INTRODUCTION

The brainstem commands most of the vital functions in our body (blood pressure, heart beat, body temperature, etc.), being responsible for the most primitive reflexes, such as cornea, pupil, pharynx, tendon and plantar reflexes 1.

The collapse of the brainstem function requires documentation of absence of pupil reflex to light, cornea, oculoencephalic, oculovestibular, oropharyngeal and respiratory reflexes. In some situations, such as when the patient is under the effect of high central nervous system (CNS) depressing drugs or induced deep hypothermia, there are no reliable tests that can access the functional integrity of the brainstem 2.

ABR (auditory brainstem response) is a competent instrument to monitor brainstem function. The ascending auditory pathways, owing to their complexity and phylogenetic origin, have numerous connections in the CNS as part of the complex reflex auditory system. Thus, decussation and inter-nuclear communication make the auditory pathways to occupy or be represented in the segments of the brainstem (pons and midbrain) 3.

ABR is an objective method to measure the electrophysiological potential of the brainstem and it is practically resistant to moderate hypothermia (temperatures higher than 30o C), high doses of barbiturics and other CNS depressors 4-6. ABR is a relatively simple and reliable alternative to assess the neurophysiological integrity of the brainstem. Starr used it for the first time in the 70's to diagnose brain death 7. The method has proved to be very useful in staging coma and its implications in the diagnosis of brain death 8-10. ABR sums up a series of advantages including its non-invasive character, its very low morbidity and reliability and reproducibility even in electrically charged environments, such as operating rooms and intensive care units (ICU) 11, 12.

Deep hypothermia and total circulatory arrest (TCA) are techniques sometimes used for surgical treatment of patients with thoracic aorta aneurysm, since we can have temporary absence of heart beat and blood circulation, promoting the appropriate surgical fields for the correction of the aneurysms. In these procedures, the patients are submitted to a process of body cooling up to reaching 18o C. At this temperature, there is TCA that can last up to 1 hour, the necessary time for the surgeon to perform the correction of the aneurysm in ideal conditions.

Deep hypothermia aims at protecting the CNS from deleterious effects of a period of anoxia that occurs during TCA when cerebral perfusion is interrupted 13, 14.

Some studies reported the effects of deep hypothermia and TCA over ABR. Through the analysis of tracings during the cooling period (increase in latency and interpeak intervals and reduction of wave amplitude) and body reheating (recovery of tracing patterns similar to pre-cooling situation), it was shown that ABR is a useful instrument to assess the brainstem function during these surgical procedures 15-22.

Since ABR depicts the electrophysiological conditions of the brainstem auditory pathways and the normal pattern represents neurophysiological integrity of the brainstem, we decided to monitor the brainstem function during the surgical procedures, by analyzing the ABR to assess whether anoxia of the patients submitted to the TCA would have caused damage to the CNS, more precisely to the brainstem.
The authors make a correlation between the ABR obtained in these patients during the maximum cooling period (18o C) and TCA, whose tracing showed isoelectrical patterns, with ABRs that also presented isoelectrical patterns in patients in coma from the study conducted by Sousa et al. 8, comparing the prognosis of those two groups of patients.

OBJECTIVE

To monitor the brainstem function through the analysis of ABR tracings during heart surgery with deep hypothermia and total circulatory arrest so as to provide objective data to the team of surgeons, anesthesiologists and intensivists about functional recovery of the brainstem.

MATERIAL AND METHOD

This study was based on the analysis of tracings of ABR in 8 adult patients, 5 male and 3 female subjects, being the youngest 52 years and the oldest 67 years, submitted to surgery with deep hypothermia and TCA. The tracings were recorded in the cooling period, during TCA and started when the temperature reached 18o C and during the body reheating period.

We recorded ABR of 20 normal subjects from the first to the ninth decades of life, in the medical office using a portable unit of recording to brainstem auditory potentials, brand Grason Stadler, model GSI 55 ABR Screener. The same patients were reexamined but this time using an evoked potential device brand Amplaid, model MK-10 Multisensory System, comparing to the morphology of tracings obtained, latency and wave amplitude. We did not detect differences between the performed exams in the two devices.

