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Respiratory failure with cervicomedullary infarctions
J Stroke Cerebraoasc Dis 1995;5:61-65 © 1995 National Stroke Association
Respiratory Failure with Cervicomedullary Infarctions IJ effrey 1. Frank, M.D., and 2J ose Biller, M.D.
Respiratory failure from brainstern and spinal cord infarction has been described without attention to ventilatory characteristics and prognosis. We describe two patients who suffered from complete aventilation with cervicomedullary infarctions. One achieved full recovery of spontaneous breathing, and the other had persistent aventilation until her death 4 months after her stroke from sepsis. The anatomical extent of the infarction as identified by magnetic resonance imaging was predictive of the recoverability of spontaneous breathing, and important clinical considerations are emphasized when considering weaning a patient from mechanical ventilation after respiratory failure from cervicomedullary infarction. Key Words: Stroke-Infarction-Brainstem-Respiratory failure.
Normal respiratory function depends on the harmonious balance of numerous factors. The most important sensors of respiratory needs are the central and peripheral chemoreceptors and airway receptors, conveying information to various levels of the nervous system which, in turn, modulate the lungs, upper airway, and respiratory musculature. The brainstem is the primary site of automatic respiratory control, and the cerebral cortex governs voluntary respiration. Integration of the output of these anatomically and functionally separate respiratory control systems occurs primarily at the spinal cord level. The final common pathway of neural effector control is the inspiratory and expiratory spinal motoneurons innervating respiratory musculature. Lesions at various sites of the nervous system can cause recognizable breathing pattern abnormalities. From IThe Cleveland Clinic Foundation, Cleveland, OH, and the 2Department of Neurology, Indiana University School of Medicine, Indianapolis, IN, U.S.A. Presented in part at the 45th Annual American Academy of Neurology Meeting in New York, April 1993. Address correspondence and reprint requests to Dr. ]. Biller at Department of Neurology, Indiana University School of Medicine, Emerson Hall, Room 125,545 Barnhill Drive, Indianapolis, IN 46202-5124, U.S.A.
Respiratory failure from aventilation has been described with a variety of cervicomedullary lesions, infarction notwithstanding. We describe two patients who suffered complete aventilation from cervicomedullary infarction, focusing on their prognosis for recovery of spontaneous breathing and review of relevant literature.
Case Reports Case 1 A previously healthy, 39-year-old man developed dysarthria, quadriplegia, and respiratory arrests over a 24-h period, 6 days after unprovoked acute neck pain. Examination, angiography, and magnetic resonance imaging (MRl) corroborated a right ventrolateral medullary infarction and bilaterally symmetric ventral cervicomedullary infarction secondary to a right vertebral artery dissection (Figs. 1 and 2). He had no inspiratory effort until 9 weeks after his stroke when he was successfully weaned from the ventilator by increasingly frequent and prolonged T-piece trials, with postweaning observation for apneic periods, particularly during sleep. He has remained stable with nor-
] STROKE CEREBROVASC DIS, VOL. 5, NO.2, 1995
61
]. 1. FRANK AND ]. BILLER
. .. . .
"
Figure 1. Case 1. Selective vertebral angiograms. The oblique (top) and lateral (middle) views of the left vertebral injection
demonstrate characteristic smooth tapering ofthelumen consistent with dissection, compared to thenormal intraluminal architecture shown in the anteroposterior view after rightvertebral injection (bottom). 62
] STROKE CEREBROVASC DIS, VOL. 5, NO.2, 1995
Figure 2. Case 1. MRl scans. There isalowsignal abnonnality in the right ventrolateral medulla on axial T1-weighted images (top). AxialTl-weighted images demonstrate highsignal abnormalities oftheright ventrolateral medulla andbilateral ventral cervical spinal cord (middle and bottom).
mal breathing for the past 25 months since mechanical ventilation was terminated, but he still is markedly debilitated and fully dependent for activities of daily living.
