Unusual pattern of somatosensory and brain-stem auditory evoked potentials after cardio-respiratory arrest

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Electroencephalograph)' and clinical Neurophysiology, 1985, 62:338-342

Elsevier Scientific Publishers Ireland, Ltd.

UNUSUAL P A T r E R N OF S O M A T O S E N S O R Y AND BRAIN-STEM AUDITORY EVOKED POTENTIALS AFTER CARDIO-RESPIRATORY ARREST E. B R U N K O *, F. DELECLUSE, A.G. HERBAUT, M. LEVIVIER and D. ZEGERS DE BEYL * Brain Research Unit, Brussels University, and Department of Neurology, Hbpital Erasme, BI070 Brussels (Belgium)

(Accepted for publication: April 3, 1985)

Summary Two patients in coma after cardio-pulmonary arrest showed bilateral absence of all brain-stem auditory evoked potentials contrasting with normal brain-stem reflexes and normal somatosensory cortical evoked potentials. In both patients pre-existing dysfunction of peripheral auditory structures could be ruled out. Subsequent neuropathological analysis showed that the anoxic-ischaemic lesions were restricted to Sommer's sector and the Purkinje cells. These unusual data suggest the hypothesis that a severe hypoxic-ischaemic insult may impair cochlear function and interfere with the activation of the intact auditory pathways.

Keywords: anoxic

coma - brain-stem auditory evoked potentials - somatosensorv evoked potentials

The combined use of brain-stem auditory evoked potentials (EPs) as a parameter of brainstem function and short-latency somatosensory EPs as a parameter of thalamo-cortical function has been shown useful in monitoring comatose patients (Starr 1976; Uziel and Denezeck 1978; Goldie et al. 1981). The somatosensory components are involved early in coma in contrast to brain-stem auditory EPs which originate from structures at pons and midbrain levels (Chiappa and Ropper 1982). Consequently, if EPs are abnormal in comatose patients most frequently the somatosensory cortical EPs are absent with normal auditory brain-stem EPs, or, if widespread brain lesions have occurred, both potentials are abnormal. The opposite situation, absence of brain-stem auditory EPs contrasting with normal somatosensory EPs has not yet been reported in studies dealing with monitoring of comatose patients. This situation suggests bilateral pre-existing damage of peripheral auditory structures such as pre-existing deafness, traumatic damage to both ears or ototoxic drug administration. Reprint requests: E. Brunko, Department of Neurology, HSpital Erasme, 808 Route de Lennik, B-1070 Brussels, Belgium.

In a recent prospective work dealing with a selected group of comatose patients shortly after cardio-respiratory arrest (Zegers de Beyl et al. 1984), two patients showed bilateral absence of all brain-stem auditory EPs, contrasting with normal somatosensory EPs. In both a careful history excluded the usual causes of pre-existing bilateral auditory lesions, raising the hypothesis of anoxic cochlear damage secondary to cardio-respiratory arrest.

Subjects and Methods Thirty-one patients with hypoxic-ischaemic brain injury after cardio-respiratory arrest were studied prospectively with serial clinical and electrophysiological examinations (Zegers de Beyl et al. 1984). Only two patients had bilateral absence of all brain-stem auditory EPs and normal somatosensory EPs and they are reported in detail. Brain-stem auditory EPs were evoked with monaural rarefaction clicks of 100/~sec at l l . 1 / s e c and an intensity of 85 dB and 95 dB HL. The bandpass was 150 H z - 3 kHz. Silver cup electrodes were applied to the earlobes referred to Cz with the ground electrode at Fz. A1-Cz and A2-Cz were

0168-5597/85/$03.30 © 1985 Elsevier Scientific Publishers Ireland, Ltd.

EPs IN ANOXIC COMA recorded simultaneously. At least two separate averages of 2000 clicks were superimposed. Somatosensory EPs were evoked by stimulating the median nerve at the wrist at minimal thumb twitch level at a rate of 3.1/sec. Bipolar records were made at the elbow and monopolar records at the spinous process of C6, the contralateral parietal and frontal scalp referred to linked earlobes. The bandpass was 5 Hz- 1.5 kHz. At least two separate trials of 512 stimuli were superimposed.

