|Year : 2015 | Volume
| Issue : 3 | Page : 370-376
Post-traumatic vertical gaze paresis in nine patients: Special vulnerability of the artery of percheron in trauma?
Neuro-ophthalmology Division, King Khaled Eye Specialist Hospital, Riyadh, Kingdom of Saudi Arabia
|Date of Web Publication||1-Jul-2015|
P.O. Box - 7191, Riyadh, 11462
Kingdom of Saudi Arabia
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Purpose: The purpose was to present a case series of vertical gaze paresis in patients with a history of cranioencephalic trauma (CET).
Methods: The clinical characteristics and management are presented of nine patients with a history of CET secondary to motor vehicle accidents with associated vertical gaze paresis.
Results: Neuroimaging studies indicated posttraumatic contusion of the thalamic-mesencephalic region in all nine patients who corresponded to the artery of Percheron region; four patients had signs of hemorrhagic transformation. Vertical gaze paresis was present in all patients, ranging from complete paralysis of the upward and downward gaze to a slight limitation of upward gaze.
Discussion: Posttraumatic vertical gaze paresis is a rare phenomenon that can occur in isolation or in association with other neurological deficits and can cause a significant limitation in the quality-of-life. Studies in the literature have postulated that the unique anatomy of the angle of penetration of the thalamoperforating and lenticulostriate arteries makes these vessels more vulnerable to isolated selective damage in certain individuals and can cause-specific patterns of CET.
Keywords: Artery of Percheron, Posttraumatic Cerebral Infarction, Vertical Gaze Paresis
|How to cite this article:|
Galvez-Ruiz A. Post-traumatic vertical gaze paresis in nine patients: Special vulnerability of the artery of percheron in trauma?. Middle East Afr J Ophthalmol 2015;22:370-6
|How to cite this URL:|
Galvez-Ruiz A. Post-traumatic vertical gaze paresis in nine patients: Special vulnerability of the artery of percheron in trauma?. Middle East Afr J Ophthalmol [serial online] 2015 [cited 2019 Jun 18];22:370-6. Available from: http://www.meajo.org/text.asp?2015/22/3/370/159765
| Introduction|| |
The characteristic signs of stroke of the artery of Percheron (AOP) are confusion/coma, vertical gaze paresis, and memory impairment. The prognosis is relatively good in ischemic thalamic lesions compared to hemorrhagic lesions.  Additional symptoms can occur in cases with simultaneous rostral mesencephalic trauma (mesencephalic-thalamic or thalamopeduncular syndrome) including cranial nerve (CN) III paresis, hemiparesis, cerebellar ataxia, and movement disorders. 
In other cases, the presence of a large embolus at the top of the basilar artery can also produce bilateral paramedian thalamic infarcts with rostral mesencephalic involvement. However, in these cases, posterior circulation infarcts (e.g., occipital and cerebellar infarctions) are also very common. When all of these signs are present together, they constitute what is called "top of the basilar syndrome." 
In the literature, posttraumatic cerebral infarction is a complication that occurs in 1.9% to 10.4% of all cranioencephalic traumas (CETs). , The most common location is the territory of the posterior cerebral artery (PCA).  A number of mechanisms that cause cerebral infarction have been proposed including vascular compression due to cerebral edema, cerebral vasospasm, vascular damage, embolism, and systemic hypotension. 
The most common mechanism of infarction is vascular compression, which occurs as a result of the mass effect of cerebral contusion or falcine or transtentorial herniation.  This mass effect, compresses the large vessels, stretches or attenuates the small perforating vessels (e.g., lenticulostriate or thalamoperforating), causing ischemia in the different regions they supply.  In cases of direct vascular damage with no mass effect, the most common mechanism of intracranial vascular damage is dissection of the internal carotid artery (usually at the supraclinoid level). In addition, in cases with cervical trauma, vertebral carotid dissection may occur at this level. 
Another mechanism of infarction is vasospasm associated with subarachnoid hemorrhage.  Vasospasm can also be associated with direct damage to the arterial wall, hypothalamic dysfunction, and impaired auto-regulation. 