RESPIRATORY FAILURE WITH CERVICOMEDULLARY INFARCTIONS
Figure 3. Case 2. MR1 scans. Sagittal Tl-weightedimages (top) demonstrate aroundhighsigrtal abnonnality in thecentral midmedullary region andalongitudinally oriented homogeneous highsignalabnormality involvingtheentire ventral cervical spinalcord. AxialTl-weighted images (bottom) show high signalabnormalities in the ventral medulla and cervical spinal cord bilaterally.
Case 2 A 23-year-old woman developed a rapidly progressive quadriplegia and respiratory arrest several hours after unprovoked acute posterior neck pain. Examination, angiography, and MRI revealed spinal cord infarction without identified arterial pathology (Fig. 3). Comprehensive evaluation for underlying cardiac pathology or coagulopathy was unrevealing. Frequent assessments of spontaneous breathing documented no inspiratory effort with associated carbon dioxide retention through 17 weeks after her event, when she died of Gram-negative sepsis. Postmortem examination revealed normal cerebral vasculature including the vertebrobasilar system. There
was a central cavitation in the midcaudal medulla extending inferiorly to the region of the right medullary pyramid. Marked gliosis of the medial longitudinal fasciculus and the medial portion of the inferior olivary nuclear complex was noted, and there was neuronal loss and gliosis of the dorsal motor and hypoglossal nuclei. Spinal cord examination revealed complete cavitation of the entire ventral cervical and upper thoracic spinal cord, extending into the ventral quadrant regions at the cervical level, right more than left. Also, there was cavitation of the central spinal cord gray matter and right dorsal horn with sparing of the dorsal columns and left dorsal horn. ] STROKE CEREBROVASC DIS, VOL. 5, NO.2, 1995
63
t. 1. FRANK AND ]. BILLER Table 1. Reference
No. of patients
Case
1
2
2
3
2
1
Case reports of respiratory failure with cervicomedullary infarctions Respiratory symptoms
Respiratory outcome
1
Complete aventilation
Persisted until death
Right caudal brainstem infarction
2
Hypoventilation
Resolved after 7 days
1
Complete aventilation
Improved to hypoventilation during sleep
2
"Ondine's curse"
N/A
"Ondine's curse"
Persisted through follow-up at 5 months Improved to full independent breathing awake and asleep by day 30
Occluded left vertebral artery; recent left dorsolateral medullary infarction Left vertebral thrornbus; left inferior cerebellar infarclion; left ventrelateral medullary infarct N/A
Discussion Case 1 had a full recovery of spontaneous breathing while awake and asleep, as opposed to Case 2 who had persistent aventilation until her death at 17 weeks after her stroke. The anatomical extent of involvement was much more confined in Case 1 with predominantly right lower brainstem infarction and midline bilateral ventral upper cervical spinal cord infarction. Case 2 had asymmetric infarction of the entire lower portion of the ventral medulla involving the entire ventrolateral cervical and thoracic spinal cord. Few case reports and series document the prognosis of respiratory failure with cervicomedullary infarction (1-3) (Table 1). Some of the most lucid reports focus on autopsy description and correlation with known respiratory control mechanisms. Two of five of these cases improved to unsupported spontaneous breathing when awake and asleep, and one improved to hypoventiIation/apnea during sleep from complete aventilation at onset. Apnea during sleep was the cause of death in two of these reported cases; one died suddenly from myocardial infarction 3 months 64
JSTROKE CEREBROVASC DIS, VOL. 5, NO.2,
1995
Anatomic lesions
Distal left vertebral stenosis Infarction of left lateral medulla and left ventrolateral upper cervical cord
Comments Respiratory symptoms began 4 days after presentation; pneumonia was cause of death Died of apnea during sleep on day 12
Died of apnea during sleep on day 31
Died suddenly 3 months after the stroke of an unknown cause; this was solely a unilateral stroke