339 of the medulla oblongata, pons, midbrain, thalamus, frontal, parietal and temporal cortex showed no abnormalities other than loss of Purkinje cells and acute ischaemic necrosis of neurones in Sommer's sector (Fig. 2). Case 2 A 79-year-old man suddenly collapsed and had a cardio-respiratory arrest of an estimated 6 min duration. An electrocardiogram showed ventricular fibrillation. Neurological examination within 3 h after resuscitation showed coma with arm flex-

Results

Case 1 A 73-year-old woman was admitted for treatment of a major depressive episode. There was no history of hearing disorders or ototoxic drug administration. On admission general physical examination was unremarkable and hearing was normal to conversational speech. Shortly after admission, she choked during dinner and collapsed. Cardio-pulmonary resuscitation was initiated after a circulatory and respiratory arrest of an estimated 4 min duration. She did not respond to painful stimuli, pupils were large and did not react to light on arrival in the intensive care unit. On the next day, she reacted to pain by arm flexion, she had spontaneous roving eye movements and was breathing spontaneously at normal rate. Pupillary, corneal and oculocephalic reflexes were present. Ears were unobstructed. Stimulation of either ear with clicks of 85 dB or 95 dB HL elicited no response on several trials (Fig. 1). Muscle potentials were eliminated by paralysing agents and the continuous monitoring of the on-line non-averaged EEG showed no electrical interference. Short-latency somatosensory EPs to left median nerve stimulation showed a normal cortical response (Fig. 1). Neurological examination and somatosensory EPs remained unchanged over the next 3 days. Two recording sessions of brain-stem auditory EPs under optimal technical conditions 2 and 4 days after onset of coma confirmed the bilateral absence of evoked responses. She then developed puhnonary infection and died from cardiac arrhythmia 5 days after cardio-pulmonary resuscitation. Detailed pathological examination

Click A .~q~

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I 1

I 2

I 3

I 4

I 5

I 6

I 7

I

I 30

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Stim. C ~

D

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E

I 0

I 10

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I 20

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Fig. l. Brain-stem auditory (A. B) and somatosensory(C-F) evoked potentials in case 1. Superimposed averages at AI-Cz on left (A) and at A2-Cz on right (B) ear stimulation. Early cortical EPs (arrows) recording at frontal (C) and parietal (D) scalp, neck at C6 (E) referred to linked earlobes and elbow (F) (bipolar). Calibration: 0.15 ~V (A, B): 1.25 ~V (C~ D, E) and 10 ~V (F).

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E. B R U N K O ET AL.

ion to painful stimuli, spontaneous regular breathing, normal pupillary, corneal and oculocaloric reflexes. Ears were unobstructed and hearing level was known to be previously normal to conversational speech. There was no history of hearing disorders or recent ototoxic drug administration. Brain-stem auditory EPs to clicks of 85 dB and 95 dB H L were absent despite several trials, use of paralysing agents and optimal technical conditions. Short-latency somatosensory EPs to right and left median nerve stimulation showed normal cortical responses. Two recording sessions of brain-stem auditory EPs 2 and 8 days after admission confirmed bilateral absence of evoked responses. On the fifth day he opened his eyes spontaneously and showed orientating eye movements. Two months later he was able to grasp objects and to mutter occasional inappropriate words. He died from recurrent cardiac arrhythmia. Neuropathological examination showed loss of Purkinje cells and of neurones in Sommer's sector. Brain-stem sections at different levels, thalamus and cortex were otherwise normal.

Discussion

Fig. 2. Neuropathological data of case 1. A: intact parietal cortex. Haematoxylin-eosin staining. × 300. B: A m m o n ' s horn. Abrupt loss of neurones in Sommer's sector (arrow). Haematoxylin-eosin staining. C: intact section at the Junction of pons and midbrain. Luxol Fast Blue counterstained by neutral red.

Brain-stem auditory EPs as a parameter of brain-stem function in comatose patients must be evaluated in the context of the patients' clinical examination. It has been emphazised that the absence of all brain-stem auditory EPs including wave ! provides no information about the function of the brain-stem as no inferences can be made about the activation of the central auditory pathways (Starr 1976; Uziel and Denezeck 1978; Goldie et al. 1981). Nevertheless it has been shown that comatose patients with bilateral absence of all brain-stem auditory EPs usually satisfy the criteria of brain death and die (Starr 1976; Goldie et al. 1981). However, these studies dealt with coma regardless of the aetiology. In fact, in traumatic coma, bilateral absence of all brain-stem auditory EPs may occur even if there is evidence of some preserved brain-stem and other cerebral functions because of bilateral traumatic damage of peripheral auditory structures.

