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Ann Thorac Surg 1999;67:1915-1918
© 1999 The Society of Thoracic Surgeons

Retrospective study of somatosensory evoked potential monitoring in deep hypothermic circulatory arrest

Sophie Ghariani, MDa, Laura Liard, PhDa, Joachim Spaey, PhDa, Philippe H. Noirhomme, MDa, Gebrine A. El Khoury, MDa, Mariane de Tourtchaninoff, MDa, Robert A. Dion, MDa, Jean-Michel Guerit, MD, PhDa

a Cliniques Universitaires Saint-Luc, UCL Brussels, Brussels, Belgium

Address reprint requests to Dr Guerit, Service Potentials Evoques, Cliniques Universitaires Saint-Luc, Ave Hippocrate, 10, B-1200 Brussels, Belgium
e-mail: guerit{at}nchm.ucl.ac.be

Presented at the Aortic Surgery Symposium VI, April 30–May 1, 1998, New York, NY.


    Abstract
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 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Background. We evaluated the efficiency of median-nerve somatosensory evoked potentials (SEPs) monitoring in determining the optimal level of hypothermia in 62 consecutive patients operated on under deep hypothermic circulatory arrest (CA).

Methods. CA was started at 1°C below the temperature at which both brainstem and cortical SEP components disappear. No additional method of cerebral protection was used.

Results. New neurological complications were observed in 15 patients: long-lasting in 11 and transient in 4. A retrospective analysis of SEP monitoring identified the origin of the complications in 12 cases: early CA with incomplete cooling due to emergency (3 cases); inefficient retrograde perfusion through the femoral artery during cooling due to the dissection flap effect (4 cases); embolism during rewarming (2 cases); delayed embolism (2 cases); hemorrhagic shock (1 case). In 2 cases, neurological sequelae involved the lower limbs (extracerebral origin). One case without intraoperative SEP changes was neurologically abnormal preoperatively and did not change postoperatively. There were no cases with sequelae due to excessive CA duration.

Conclusions. The use of SEP monitoring to determine the optimal level of hypothermia efficiently prevents neurological sequelae of CA. It helps in monitoring the degree of cerebral protection during cooling (flap effect), and rewarming.


    Introduction
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 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Besides its impact on ongoing operations, SEP monitoring also helps improve surgical strategy in subsequent operations. Indeed, the retrospective analysis of SEP data and their correlation with intraoperative events do help in understanding the pathophysiology of neurological complications and therefore in developing surgical strategies aimed at preventing them [1]. This paper presents a retrospective analysis of the neurological outcome in a series of 62 patients who underwent surgery under deep hypothermic circulatory arrest (CA).


    Patients and methods
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 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Median nerve SEP monitoring was performed in 62 patients (mean age 55.4 years) operated on under deep hypothermic CA. The mean nasopharyngeal temperature at the time of arrest was 14.6°C (range 10.2–20°), the mean CA duration was 44.3 minutes (range 2–98). Forty patients (64.5%) were operated on as emergencies.

Our SEP techniques have been described previously [2]. Briefly, SEPs were obtained immediately after induction of anesthesia by alternative electrical stimulation (3.1 Hz; 200 µsec duration, constant voltage, 20 to 39 mAmp intensity) of both median nerves at the wrist. These signals were analyzed on 4 channels: C6 spinous process, C’3 and C’4 (2 cm behind C3 and C4), and Fpz with a common linked-ear reference. The analysis time was 100 ms, band-pass from 5 to 1500 Hz. Examples of recordings obtained after induction and during the cooling process are shown in Figure 1.



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Fig 1. Example of SEPs obtained at relative normothermia (upper curves, nasopharyngeal temperature 34.2°C) and during the cooling process. Two peaks are considered in this figure: the N20 generated in the parietal cortex, and the brainstem P14, best evidenced in frontal recordings. Cooling causes a progressive increase in all peak latencies, followed by the successive disappearance of cortical activity (N20 disappears between 22.7 and 20.7°C and brainstem activity, P14, disappears between 78.0 and 75.7°C). CA is performed at 1°C below the temperature at which P14 disappears.

 
After midline sternotomy, extracorporeal circulation was instituted by cannulating the right common femoral artery and the right atrium. Rapid cooling was initiated. CA was started at 1°C below the temperature at which both brainstem and cortical SEP components disappeared [2]. No additional methods of cerebral protection were used.


    Results
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 Abstract
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 Patients and methods
 Results
 Discussion
 References
 
Six patients died intraoperatively from non-neurological causes. One of these demonstrated SEP loss during rewarming by means of retrograde perfusion before dying from intraoperative bleeding. Two patients died 20 and 73 days postoperatively from multiorgan failure, and 3 died postoperatively after having had neurological complications: one of these was neurologically abnormal preoperatively. Amongst the long-term survivors, 11 hadneurological complications, long-lasting in 7 and transient in 4. Thus, neurological problems occurred in 15 patients (24.2%): 1 patient who died intraoperatively, 3 patients who died postoperatively, and, among the long-term survivors, 7 with long-lasting sequelae, and 4 with transient problems. These 15 patients constitute the core of this retrospective study. Their main clinical features are summarized in Table 1.


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Table 1. Clinical Features, CA Duration and Temperature, Neurological Sequelae, and Distribution of Intraoperative SEP Alterations

 
Retrospective analysis of intraoperative SEP alterations
Five types of neurological complications were defined on the basis of SEP evolution as a function of body temperature and its relationship to intraoperative events:

Type 1 alterations correspond to brain hypoperfusion due to circulatory failure before the initiation of retrograde perfusion. These alterations were observed in 3 patients (2 due to ventricular fibrillation, and 1 after rupture of the aneurysm). These Type 1 alterations consisted of the sudden disappearance of cortical SEPs. Retrograde perfusion was immediately instituted and cooling accelerated. Transient neurological sequelae were observed in 2 patients (13 and 14), and 1 patient (5) had long-lasting lateral hemianopia.

