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Vertical gaze palsy associated with bilateral ptosis following right putaminal hemorrhage
Case Report
Vertical Gaze Palsy Associated With Bilateral Ptosis Following Right Putaminal Hemorrhage Tadashi Kanda,
MD,*
Kunihiko Azuma,
MD,†
and Fumihiko Sakai,
MD,†
Previous reports suggest that right hemispheric lesions may produce a variety of disorders in eye opening, including bilateral eyelid ptosis. More recently, bilateral ptosis and a severe deficit of upward gaze while preserving the downward gaze have been reported in patients with right hemispheric infarction. In the present report, we describe 2 patients who showed downward gaze palsy in addition to upward gaze palsy, accompanied by bilateral ptosis following right putaminal hemorrhage. The 2 patients displayed acute onset of similar ocular manifestations, such as difficulty in eye opening, upward and downward gaze palsy, and conjugate horizontal deviation in addition to left hemiparesis. The principal cause of difficulty in eye opening was considered to be bilateral ptosis. Computed tomography performed on admission revealed a moderate-sized hematoma in the right putamen. There was no evidence of midbrain involvement. These ocular symptoms were restored within a few weeks after the onset of stroke. The ocular manifestations noted in our patients suggest that the descending pathways arising from the supranuclear centers to the midbrain, which control vertical movement of the eyes and the eyelids, may be impaired by putaminal hemorrhage. To our knowledge, this is the first report of such ocular manifestations in the right hemispheric lesion. Key Words: Vertical gaze palsy—ptosis—putaminal hemorrhage. Copyright © 2002 by National Stroke Association
Eyelid ptosis or vertical gaze palsy is caused by midbrain lesions.1,2 In addition, large lesions within the cerebral hemisphere may also produce impairment of vertical eye movement3 or a variety of disorders in eye opening, including bilateral eyelid ptosis.4-10 However, such cases are quite uncommon, and the anatomical site
From the *Department of Neurology, Kitasato University Hospital and School of Allied Health Sciences, Kitasato University, and †Department of Neurology, Kitasato University School of Medicine, Kanagawa, Japan. Received February 12, 2002, accepted April 4, 2002. Address reprint requests to Fumihiko Sakai, MD, Department of Neurology, Kitasato University School of Medicine, 1-15-1 Kitasato, Sagamihara-shi, Kanagawa 228-8555, Japan. Copyright © 2002 by National Stroke Association 1052-3057/02/1102-0001$35.00/0 doi:10.1053/jscd.2002.126692
of the hemispheric lesion responsible for these ocular manifestations is poorly documented. In the present report, we describe 2 patients who developed bilateral ptosis with vertical gaze palsy following the onset of right putaminal hemorrhage. These ocular abnormalities may contribute to a clarification of the mechanisms that work in the supranuclear ocular control system.
Case Reports Patient 1 A 56-year-old, right-handed, hypertensive woman was admitted to the hospital 4 hours after the onset of weakness in her left limbs. On admission she looked obtunded, but was well-oriented. She was able to select and show her right finger exactly without failure upon verbal com-
Journal of Stroke and Cerebrovascular Diseases, Vol. 11, No. 2 (March-April), 2002: pp 113-116
113
T. KANDA ET AL.
114
Figure 1. Photograph shows vertical gaze palsy associated with bilateral eyelid ptosis in patient 1. (A) The eyebrows were markedly elevated and many wrinkles were produced in the forehead. Photograph was taken 2 days after onset. (B, C) Two slices of the cranial computed tomography reveal a medium-sized circumscribed hematoma in the right putamen. The scanning was performed 2 days after onset. (D, E, F) Photograph shows ocular movement in the vertical direction, (D) upward gaze, (E) primary position, and (F) downward gaze. (G) The ptosis subsequently became completely resolved. The photograph was taken on the 30th day after onset.