EPs 1N ANOXIC COMA

On the other hand, in patients with non-traumatic coma, if no brain-stem auditory EPs can be elicited bilaterally, the clinical situation suggests either brain death or severe pre-existing deafness. As absence of all brain-stem auditory EPs implies hearing loss greater than 75 dB, a severe social handicap, the suspicion of pre-existing deafness can usually be confirmed by the patients' relatives. Thus when pre-existing or traumatic damage can be ruled out, the recording of somatosensory EPs in patients with bilateral absence of brain-stem auditory EPs usually shows no activity above the lower medulla, confirming widespread brain-stem damage (Goldie et al. 1981). The absence of brain-stem auditory EPs in our patients contrasted with their neurological examination and the presence of normal short-latency somatosensory EPs. The presence of spontaneous regular breathing, pupillary, corneal and oculocephalic reflexes indicated normal brain-stem function. Also, normal somatosensory EPs ruled out anoxic-ischaemic damage of the somatosensory pathways in brain-stem, thalamus and cortex. Pre-existing damage of peripheral auditory structures had to be ruled out. The normal hearing level to conversational speech up to a few hours prior to the anoxic insult excluded severe deafness, otoscopy showed no obstruction and history excluded traumatic damage of the ears. Ischaemic damage of the eighth nerve, secondary to the anoxic-ischaemic insult, is very unlikely since no evidence of ischaemic brain-stem damage was seen on detailed neuropathological analysis. Unfortunately the cochlea was not available for pathological analysis and consequently there is no confirmation of possible cochlear ischaemic anoxic dysfunction. The cochlea is known to be affected by hypoxia (Pierson and MC~ller 1982) and in animals hypoxia severe enough to impair the systemic circulation suppresses brain-stem auditory EPs including wave I (Sohmer et al. 1982). As cardio-respiratory arrest was the only major event between the moment when audition was normal to conversational speech and the moment of recording EPs, we suppose that cochlear function was impaired by this prolonged anoxia. This hypothesis, however, remains speculative without pathological data.

341

To our knowledge the bilateral absence of brain-stem auditory EPs without pre-existing hearing loss and with normal early cortical somatosensory EPs is a unique combination not reported in previous studies dealing with non-traumatic coma. The usual well known picture is one of absence of all brain-stem auditory EPs and no activation of the somatosensory pathways above the medulla. In our patients the absence of all brain-stem auditory EPs could not be due to widespread damage of the brain-stem in view of the clinical findings. When, however, clinical evaluation of brain-stem reflexes is unreliable because of coexisting hypothermia or drug intoxication, wrong conclusions might be drawn from the loss of brain-stem auditory EPs. Our report emphasizes that, if electrophysiological data are recorded to evaluate the extent of anoxic-ischaemic lesions after cardio-pulmonary arrest, brain-stem auditory and somatosensory EPs should be recorded. As the somatosensory pathway can be monitored throughout the peripheral and central nervous system, erroneous conclusions due to lesions of the peripheral receptor organs are unlikely with this multimodal approach. Finally, the hypothesis that hypoxic-ischaemic cochlear damage might interfere with the activation of auditory pathways after cardio-pulmonary resuscitation has to be tested in further studies.

R~sum~

Configuration inhabituelle des potentiels bvoquks somatosensoriels et auditifs du tronc cbrbbral aprbs arr~t cardio-respiratoire Deux patients en coma h la suite d'un arrEt cardio-respiratoire pr6sentaient une absence bilat6rale de routes les ondes des potentiels 6voqu6s acoustiques du tronc c6r6bral. I1 y avait un net contraste entre l'absence des potentiels acoustiques et l'6valuation clinique montrant des r6flexes du tronc normaux. De plus, les potentiels 6voqu6s somesth6siques pr6coces 6taient normaux. Une surdit6 ou des 16sions acoustiques p6riph6riques pr6existantes ont pu Etre exclues. La neuropathologie confirmait des 16sions anoxiques-

342 i s c h 6 m i q u e s r e s t r e i n t e s au s e c t e u r de S o m m e r et a u x cellules de P u r k i n j e . C e t e n s e m b l e de d o n n 6 e s i n h a b i t u e l l e s sugg6re l ' h y p o t h 6 s e q u ' u n 6 p i s o d e a n o x i q u e aigu p o u r r a i t 16ser la c o c h l 6 e et ainsi e m p 6 c h e r l ' a c t i v a t i o n des s t r u c t u r e s a c o u s t i q u e s c e n t r a l e s intactes.

References Chiappa, K.H. and Ropper, A.H. Evoked potentials in clinical medicine. New Engl. J. Med., 1982, 306: 1205-1211. Goldie, W.D., Chiappa, K.H., Young, R.R. and Brooks, E.B. Brain-stem auditory and short-latency somatosensory evoked responses in brain death. Neurology (NY), 1981, 31: 248-256.

E. BRUNKO ET AL. Pierson, M.G. and M¢ller, A.R. Corresponding effects of hypoxia on the cochlear microphonic and the compound action potential. Hear. Res., 1982, 6: 83-101. Sohmer, H., Gafni, M. and Ghisin, R. Auditory nerve-brainstern potentials in man and cat under hypoxic and hypercapnic conditions. Electroenceph. clin. Neurophysiol., 1982, 53: 506-512. Starr, A. Auditory brain-stem responses in brain death. Brain, 1976, 99: 543-554, Uziel, A. and Denezeck, J. Auditory brain-stem responses in comatose patients: relationship with brain-stem reflexes and levels of coma. Electroenceph. clin. Neurophysiol., 1978, 45: 515-524. Zegers de Beyl, D., Borenstein, S., Dufaye, P. and Brunko, E. Irreversible cortical damage in acute postanoxic coma: predictive value of somatosensory evoked potentials. Transplant. Proc.. 1984, 16: 98-101.