after the stroke, and one died of sepsis from Pseudomonas pneumonia. Of the four who died, death occurred from 12 to 31 days after the stroke (mean, 21 days). Unilateral brainstem infarction has been reported to cause respiratory failure similar to Case I, and two of the three most recently reported cases ultimately achieved full recovery of spontaneous breathing (awake and asleep), 7 and 30 days after their strokes. However, the one with "recovery" on day 7 died from apnea on day 12. Persistent aventilation is wellrecognized to occur with bilateral lower brainstem and cervical spinal cord lesions as extensive as the infarction of Case 2, and the MRI identification of the extent of her infarction was predictive of her poor prognosis for recovery of spontaneous breathing. We conclude that: (a) cervicomedullary infarction is an important cause of prolonged aventilation; (b) the prognosis for respiratory recovery depends on the extent of the infarction and can be estimated with the assistance ofMRI studies; and (c) frequent assessment of spontaneous respiratory parameters optimizes potential for successful discontinuance of
RESPIRATORY FAILURE WITH CERVICOMEDULLARY INFARCTIONS
mechanical ventilation. Due to the separate anatomical control of automatic and voluntary breathing, successful weaning from a mechanical ventilator during wakefulness does not necessarily translate to effective breathing during sleep. Prolonged apnea monitoring, or continuous end-tidal carbon dioxide monitoring and pulse oximetry in those patients with continued endotracheal intubation or tracheostomy, is strongly recommended after "successful" weaning from mechanical ventilation.
References 1. Bogousslavsky J, Khurana R, Derauz JP, et al. Respiratory failure and unilateral caudal brainstem infarction. Ann Neurol1990;28:668-73.
2. Devereaux NM, Kean JR, Davis RL Automatic respiratory failure associated with infarction of the medulla. Arch Neurol1973;29:46-52. 3. Levin BE, Margolis G. Acute failure of automatic respirations secondary to unilateral brainstem infarct. Ann Neurol1977;1:583-6.
J STROKE CEREBROVASC DIS, VOL. 5, NO.2,
1995
65
Respiratory Failure with Cervicomedullary Infarctions IJ effrey 1. Frank, M.D., and 2J ose Biller, M.D.
Respiratory failure from brainstern and spinal cord infarction has been described without attention to ventilatory characteristics and prognosis. We describe two patients who suffered from complete aventilation with cervicomedullary infarctions. One achieved full recovery of spontaneous breathing, and the other had persistent aventilation until her death 4 months after her stroke from sepsis. The anatomical extent of the infarction as identified by magnetic resonance imaging was predictive of the recoverability of spontaneous breathing, and important clinical considerations are emphasized when considering weaning a patient from mechanical ventilation after respiratory failure from cervicomedullary infarction. Key Words: Stroke-Infarction-Brainstem-Respiratory failure.
Normal respiratory function depends on the harmonious balance of numerous factors. The most important sensors of respiratory needs are the central and peripheral chemoreceptors and airway receptors, conveying information to various levels of the nervous system which, in turn, modulate the lungs, upper airway, and respiratory musculature. The brainstem is the primary site of automatic respiratory control, and the cerebral cortex governs voluntary respiration. Integration of the output of these anatomically and functionally separate respiratory control systems occurs primarily at the spinal cord level. The final common pathway of neural effector control is the inspiratory and expiratory spinal motoneurons innervating respiratory musculature. Lesions at various sites of the nervous system can cause recognizable breathing pattern abnormalities. From IThe Cleveland Clinic Foundation, Cleveland, OH, and the 2Department of Neurology, Indiana University School of Medicine, Indianapolis, IN, U.S.A. Presented in part at the 45th Annual American Academy of Neurology Meeting in New York, April 1993. Address correspondence and reprint requests to Dr. ]. Biller at Department of Neurology, Indiana University School of Medicine, Emerson Hall, Room 125,545 Barnhill Drive, Indianapolis, IN 46202-5124, U.S.A.