Next, we checked the reliability and reproducibility of GSI 55 in the hospital setting (operating rooms, heart surgery room), comparing the ABR in 5 young adult subjects from the previous group in the office with those conducted in the operating room under normal conditions of monitoring of the heart surgery room (oxymeter, thermometer, EGC, etc.). We did find any differences between the exams conducted in the office and in the operating room.

Interferences caused by static power (background noise) were identified through observation of the base line, without deflagration of auditory stimuli, and the exam was conducted only after the temporary suppression of the noise source.

The exams were performed by the author, using a portable unit of brainstem evoked potentials, brand Grason Stadler, model GSI 55 ABR Screener, with averager of one channel and two memories, with analysis time window of 12 msec and repetition rate of 10Hz. Stimuli were brief clicks (100 msec) with alternate polarity and 85dB HL intensity, presented to one ear, through insertion phones, amounting to a total of 1,024 stimuli. We recorded two tracings in each ear in the available memories, making wave overlapping so as to demonstrate consistency and reproducibility of tracing. The device was powered by batteries, reducing the possibility of interferences caused by background electrical noise.

Surface electrodes were applied after soft skin scarification with gauze soaked in ether, using a lotion brand Med-TraceT (Buffalo, New York, USA), and fixed with MicroporeT.

The tracings were obtained obeying the classical pattern: (a) hairline (Fpz+); (b) earlobe on the tested ear (negative) and (c) earlobe on the contralateral ear (grounding).

ABR tracings were recorded in the following steps: before the beginning of hypothermia (35oC), during the cooling process (32 to 26oC), during the TCA (18o C), and during heating process (27o C) up to the initial temperature (35o C).

Patients were carefully cooled. It took approximately 1 hour to reach the body temperature of 18o C, measured through esophageal thermometer. At this moment, the total circulatory arrest started and it could last as long as 1 hour. Next, the process of reheating the patient started, which lasted for another 1 hour.

The technique of extrabody circulation was used (device Macchi model BM-6 and adult membrane oxygenators brand Macchi-OXIM II-34 and Brailer-MRX-Biomédica). The blood was bombed to the oxygenator and cooled or heated by the thermo-exchanger through which there was circulating cold or hot water. A plastic bag with ice was placed over the heads of the patients to help the cooling process.

RESULTS

We studied the behavior of the ABR tracings in 8 patients submitted to surgery to repair a thoracic aorta aneurysm, with deep hypothermia and total circulatory arrest.

The initial tracings (35o C) were within the normal range (morphology, synchrony, latency of waves I, III and V). When body temperature reached 26o C, there were signals of electrical activity in the tracing and disappearance of the ABR waves. During the maximum cooling period (18o C) and total circulatory arrest, ABR tracing showed an isoelectrical pattern.

In the process of reheating, when body temperature reached 27o C, we observed recovery of waves I, III and V with increase latencies and prolonged interpeak intervals. Waves III and V were later than wave I. As of 35o C, absolute values of wave latency came close to the initial tracing.

In Table 1 we can observe the behavior of the tracings of ABR in the many phases that comprised the cooling process (Phases A, B and C), total circulatory arrest when we reached the minimum temperature of 18o C (phase D) and body reheating (phases E and F). In phase A (35o C), ABR was normal, in phase B (32o C) we observed mild tracing irregularity, with preserved wave synchrony, in phase C (26o C), we detected absence of wave and only electrical activity present; in phase D (18o C), the tracing was isoelectrical, in phase E (27o C) we observed recovery of all waves, with increase in latencies, and in phase F (35o C), we observed complete recovery of ABR waves.

Of the 8 studied cases, one died after the surgical procedure, still in the operating room, and 7 went to the ICU (early postoperative period) in good clinical conditions.

Next, we present two clinical cases that had completely different evolutions. The first case died by the end of the heating process as a result of surgical complications and blood coagulation; the second one was discharged from the ICU in good clinical conditions.

Patient 1: ARG, 62-year-old female patient. Surgical treatment to repair a dissecating aneurysm of the thoracic aorta. At the end of the surgical procedures, she presented hemorrhage in the anastomosis, which led to hypovolemic chock and cardio-respiratory arrest. In the occasion, the body temperature was 35o C, and ABR that had already presented complete recovery of normal pattern, started to degenerate (Table 1 - phases F and G). The last record occurred one minute after the cardio-respiratory arrest (in electrical activity, without pulse). At that time, ABR was isoelectrical (Phase H).