mand. She had severe left hemiparesis involving the face and tongue with hemihypesthesia. She neglected the left side of her body and denied disability in the left extremities. Her eyes were in a state of closure. However, when asked to open her eyes, the forehead muscles markedly contracted with elevation of the eyebrows, and the bilateral eyes opened slightly (Fig 1A). She was able to close her eyes tightly in response to verbal command. She was well aware of the difficulties in opening her eyes and occasionally raised her eyelids with her right fingers to see objects. Although her eyes tended to deviate to the right, horizontal extraocular movements were full. Complete paralysis of upward and downward gaze was evident. Bell’s phenomenon was preserved. The pupils were 3.5 mm in diameter, equal, and promptly reactive to light and near stimuli. Computed tomography (CT) performed on admission revealed a circumscribed hematoma in the
right putamen. No evidence of midbrain involvement was observed (Fig 1B and C). Within 48 hours of onset, improvement in eyelid ptosis gradually occurred. However, bilateral lid ptosis and vertical gaze impairment were still evident (Fig 1D-F). By the end of the second hospital week, she was able to open the eyes without difficulty (Fig 1G), (all photographs were taken after obtaining informed consent from the patient to report and/or publish case details). Vertical gaze palsy also gradually improved and completely disappeared within 2 weeks after the onset of hemorrhage. Recovery of left hemiparesis was poor, and she was discharged in a wheelchair. Patient 2 A 56-year-old, right-handed man who had a longstanding history of hypertension was admitted with
VERTICAL GAZE PALSY AFTER RIGHT PUTAMINAL HEMORRHAGE
acute onset of left-sided weakness. On examination 3 hours after onset, he was slightly lethargic but was able to follow simple verbal commands and to answer questions correctly. He demonstrated left hemiparesis involving the face and tongue with an extensor plantar response. Although his eyes remained closed, he attempted to open them occasionally. He was fully aware of difficulties in opening his eyes and complained of the trouble. When he tried to open his eyes in response to verbal commands, the eyebrows were elevated and many wrinkles appeared on the forehead. He showed some difficulty in initiating eye opening, and the eyes were not fully opened, even when the eyelids were voluntarily raised. Although conjugate ocular deviation to the right was noted, he was able to move his eyes to the left on command. He displayed almost complete paralysis of upward and downward gaze. The pupils were equal and 4 mm in diameter, and direct and consensual light reflexes were prompt bilaterally. In response to verbal commands, he was able to close his eyes tightly and to protrude his tongue without any difficulty. A CT scan demonstrated a moderate-sized hematoma in the right putamen. No ventricular extension of the hematoma was detected. Difficulties in eye opening improved gradually after admission, and the palpebral fissures widened by degrees. In the following 2 weeks, ptosis resolved and conjugate deviation of the eyes and paralysis of vertical gaze recovered.
Discussion The 2 patients described herein displayed acute onset of common ocular manifestations, such as difficulties in eye opening, vertical gaze palsy, and conjugate horizontal deviation, in addition to left hemiparesis following right putaminal hemorrhage. These symptoms resolved within a few weeks, while left hemiparesis persisted. Although Patient 2 displayed some difficulties in initiating eye opening in addition to ptosis, which might be ascribed to a kind of apraxia, the principal cause of impaired eye opening was considered to be bilateral ptosis. The central caudal nucleus (CCN), which contains bilateral levator neurons, lies in conjoined portions of the oculomotor nuclear complex, and the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) concerned with vertical eye movement is located in the midbrain. Therefore, lesions of the midbrain are known to cause eyelid ptosis and/or vertical gaze palsy.1,2 However ocular manifestations of the present 2 patients seem unlikely to have occurred due to direct involvement of the oculomotor nuclear complex following putaminal hemorrhage, since pupil reactivity was well-preserved throughout the clinical course. When examining whether hemispheric lesions were responsible for bilateral ptosis, Nutt et al.5 speculated
115
that ptosis is produced only when the cortical fibers from both hemispheres are bilaterally disrupted, as noted in manifestations of bilateral cortical disease, such as pseudobulbar palsy. However, in most reported cases of bilateral ptosis or lid abnormalities, patients had difficulty in eye opening following the acute hemispheric lesion, predominantly with extensive right-sided lesions.4-7 These results suggest that the bilateral ptosis noted in our patients might be attributable to right hemispheric lesions. Recently, Averbuch-Heller et al.10 reported 3 patients with right hemispheric infarction, in whom bilateral ptosis was accompanied by impaired upward gaze while preserving downward gaze. They presumed that the reason for the preserved downward gaze was the tight cerebral hemispheric coordination existing between upward movements of the eyes and eyelids. Previously, we reported 3 patients with bilateral ptosis secondary to acute right hemispheric infarction. One of those patients revealed downgaze palsy in addition to upgaze palsy,7 as observed in the present 2 patients. To our knowledge, similar ocular abnormalities have not been previously reported. Studies have shown that lesions in the unilateral cerebral cortex or unilateral electrical stimulation within the diencephalon cause paralysis of vertical eye movements.3 Furthermore, premotor saccadic signals to the levator palpebrae and vertical eye muscles are presumed to originate from a common source, and signals for both upward gaze and downward gaze contribute to the control of the levator palpebrae muscle.9 Accordingly, the ocular manifestations observed in the present patients might have been produced by lesions in the pathways arising from the eye field of the frontal lobe to the midbrain. The possibility exists, however, that vertical gaze palsy resulted from compression of the vertical gaze center or related supranuclear pathways in the mesencephalic-diencephalic junction following putaminal hemorrhage. Vertical gaze palsy associated with bilateral ptosis may be frequently overlooked in routine clinical examinations in patients with acute hemispheric stroke, since an inability to open the eyes is apt to be mistaken for unconsciousness. These ocular manifestations seem to be identified more frequently than expected if ocular symptoms are carefully examined in patients with acute right hemispheric stroke.