Respiratory failure from aventilation has been described with a variety of cervicomedullary lesions, infarction notwithstanding. We describe two patients who suffered complete aventilation from cervicomedullary infarction, focusing on their prognosis for recovery of spontaneous breathing and review of relevant literature.
Case Reports Case 1 A previously healthy, 39-year-old man developed dysarthria, quadriplegia, and respiratory arrests over a 24-h period, 6 days after unprovoked acute neck pain. Examination, angiography, and magnetic resonance imaging (MRl) corroborated a right ventrolateral medullary infarction and bilaterally symmetric ventral cervicomedullary infarction secondary to a right vertebral artery dissection (Figs. 1 and 2). He had no inspiratory effort until 9 weeks after his stroke when he was successfully weaned from the ventilator by increasingly frequent and prolonged T-piece trials, with postweaning observation for apneic periods, particularly during sleep. He has remained stable with nor-
] STROKE CEREBROVASC DIS, VOL. 5, NO.2, 1995
61
]. 1. FRANK AND ]. BILLER
. .. . .
"
Figure 1. Case 1. Selective vertebral angiograms. The oblique (top) and lateral (middle) views of the left vertebral injection
demonstrate characteristic smooth tapering ofthelumen consistent with dissection, compared to thenormal intraluminal architecture shown in the anteroposterior view after rightvertebral injection (bottom). 62
] STROKE CEREBROVASC DIS, VOL. 5, NO.2, 1995
Figure 2. Case 1. MRl scans. There isalowsignal abnonnality in the right ventrolateral medulla on axial T1-weighted images (top). AxialTl-weighted images demonstrate highsignal abnormalities oftheright ventrolateral medulla andbilateral ventral cervical spinal cord (middle and bottom).
mal breathing for the past 25 months since mechanical ventilation was terminated, but he still is markedly debilitated and fully dependent for activities of daily living.
RESPIRATORY FAILURE WITH CERVICOMEDULLARY INFARCTIONS
Figure 3. Case 2. MR1 scans. Sagittal Tl-weightedimages (top) demonstrate aroundhighsigrtal abnonnality in thecentral midmedullary region andalongitudinally oriented homogeneous highsignalabnormality involvingtheentire ventral cervical spinalcord. AxialTl-weighted images (bottom) show high signalabnormalities in the ventral medulla and cervical spinal cord bilaterally.
Case 2 A 23-year-old woman developed a rapidly progressive quadriplegia and respiratory arrest several hours after unprovoked acute posterior neck pain. Examination, angiography, and MRI revealed spinal cord infarction without identified arterial pathology (Fig. 3). Comprehensive evaluation for underlying cardiac pathology or coagulopathy was unrevealing. Frequent assessments of spontaneous breathing documented no inspiratory effort with associated carbon dioxide retention through 17 weeks after her event, when she died of Gram-negative sepsis. Postmortem examination revealed normal cerebral vasculature including the vertebrobasilar system. There
was a central cavitation in the midcaudal medulla extending inferiorly to the region of the right medullary pyramid. Marked gliosis of the medial longitudinal fasciculus and the medial portion of the inferior olivary nuclear complex was noted, and there was neuronal loss and gliosis of the dorsal motor and hypoglossal nuclei. Spinal cord examination revealed complete cavitation of the entire ventral cervical and upper thoracic spinal cord, extending into the ventral quadrant regions at the cervical level, right more than left. Also, there was cavitation of the central spinal cord gray matter and right dorsal horn with sparing of the dorsal columns and left dorsal horn. ] STROKE CEREBROVASC DIS, VOL. 5, NO.2, 1995
63
t. 1. FRANK AND ]. BILLER Table 1. Reference
No. of patients
Case
1
2
2
3
2
1
Case reports of respiratory failure with cervicomedullary infarctions Respiratory symptoms
Respiratory outcome
1
Complete aventilation
Persisted until death
Right caudal brainstem infarction
2
Hypoventilation
Resolved after 7 days