In this study, we reviewed nine patients with a history of CET secondary to motor vehicle accidents and associated with vertical gaze paresis with bilateral posttraumatic contusion of the thalamic-mesencephalic region corresponding to AOP region. This study evaluates the etiopathogenic mechanisms of damage in this specific region (thalamic-mesencephalic) in these patients. We hypothesize that the pathogenesis of this damage occurs by the specific involvement of the AOP.
| Methods|| |
We present nine patients with a history of CET secondary to automobile accidents and associated vertical gaze paresis. Inclusion criteria were patients with any type of vertical paresis and anatomical lesions imaged by magnetic resonance imaging (MRI) the AOP region. Patients were excluded it they had complex disorders of ocular motility (e.g., patients with paresis of multiple CNs), there were no neuroimaging studies and a proper ocular motility examination could not be performed due to cooperation, lack of understanding, etc. Data were collected on age, gender, time since the accident, pupillary reaction, extraocular motility, fundus examination, presence of associated neurological signs, neuroimaging findings, and possible anatomical structures involved in the vertical gaze paresis.
| Results|| |
[Table 1] presents the patient demographics and clinical signs. Neuroimaging studies showed posttraumatic contusion of the thalamic-mesencephalic region corresponding to the AOP region in all patients; four patients had signs of hemorrhagic transformation. [Figure 1] presents axial computed tomography (CT) slices at the rostral mesencephalic and thalamic levels of the cranial scan for patient 1 and brain MRI scans (T2-Weighted and fluid-attenuated inversion recovery (FLAIR) sequences) for patients 2-9.
|Figure 1: Axial slices at the rostral mesencephalic and thalamic levels of cranial computed tomography scans of patient 1 and brain magnetic resonance imaging scans (T2-weighted and fluid-attenuated inversion recovery sequences) of patients 2-9 with evidence of traumatic thalamic-mesencephalic injury|
Click here to view
|Table 1: Demographics and clinical characteristics of nine patients with posttraumatic vertical gaze paresis|
Click here to view
[Figure 2] presents the different degrees of vertical gaze paresis patients 1-9 (no pictures were available for patient 7). All of the patients (100%) had some degree of vertical gaze paresis, ranging from complete paralysis of the upward and downward gaze (one patient) to a slight limitation of the upward gaze (one patient), as well as varying degrees of partial vertical gaze paresis (four patients).
|Figure 2: Composite photographs showing the examination of the different degrees of vertical gaze paresis in patients 1-9 (there are no pictures of patient 7). For each patient, the photograph on the left corresponds to the upward gaze, and the photograph on the right corresponds to the downward gaze|
Click here to view
Other associated neurological signs were CN III partial paresis, posttraumatic CN VI paresis, posttraumatic optic neuropathy, residual hemiparesis, and ataxia.
| Discussion|| |
This study reviewed nine patients with a history of CET secondary to automobile accidents and associated vertical gaze paresis with posttraumatic contusion of the thalamic-mesencephalic region corresponding to the AOP.
The paramedian thalamic region is supplied by paramedian or thalamoperforating arteries arising from the P1 segment of the PCA. These arteries show significant anatomical variability in the number, size, and regions supplied. 
In addition, the arteries that supply the rostral mesencephalic region (superior mesencephalic or rubral arteries) can arise independently from the P1 segment of the PCA or share a common starting point with paramedian arteries such that both territories share the same blood supply. Complicating this picture, the AOP is an uncommon anatomical variant consisting of a single dominant thalamoperforating artery supplying the paramedian thalamic region bilaterally. Not surprisingly, its occlusion causes bilateral paramedian thalamic infarction, with or without mesencephalic involvement.  Although the prevalence of AOP infarction is unknown, in studies evaluating large series of cerebral infarctions, the characteristic pattern of AOP infarction is observed in 0.1% to 0.7% of all registered brain infarcts. ,,,
When an occlusion of the AOP occurs, there are 4 possibilities, according to Lazzaro et al.  Joint involvement of the bilateral paramedian thalamic and mesencephalic regions (43% of the patients in their series cases).
Ischemic injury of the bilateral paramedian thalamic region in isolation (38% of the patients in their series cases); Ischemic injury of the anterior thalamus, bilateral paramedian thalamus, and rostral mesencephalon (14% of the patients); Ischemic injury of the anterior thalamus and bilateral paramedian thalamic region with an intact mesencephalic region (5% of the patients).
In our patients, there was a mesencephalic-thalamic involvement (mesencephalic-thalamic syndrome), likely due to the existence of a common blood supply to the rostral mesencephalic and paramedian thalamic regions (as already discussed). In these patients, the vertical gaze disturbance was due to disruption of the mesencephalic structures controlling vertical gaze.
The mesencephalic structures involved in vertical gaze control are the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF), the interstitial nucleus of Cajal (INC), the posterior commissure (PC), the oculomotor complex, and the nucleus of CN IV. 
The riMLF controls the speed of vertical saccades and the quick phase of the torsional component of nystagmus. The INC stabilizes the eyeball in an eccentric position after a vertical saccade. Injury to this nucleus causes a limitation in the amplitude of upward and downward vertical movements without interfering with a saccade speed. 