It is important to note the 2 different electrophysiological moments of the brainstem, both in body temperature of 35o C. In the first moment, with cardio-respiratory stability, ABR is normal; in the second one, in severe hypovolemic status and electrical activity without pulse, we can clearly see the impairment of synchrony of tracing as well as increase in latency of waves (Phase G). Phase H shows the isoelectrical tracing that was recorded one minute after the cardio-respiratory arrest (asystole).

Patient 2: MSL, 56-year-old male patient. Surgical treatment for the repair of dissecating aneurysm of thoracic aorta. The surgical procedure was uneventful. We observed complete recovery of latency and morphology of the tracings at the end of body heating (Table 1 - phase F). The patient was discharged from ICU in good clinical conditions.





DISCUSSION

ABR has proved to be a useful instrument in detecting different types of diseases that affect the central nervous system. In past years, working together with intensivists, neurologists and neurosurgeons, the authors acquired experience using ABR as the method of assessment of the brainstem function 8, 9, 23.

The literature is extensive in reporting extreme use of ABR as a non-invasive, reliable, and objective method, in the follow up of the variations of electrophysiological patterns of the brainstem. This method has been employed in monitoring the coma status and prognosis of brain death since 1976 7.

ABR is a competent instrument for the monitoring of the brainstem function since the ascending airways pathways occupy all the segments of the noble structure of the central nervous system, responsible for the vital functions of our body. Its functional collapse is synonym of brain death.

The assessment of neurophysiological integrity of the brainstem through ABR follows an electrophysiological reasoning, which is based fundamentally on the assessment of the neural element synchrony (peripheral and brainstem auditory pathways). In normal subjects, it is observed that there is an overlapping of tracings of both memories. The deflections are identical to the baseline without temporal discrepancies between waves I, III and V.

We believe that the tracing pattern of ABR, taking into account elements such as morphology, synchrony, wave latency and interpeak intervals, pictures the neurophysiological integrity of the brainstem. Reproducibility of the wave pattern is the most marked quality of ABR, found in the morphology of tracing, in wave latency and in interpeak intervals, exceptionally reliable indexes.

Some studies have demonstrated a behavior of tracings of ABR in surgeries with deep hypothermia and total circulatory arrest. During the cooling process, there is increase in latency of waves I, III and V and interpeak intervals. When body temperature reaches 25o C, all waves disappear. Wave V starts to reappear during the reheating process also at 25o C, reestablishing a normal tracing pattern of 34o C 15. According to Markand et al, ABR waves are present in temperatures above 23o C and absent below 20 o C. With reheating, the abnormalities revert and retrieve pre-hypothermia levels 17. Similar results were obtained by Rodrigues, Rosenblum and Hayashi.[18-20]. Electroencephalogram activity is absent between brain temperatures of 19 to 26o C 24.

Our results obtained in the behavior analysis of ABR were similar to those reported by the literature. During the process of body reheating, when the temperature reached 27o C, we observed resurge of the ABR waves with increased latencies and prolonged interpeak intervals, especially owing to delay in waves III and V. The increased latency of waves III and V was greater than observed in wave I, when compared with the baseline tracing of patients (35o C). Hayashi et al. demonstrated that wave I is the first to resurge in the reheating period (24o C) 20. The analysis of the behavior of wave latencies makes us believe that reheating of auditory pathways is processed from the periphery to CNS. The cochlea and the 8th nerve (wave I) resume their functions before the central pathways, in the pons (wave III) and midbrain (wave V).

In the cooling period there seems to be the opposite, the rostro-caudal process, that is, first it cools (depresses) the midbrain, then the pons and lastly, the 8th nerve and the cochlea. Hayashi et al. registered only the presence of wave I during body cooling of 22o C, in 6 of the 22 patients submitted to deep hypothermia and TCA 20.

The proposition of our study was to conduct electrophysiological monitoring of brainstem (ABR) during heart surgery with deep hypothermia and TCA, whose main purpose was to detect recovery of initial patterns of ABR tracing during reheating process, showing the resume of functional normal status of the brainstem (Table 1), which allows to inform the surgical team of the success of the procedures to protect the central nervous system by cooling the body. We assessed whether the central nervous system suffered any damage resultant from the period of anoxia caused by absence of perfusion to which it was submitted.