References 1. Buttner-Ennever J, Buttner U, Cohen B, et al. Vertical gaze paralysis and the rostral interstitial nucleus of the medial longitudinal fasciculus. Brain 1982;105:125149.
116 2. Growdon JH, Winkler GF, Wray SH. Midbrain ptosis; A case with clinicopathologic correlation. Arch Neurol 1974;30:179-181. 3. Bender MB. Brain control of conjugate horizontal and vertical eye movements: A survey of the structural and functional correlates. Brain 1980;103:23-69. 4. Caplan LR. Ptosis. J Neurol Neurosurg Psychiatry 1974; 37:1-7. 5. Nutt JG. Lid abnormalities secondary to cerebral hemisphere lesions. Ann Neurol 1977;1:149-151. 6. Lepore FE: Bilateral cerebral ptosis. Neurology 1987;37: 1043-1046.
T. KANDA ET AL. 7. Azuma K, Kanda T, Aoki S, et al. Bilateral eyelid ptosis due to cerebral hemispheric infarction. Rinsho Shinkeigaku 1988;28:1017-1022. 8. Johnston JC, Rosenbaum DM, Picone CM, et al. Apraxia of eyelid opening secondary to right hemisphere infarction. Ann Neurol 1989;25:622-624. 9. Schmidtke K, Buttner-Ennever JA. Nervous control of eyelid function. A review of clinical, experimental and pathological data. Brain 1992;115:227-247. 10. Averbuch-Heller L, Stahl JS, Remler BF, et al. Bilateral ptosis and upgaze palsy with right hemispheric lesions. Ann Neurol 1996;40:465-468.
Vertical Gaze Palsy Associated With Bilateral Ptosis Following Right Putaminal Hemorrhage Tadashi Kanda,
MD,*
Kunihiko Azuma,
MD,†
and Fumihiko Sakai,
MD,†
Previous reports suggest that right hemispheric lesions may produce a variety of disorders in eye opening, including bilateral eyelid ptosis. More recently, bilateral ptosis and a severe deficit of upward gaze while preserving the downward gaze have been reported in patients with right hemispheric infarction. In the present report, we describe 2 patients who showed downward gaze palsy in addition to upward gaze palsy, accompanied by bilateral ptosis following right putaminal hemorrhage. The 2 patients displayed acute onset of similar ocular manifestations, such as difficulty in eye opening, upward and downward gaze palsy, and conjugate horizontal deviation in addition to left hemiparesis. The principal cause of difficulty in eye opening was considered to be bilateral ptosis. Computed tomography performed on admission revealed a moderate-sized hematoma in the right putamen. There was no evidence of midbrain involvement. These ocular symptoms were restored within a few weeks after the onset of stroke. The ocular manifestations noted in our patients suggest that the descending pathways arising from the supranuclear centers to the midbrain, which control vertical movement of the eyes and the eyelids, may be impaired by putaminal hemorrhage. To our knowledge, this is the first report of such ocular manifestations in the right hemispheric lesion. Key Words: Vertical gaze palsy—ptosis—putaminal hemorrhage. Copyright © 2002 by National Stroke Association
Eyelid ptosis or vertical gaze palsy is caused by midbrain lesions.1,2 In addition, large lesions within the cerebral hemisphere may also produce impairment of vertical eye movement3 or a variety of disorders in eye opening, including bilateral eyelid ptosis.4-10 However, such cases are quite uncommon, and the anatomical site
From the *Department of Neurology, Kitasato University Hospital and School of Allied Health Sciences, Kitasato University, and †Department of Neurology, Kitasato University School of Medicine, Kanagawa, Japan. Received February 12, 2002, accepted April 4, 2002. Address reprint requests to Fumihiko Sakai, MD, Department of Neurology, Kitasato University School of Medicine, 1-15-1 Kitasato, Sagamihara-shi, Kanagawa 228-8555, Japan. Copyright © 2002 by National Stroke Association 1052-3057/02/1102-0001$35.00/0 doi:10.1053/jscd.2002.126692
of the hemispheric lesion responsible for these ocular manifestations is poorly documented. In the present report, we describe 2 patients who developed bilateral ptosis with vertical gaze palsy following the onset of right putaminal hemorrhage. These ocular abnormalities may contribute to a clarification of the mechanisms that work in the supranuclear ocular control system.