The PC consists of a number of neuronal cell bodies that form the core of the PC. PC lesions often cause impairment of the upward and downward vertical gaze, affecting all vertical eye movements. Such lesions are associated with Parinaud's syndrome, which consists of convergence-retraction nystagmus when attempting upward gaze, light-near dissociation, and palpebral retraction or Collier's sign. 
However, some publications have described patients with isolated paramedian thalamic infarctions (without mesencephalic involvement) with vertical gaze paresis. In these cases, the most widely accepted explanation is that the vertical paresis is due to interruption of the supranuclear inputs when passing through the thalamic region to the pretectal and prerubral areas. 
Clearly, it is difficult to establish precise anatomical correlations in our patients due to the time elapsed from the motor vehicle accidents and the lack of an initial clinical examination. However, MRI studies (except in one patient who only underwent a CT scan) allowed locations of the specific lesion to the AOP region in many of the patients, and bilateral thalamic-mesencephalic involvement was observed in all patients (except for patient 8, who only had a left-sided paramedian thalamic-mesencephalic contusion). In addition, in patient 1, only a left-sided thalamic-mesencephalic injury was observed, but a bilateral paramedian lesion was assumed due to the bilateral CN III paresis. Based on the anatomical locations of the lesions on brain MRI and the clinical examination characteristics of the vertical paresis in our patients, it was assumed that there was an injury to the riMLF, INC, and PC in all patients (and in some cases, joint injury to CN III). This assumption was supported by the finding that all movement types were affected in all of the patients (tracking, saccades, and no improvement with vestibulo-ocular reflexes [VORs]). In patient 3, it was assumed that there was a partial alteration of the PC because the vertical gaze paresis involved only a slight limitation of supraduction in the left eye without improvement with VORs. In patient 8, it was assumed that there was a partial disorder of the INC because the only deficit was the range of higher saccades without modification of the speed. Collier's sign was only present in patient 1.
In the vast majority of our patients, vertical gaze paresis (associated in some patients with a CN III paresis) was the fundamental and most disabling neurological sign. Only patient 4 had extensive brain damage with multiple sequelae after CET in addition to the vertical gaze paresis (left horizontal gaze paresis, partial paresis of the left CN III, posttraumatic right optic neuropathy, right hemiparesis, and right homonymous hemianopsia).
The relatively selective posttraumatic injury to the territory of the AOP in this group of patients was striking and raises some questions. First, what could be the mechanism of injury to the thalamoperforating branches when these vessels are affected in isolation or in association with other injuries in CET? Second, why is this region affected and not another?
Some authors have suggested that the unique anatomy of the angle of penetration of the lenticulostriate arteries makes them more vulnerable to selectively isolated damage in certain individuals that gives rise to certain CET patterns. ,, These authors propose a mechanism of intimal damage during trauma with subsequent thrombosis, ,, although vasospasm is not ruled out as the primary process. A similar pathogenic mechanism (unique anatomy of the angle of penetration) could be considered in the case of the thalamoperforating branches, which would explain the clinical and radiological findings in our patients. For example, we found one case of isolated thalamic involvement after CET presented in the literature by Kuroiwa et al.  This case involved a patient who presented with isolated areas of infarct in the thalamic-mesencephalic region after suffering an automobile accident. Cerebral angiography showed an irregularity of the basilar artery and fusiform dilatation of the thalamoperforating branches. The authors proposed that the compression of the basilar artery in the clivus caused thrombus formation that in turn, occluded the thalamoperforating branches.
Finally, it is also noteworthy that there were signs of hemorrhagic transformation in the thalamic-mesencephalic region on T2-Weighted sequences of brain MRI scans in four patients in our study. These findings may represent hemorrhagic suffusions after injury to the thalamoperforating branches, although a hemorrhagic contusion could not be ruled out in some patients. As discussed above, the prognosis is relatively good in ischemic thalamic lesions compared with hemorrhagic lesions. 
There are other possible pathogenetic mechanisms described in the literature that could explain the semiology of our patients. For example, the most common mechanism of infarction is vascular compression, which occurs as a result of the mass effect of cerebral contusion or falcine or transtentorial herniation.  This mass effect can also produce stretching of the small perforating vessels (e.g. lenticulostriate or thalamoperforating arteries), causing ischemia. However, in the cases in our study, there was no documentation in any cases of cerebral herniation or diffuse cerebral edema in the neuroimaging studies performed in the acute phase immediately after the trauma.
