degree of stenosis and the extent of longitudinal extension may be overestimated, hemodynamic parameters cannot be obtained, and, particularly for intracranial dissection and posterior circulation stroke, MRI/MRA may be limited.2 Therefore, MRI/MRA and conventional angiography are complementary and should be selected depending on the individual findings. Differences in neuroimaging findings between pediatric and adult CAD are shown in the literature and by our study.2, 9, 12, 20 In children, CAD typically occurs in the distal cervical segment of the ICA before entering the carotid canal at the skull base. This is due to the immature cranio-cervical stability resulting from the weak neck musculature, high dependency on more lax pediatric ligaments rather than bony structures, large head to neck proportion and underdeveloped protective reflexes.6, 7 In adults, however, CAD occurs more frequently at the level of the carotid bifurcation, where atheromatous plaques are typically located and may increase the risk for posttraumatic dissections.
In children, however, carotid arteries are usually healthy without degenerative pathology. We are aware of some limitations in our study: The small sample size and the lack of some clinical data as well as unavailability of comparison between the different imaging techniques in all patients due to the retrospective character of this study.
Conclusion PTCAD is one of the most common causes of pediatric AIS and may be associated with high morbidity and long-term neurological sequelae. Usually, PTCAD is diagnosed after onset of focal neurological symptoms due to AIS. Neuroradiologists should be aware of the increased risk for PTCAD in children with head and neck trauma due to the unique biomechanical properties of the pediatric cranio-cervical junction and mobility of the neck. Consequently, if there is a blunt or penetrating injury of the pediatric head and neck region with history of acute acceleration/deceleration or rotational forces, a PTCAD should actively be ruled out. In addition, if air inclusions extending along the course of the carotid canal are noted secondary to a skull base fracture, PTCAD may be present. An early diagnosis of PTCAD with immediate start of an appropriate therapy prior to the onset of neurological symptoms is important in terms of long-term outcome.
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