Case Reports Patient 1 A 56-year-old, right-handed, hypertensive woman was admitted to the hospital 4 hours after the onset of weakness in her left limbs. On admission she looked obtunded, but was well-oriented. She was able to select and show her right finger exactly without failure upon verbal com-
Journal of Stroke and Cerebrovascular Diseases, Vol. 11, No. 2 (March-April), 2002: pp 113-116
113
T. KANDA ET AL.
114
Figure 1. Photograph shows vertical gaze palsy associated with bilateral eyelid ptosis in patient 1. (A) The eyebrows were markedly elevated and many wrinkles were produced in the forehead. Photograph was taken 2 days after onset. (B, C) Two slices of the cranial computed tomography reveal a medium-sized circumscribed hematoma in the right putamen. The scanning was performed 2 days after onset. (D, E, F) Photograph shows ocular movement in the vertical direction, (D) upward gaze, (E) primary position, and (F) downward gaze. (G) The ptosis subsequently became completely resolved. The photograph was taken on the 30th day after onset.
mand. She had severe left hemiparesis involving the face and tongue with hemihypesthesia. She neglected the left side of her body and denied disability in the left extremities. Her eyes were in a state of closure. However, when asked to open her eyes, the forehead muscles markedly contracted with elevation of the eyebrows, and the bilateral eyes opened slightly (Fig 1A). She was able to close her eyes tightly in response to verbal command. She was well aware of the difficulties in opening her eyes and occasionally raised her eyelids with her right fingers to see objects. Although her eyes tended to deviate to the right, horizontal extraocular movements were full. Complete paralysis of upward and downward gaze was evident. Bell’s phenomenon was preserved. The pupils were 3.5 mm in diameter, equal, and promptly reactive to light and near stimuli. Computed tomography (CT) performed on admission revealed a circumscribed hematoma in the
right putamen. No evidence of midbrain involvement was observed (Fig 1B and C). Within 48 hours of onset, improvement in eyelid ptosis gradually occurred. However, bilateral lid ptosis and vertical gaze impairment were still evident (Fig 1D-F). By the end of the second hospital week, she was able to open the eyes without difficulty (Fig 1G), (all photographs were taken after obtaining informed consent from the patient to report and/or publish case details). Vertical gaze palsy also gradually improved and completely disappeared within 2 weeks after the onset of hemorrhage. Recovery of left hemiparesis was poor, and she was discharged in a wheelchair. Patient 2 A 56-year-old, right-handed man who had a longstanding history of hypertension was admitted with
VERTICAL GAZE PALSY AFTER RIGHT PUTAMINAL HEMORRHAGE
acute onset of left-sided weakness. On examination 3 hours after onset, he was slightly lethargic but was able to follow simple verbal commands and to answer questions correctly. He demonstrated left hemiparesis involving the face and tongue with an extensor plantar response. Although his eyes remained closed, he attempted to open them occasionally. He was fully aware of difficulties in opening his eyes and complained of the trouble. When he tried to open his eyes in response to verbal commands, the eyebrows were elevated and many wrinkles appeared on the forehead. He showed some difficulty in initiating eye opening, and the eyes were not fully opened, even when the eyelids were voluntarily raised. Although conjugate ocular deviation to the right was noted, he was able to move his eyes to the left on command. He displayed almost complete paralysis of upward and downward gaze. The pupils were equal and 4 mm in diameter, and direct and consensual light reflexes were prompt bilaterally. In response to verbal commands, he was able to close his eyes tightly and to protrude his tongue without any difficulty. A CT scan demonstrated a moderate-sized hematoma in the right putamen. No ventricular extension of the hematoma was detected. Difficulties in eye opening improved gradually after admission, and the palpebral fissures widened by degrees. In the following 2 weeks, ptosis resolved and conjugate deviation of the eyes and paralysis of vertical gaze recovered.