1
Complete aventilation
Improved to hypoventilation during sleep
2
"Ondine's curse"
N/A
"Ondine's curse"
Persisted through follow-up at 5 months Improved to full independent breathing awake and asleep by day 30
Occluded left vertebral artery; recent left dorsolateral medullary infarction Left vertebral thrornbus; left inferior cerebellar infarclion; left ventrelateral medullary infarct N/A
Discussion Case 1 had a full recovery of spontaneous breathing while awake and asleep, as opposed to Case 2 who had persistent aventilation until her death at 17 weeks after her stroke. The anatomical extent of involvement was much more confined in Case 1 with predominantly right lower brainstem infarction and midline bilateral ventral upper cervical spinal cord infarction. Case 2 had asymmetric infarction of the entire lower portion of the ventral medulla involving the entire ventrolateral cervical and thoracic spinal cord. Few case reports and series document the prognosis of respiratory failure with cervicomedullary infarction (1-3) (Table 1). Some of the most lucid reports focus on autopsy description and correlation with known respiratory control mechanisms. Two of five of these cases improved to unsupported spontaneous breathing when awake and asleep, and one improved to hypoventiIation/apnea during sleep from complete aventilation at onset. Apnea during sleep was the cause of death in two of these reported cases; one died suddenly from myocardial infarction 3 months 64
JSTROKE CEREBROVASC DIS, VOL. 5, NO.2,
1995
Anatomic lesions
Distal left vertebral stenosis Infarction of left lateral medulla and left ventrolateral upper cervical cord
Comments Respiratory symptoms began 4 days after presentation; pneumonia was cause of death Died of apnea during sleep on day 12
Died of apnea during sleep on day 31
Died suddenly 3 months after the stroke of an unknown cause; this was solely a unilateral stroke
after the stroke, and one died of sepsis from Pseudomonas pneumonia. Of the four who died, death occurred from 12 to 31 days after the stroke (mean, 21 days). Unilateral brainstem infarction has been reported to cause respiratory failure similar to Case I, and two of the three most recently reported cases ultimately achieved full recovery of spontaneous breathing (awake and asleep), 7 and 30 days after their strokes. However, the one with "recovery" on day 7 died from apnea on day 12. Persistent aventilation is wellrecognized to occur with bilateral lower brainstem and cervical spinal cord lesions as extensive as the infarction of Case 2, and the MRI identification of the extent of her infarction was predictive of her poor prognosis for recovery of spontaneous breathing. We conclude that: (a) cervicomedullary infarction is an important cause of prolonged aventilation; (b) the prognosis for respiratory recovery depends on the extent of the infarction and can be estimated with the assistance ofMRI studies; and (c) frequent assessment of spontaneous respiratory parameters optimizes potential for successful discontinuance of
RESPIRATORY FAILURE WITH CERVICOMEDULLARY INFARCTIONS
mechanical ventilation. Due to the separate anatomical control of automatic and voluntary breathing, successful weaning from a mechanical ventilator during wakefulness does not necessarily translate to effective breathing during sleep. Prolonged apnea monitoring, or continuous end-tidal carbon dioxide monitoring and pulse oximetry in those patients with continued endotracheal intubation or tracheostomy, is strongly recommended after "successful" weaning from mechanical ventilation.
References 1. Bogousslavsky J, Khurana R, Derauz JP, et al. Respiratory failure and unilateral caudal brainstem infarction. Ann Neurol1990;28:668-73.
2. Devereaux NM, Kean JR, Davis RL Automatic respiratory failure associated with infarction of the medulla. Arch Neurol1973;29:46-52. 3. Levin BE, Margolis G. Acute failure of automatic respirations secondary to unilateral brainstem infarct. Ann Neurol1977;1:583-6.
J STROKE CEREBROVASC DIS, VOL. 5, NO.2,
1995
65