In a recent study, Sousa et al. analyzed the tracing of ABR in 100 patients in coma. Among the 100 studied patients, 64 presented tracings with isoelectrical pattern and they had score 3 in Glasgow scale (absence of verbal or motor response, ocular opening). All the 64 patients whose ABR tracings were isoelectrical progressed to death. The isoelectrical tracing in ABR proved to be an efficient support in the decision of predicting death in the ICU (brain death) 8.

The choice of body temperatures in which the tracings were made, especially the ones in the reheating period, were based on the fact that what mattered to us was not the detection of the start of the waves (real instant of resurge), but rather whether they would resurge or not. We decided to choose the body temperature 28o C to that end, since this temperature, in the literature, is reported to be the one in which all waves should have already resurged. If ABR waves do not reappear, that is, if the isoelectrical pattern is maintained after body reheating, this fact would be related to severe brainstem damage.

Our main concern was the period of body reheating, when the tracing changed from isoelectrical pattern (18o C) to normal range (35o C). Out attention was directed to this period that we considered essential. In this phase of reheating, we could observe the restoration of the brainstem function, the recovery of the electrophysiological integrity. We believe that the maintenance of the isoelectrical pattern of ABR during body reheating period could be clinically translated into irreversible ischemic lesions of the brainstem.

After completing the reheating phase, the patient persisted under the effect of high doses of CNS depressing drugs. The anesthesiologists and intensivists do not have, however, how to clinically access the functional integrity of the brainstem. The parameter we proposed to this end is the reappearance of ABR waves after body reheating process.

Katbamna et al. recorded ABR abnormalities of Marmota monax and confirmed that auditory brainstem potentials disappeared when low body temperature was reached during the hibernation period and reappeared when they woke up, when the body temperate reached normal levels 25.

The definition of an isoelectrical tracing in normal body temperatures in patients in coma, as reported by Sousa et al., is related with brain death 8, 9. The same pattern of tracing during deep hypothermia period is related to a status of induced hibernation of the CNS, when the metabolism of the nervous cell reaches very low levels, becoming exempt from harmful effects of prolonged anoxia during the period of total circulatory arrest.

Norwood et al. demonstrated that the stocks of adenosine triphosphate (ATF) and phosphocreatinine are not consumed during deep hypothermia and TCA 13. Hypothermia is the primary component of central nervous system protection, increasing considerably the brain tolerance to ischemia during the TCA period 14.

We believe that ABR is a competent instrument to detect occasional impairments of brainstem functional integrity as a result of periods of ischemia during heart surgeries with deep hypothermia and TCA.

CONCLUSION

ABR is a competent instrument in monitoring functional integrity of the brainstem in heart surgeries with deep hypothermia and TCA.

Waves I, III and V disappear during body cooling period, the tracing reaches isoelectrical pattern at 18o C and the waves resurge during the reheating process.

After the end of the period of total circulatory arrest and body reheating, the anesthesiologists and intensivists do not have any reliable clinical measures to access brainstem functional integrity. ABR is a non-invasive, reliable and objective method to deal with this issue. The resurge of ABR waves after body reheating is our parameter to assess the restoration of brainstem function.

The maintenance of an isoelectrical pattern after body reheating can be translated into severe impairment of the functional integrity of the brainstem, as a result of the ischemia period during heart surgeries with deep hypothermia and TCA.

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1Associação Paparella de Otorrinolaringologia, Hospital Santa Lydia, Ribeirão Preto.
2Professor of Otorhinolaryngology, Medical School, University of Ribeirão Preto (UNAERP).
3Medical Director, Intensive Care Unit, Hospital São Francisco de Ribeirão Preto.
4Trainee, Service of Otorhinolaryngology, Hospital Santa Lydia.
Address correspondence to: Luiz Carlos Alves de Sousa - Rua Bernardino de Campos, 1503 - Ribeirão Preto, SP 14015-130 - Tel/Fax: 016-610-6755 - 610-6515
E-mail: lcarlos@clinicapaparella.com.br
Study presented as Free Communication at II Congresso Triológico de ORL, Goiânia, August 26, 2001.
This study was supported by Associação Paparella de Otorrinolaringologia, Hospital Santa Lydia de Ribeirão Preto.
Article submitted on June 26, 2003. Article accepted on August 20, 2003.