Discussion The 2 patients described herein displayed acute onset of common ocular manifestations, such as difficulties in eye opening, vertical gaze palsy, and conjugate horizontal deviation, in addition to left hemiparesis following right putaminal hemorrhage. These symptoms resolved within a few weeks, while left hemiparesis persisted. Although Patient 2 displayed some difficulties in initiating eye opening in addition to ptosis, which might be ascribed to a kind of apraxia, the principal cause of impaired eye opening was considered to be bilateral ptosis. The central caudal nucleus (CCN), which contains bilateral levator neurons, lies in conjoined portions of the oculomotor nuclear complex, and the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) concerned with vertical eye movement is located in the midbrain. Therefore, lesions of the midbrain are known to cause eyelid ptosis and/or vertical gaze palsy.1,2 However ocular manifestations of the present 2 patients seem unlikely to have occurred due to direct involvement of the oculomotor nuclear complex following putaminal hemorrhage, since pupil reactivity was well-preserved throughout the clinical course. When examining whether hemispheric lesions were responsible for bilateral ptosis, Nutt et al.5 speculated
115
that ptosis is produced only when the cortical fibers from both hemispheres are bilaterally disrupted, as noted in manifestations of bilateral cortical disease, such as pseudobulbar palsy. However, in most reported cases of bilateral ptosis or lid abnormalities, patients had difficulty in eye opening following the acute hemispheric lesion, predominantly with extensive right-sided lesions.4-7 These results suggest that the bilateral ptosis noted in our patients might be attributable to right hemispheric lesions. Recently, Averbuch-Heller et al.10 reported 3 patients with right hemispheric infarction, in whom bilateral ptosis was accompanied by impaired upward gaze while preserving downward gaze. They presumed that the reason for the preserved downward gaze was the tight cerebral hemispheric coordination existing between upward movements of the eyes and eyelids. Previously, we reported 3 patients with bilateral ptosis secondary to acute right hemispheric infarction. One of those patients revealed downgaze palsy in addition to upgaze palsy,7 as observed in the present 2 patients. To our knowledge, similar ocular abnormalities have not been previously reported. Studies have shown that lesions in the unilateral cerebral cortex or unilateral electrical stimulation within the diencephalon cause paralysis of vertical eye movements.3 Furthermore, premotor saccadic signals to the levator palpebrae and vertical eye muscles are presumed to originate from a common source, and signals for both upward gaze and downward gaze contribute to the control of the levator palpebrae muscle.9 Accordingly, the ocular manifestations observed in the present patients might have been produced by lesions in the pathways arising from the eye field of the frontal lobe to the midbrain. The possibility exists, however, that vertical gaze palsy resulted from compression of the vertical gaze center or related supranuclear pathways in the mesencephalic-diencephalic junction following putaminal hemorrhage. Vertical gaze palsy associated with bilateral ptosis may be frequently overlooked in routine clinical examinations in patients with acute hemispheric stroke, since an inability to open the eyes is apt to be mistaken for unconsciousness. These ocular manifestations seem to be identified more frequently than expected if ocular symptoms are carefully examined in patients with acute right hemispheric stroke.
References 1. Buttner-Ennever J, Buttner U, Cohen B, et al. Vertical gaze paralysis and the rostral interstitial nucleus of the medial longitudinal fasciculus. Brain 1982;105:125149.
116 2. Growdon JH, Winkler GF, Wray SH. Midbrain ptosis; A case with clinicopathologic correlation. Arch Neurol 1974;30:179-181. 3. Bender MB. Brain control of conjugate horizontal and vertical eye movements: A survey of the structural and functional correlates. Brain 1980;103:23-69. 4. Caplan LR. Ptosis. J Neurol Neurosurg Psychiatry 1974; 37:1-7. 5. Nutt JG. Lid abnormalities secondary to cerebral hemisphere lesions. Ann Neurol 1977;1:149-151. 6. Lepore FE: Bilateral cerebral ptosis. Neurology 1987;37: 1043-1046.
T. KANDA ET AL. 7. Azuma K, Kanda T, Aoki S, et al. Bilateral eyelid ptosis due to cerebral hemispheric infarction. Rinsho Shinkeigaku 1988;28:1017-1022. 8. Johnston JC, Rosenbaum DM, Picone CM, et al. Apraxia of eyelid opening secondary to right hemisphere infarction. Ann Neurol 1989;25:622-624. 9. Schmidtke K, Buttner-Ennever JA. Nervous control of eyelid function. A review of clinical, experimental and pathological data. Brain 1992;115:227-247. 10. Averbuch-Heller L, Stahl JS, Remler BF, et al. Bilateral ptosis and upgaze palsy with right hemispheric lesions. Ann Neurol 1996;40:465-468.