Another possible mechanism of intracerebral vascular damage is arterial dissection. This mechanism occurs frequently by direct damage at the cervical carotid artery or at the supraclinoid level.  In our patients, in the neuroimaging studies conducted we didn't detect any arterial dissection neither in acute or chronic phase, hence, it is unlikely that this etiopathogenic mechanism occurred in our series of cases.
Finally, in many patients, there is a mechanism of diffuse axonal injury, which results from accelerative-decelerative forces associated with high-energy head trauma. The most susceptible areas to this type of damage are the union of the gray matter to white matter and the region adjacent to the falx. MRI of the brain indicated that none of the patients in our study had damage located in these areas. Patients with diffuse axonal injury often have extensive damage in regions of the brain that do not correspond to anatomical regions of arterial supply. This observation contrasts with the midbrain-thalamic area specifically involved in our patients which strictly corresponds to the territory supplied by the AOP. 
Therefore, we believe that the mechanism that best explains the semiology found in our patients is the unique anatomy of the angle of penetration of the lenticulostriate arteries making them more vulnerable to selective isolated damage in certain individuals that gives rise to certain CET patterns. ,,
In summary, posttraumatic vertical gaze paresis associated with posttraumatic contusion of the bilateral thalamic-mesencephalic region corresponding to the territory of the AOP is a rare phenomenon reported in the scientific literature that can occur in isolation or in association with other neurological deficits and cause significantly reduced quality-of-life for patients.
| References|| |
Amin OS, Shwani SS, Zangana HM, Hussein EM, Ameen NA. Bilateral infarction of paramedian thalami: A report of two cases of artery of percheron occlusion and review of the literature. BMJ Case Rep 2011;2011:pii: Bcr0920103304.
Lazzaro NA, Wright B, Castillo M, Fischbein NJ, Glastonbury CM, Hildenbrand PG, et al.
Artery of percheron infarction: Imaging patterns and clinical spectrum. AJNR Am J Neuroradiol 2010;31:1283-9.
Server A, Dullerud R, Haakonsen M, Nakstad PH, Johnsen UL, Magnaes B. Post-traumatic cerebral infarction. Neuroimaging findings, etiology and outcome. Acta Radiol 2001;42:254-60.
Fukuda T, Hasue M, Ito H. Does traumatic subarachnoid hemorrhage caused by diffuse brain injury cause delayed ischemic brain damage? Comparison with subarachnoid hemorrhage caused by ruptured intracranial aneurysms. Neurosurgery 1998;43:1040-9.
Takahashi I, Abumiya T, Imamura H, Saitoh H, Nomura M, Hokin K, et al.
A case of posttraumatic delayed cerebral arterial spasm; case report and review of the literature on the pathogenesis. No Shinkei Geka 1992;20:161-4.
Carrera E, Michel P, Bogousslavsky J. Anteromedian, central, and posterolateral infarcts of the thalamus: Three variant types. Stroke 2004;35:2826-31.
Kumral E, Evyapan D, Balkir K, Kutluhan S. Bilateral thalamic infarction. Clinical, etiological and MRI correlates. Acta Neurol Scand 2001;103:35-42.
Jiménez Caballero PE. Bilateral paramedian thalamic artery infarcts: Report of 10 cases. J Stroke Cerebrovasc Dis 2010;19:283-9.
Rubio-Pérez MÁ, Gálvez-Ruiz AL, Sepúlveda-Gázquez M, Planellas-Giné L, Roquer-González J. Review of the model of vertical gaze control. Rev Neurol 2011;53:477-82.
Clark JM, Albers GW. Vertical gaze palsies from medial thalamic infarctions without midbrain involvement. Stroke 1995;26:1467-70.
Seçkin H, Demirci AY, Degerliyurt A, Dagli M, Bavbek M. Posttraumatic infarction in the basal ganglia after a minor head injury in a child: Case report. Turk Neurosurg 2008;18:415-9.
Dharker SR, Mittal RS, Bhargava N. Ischemic lesions in basal ganglia in children after minor head injury. Neurosurgery 1993;33:863-5.
Umansky F, Gomes FB, Dujovny M, Diaz FG, Ausman JI, Mirchandani HG, et al.
The perforating branches of the middle cerebral artery. A microanatomical study. J Neurosurg 1985;62:261-8.
Kuroiwa T, Tanabe H, Takatsuka H, Arai M, Ozaki T, Nagasawa S, et al.
Paramedian thalamic infarction following blunt head injury - Case report. Neurol Med Chir (Tokyo) 1994;34:20-2.
Liu J, Kou Z, Tian Y. Diffuse axonal injury after traumatic cerebral microbleeds: An evaluation of imaging techniques. Neural Regen Res 2014;9:1222-30.
[Figure 1], [Figure 2]