Type 2 alterations reflect a "flap effect" or malperfusion due to the entry into the false lumen of blood being perfused retrograde, with compromise of cerebral perfusion as a consequence of exclusion of the supraaortic vessels from the perfused false channel. Four patients manifested this complication, associated with brisk disappearance of cortical SEPs. One patient died during surgery (1), 2 patients had long-lasting complications (9 and 11) and 1 patient had transient complications (delayed recovery, 12).

Type 3 alterations correspond to embolism during rewarming. SEP recordings were normal during cooling and reappeared normally at the beginning of the rewarming procedure, but then suddenly disappeared later. Type 3 alterations were observed in 2 patients: one died and one manifested long-lasting neurological sequelae.

Type 4 alterations correspond to post-operative complications. SEPs remained normal throughout the whole procedure but deteriorated on the day after surgery. Type 4 alterations were observed in 3 patients, 2 due to embolism (3 and 10) and one to hemodynamic events (4).

Three patients with neurological complications did not manifest any SEP worsening: the neurological deficit was already present preoperatively in 1 (4) and consisted of a new paraplegia in 2 (8 and 15). In these last 2 patients, only SEP recording after posterior tibial nerve stimulation could have revealed these abnormalities during surgery.

The mean CA duration was 46.5 minutes (2 to 98) in the patients who did not have neurological sequelae and 38.8 minutes (2 to 80) in the patients with neurological sequelae. It is noteworthy that there were no patients in whom neurological sequelae were due to too long an interval of CA.


    Discussion
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 
Three arguments justify the need for individual adjustment of CA temperature: the fact that the nasopharyngeal temperature does not necessarily reflect brain temperature; that individual brain susceptibility to hypothermia is a function of basal brain metabolism, pH, blood gases, and glucose level [3]; and the fact that too deep a level of cooling is also likely to be prejudicial [38]. Our strategy, which consists of determining the optimal level of hypothermia on the basis of subcortical SEP disappearance [2], appears to be efficient since there were no patients in whom neurological complications appeared as a consequence of too long an interval of CA.

Our monitoring technique appears both extremely sensitive and specific. On the one hand, there were no patients developing immediate new neurological sequelae despite unaltered intraoperative SEPs (with the exception of 2 paraplegias that could not be forecast on the basis of median nerve SEPs). On the other hand, a definite explanation was found in all patients in whom intraoperative SEP alterations occurred, and all these patients eventually developed at least transient neurological sequelae.

Two mechanisms are traditionally proposed to explain the neurological sequelae of cardiovascular surgery: hemodynamic events and embolism [913]. Our study demonstrates that both mechanisms can play a role. Hemodynamic events are more likely to occur during the first stage of the operation, either before (type 1) or during (type 2) retrograde perfusion. In contrast, the risk of embolic events is higher after recirculation (type 3) and even after operation (type 4). Two patients became paraplegic, which could not be forecast on the basis of median serve SEPs. This raises the issue of the desirability of combining posterior tibial nerve with median nerve SEP monitoring.

The value of SEP monitoring is not limited to its role in determining the optimal level of hypothermia; SEP monitoring is also useful in evaluating other hemodynamic events occurring during the procedure. This is reflected by type 1 and type 2 alterations. The rapid SEP deterioration observed before institution of retrograde perfusion allowed us immediately to speed cooling in the 3 patients in whom these type 1 alterations were observed. It is worth noting that 2 of these 3 patients only manifested transient neurological sequelae, and that the long-lasting sequela observed in the third patient was limited to a lateral hemianopia.

Type 2 alterations deserve more comments since they illustrate the possible dual impact of SEP monitoring [1]: modification of current surgical strategy and improvement of subsequent procedures. Type 2 alterations reflect what we call the "flap effect." In aortic dissection, the dissociation between the intima and the media creates a false lumen extending toward the descending aorta, which is separated from the true lumen by an intimal septum. Usually there are several fenestrations in this intimal septum, acting as re-entry sites. During cooling and retrograde perfusion through the common femoral artery, these fenestrations may allow filling of the false lumen, and the intimal septum may then occlude the true lumen, leading to malperfusion of the upper thoracic aorta and of the supraaortic vessels, and to potentially severe cerebral hypoperfusion. In the absence of monitoring, this harmful complication may remain unrecognized for some time, resulting in severe brain ischemia. In the first of our patients in whom this complication occurred (case 1, who died intraoperatively), we failed to identify the exact origin of the SEP alterations intraoperatively, but a retrospective analysis clearly disclosed the arrest of P14 latency changes as a function of body temperature, which argued in favor of a hemodynamic problem and led us to suspect the flap effect. This made us aware of the possibility of malperfusion in subsequent operations, and accordingly led us to develop new strategies, including initiation of antegrade perfusion in emergencies. It should be noted that 2 of the 3 subsequent patients in whom this effect was found (cases 11 and 12) only developed transient neurological sequelae.

Finally, 3 patients developed delayed complications, 2 due to embolism and 1 to hemodynamic disturbances. These complications are not specific for ascending aorta surgery (for instance, late hemodynamic compromise accounts for about 50% of delayed paraplegia in descending aorta surgery [14]) and should not be considered as a false negative of the technique. They suggest the desirability of prolonging neuromonitoring into the postoperative period.

Our technique of SEP monitoring has proven useful in determining the optimal temperature of CA since there were no neurological complications due only to CA duration. The technique appeared very sensitive, since there were no patients who manifested new neurological complications (except paraplegia) despite unchanged intraoperative SEPs. It also appeared very specific, since all intraoperative SEP alterations could be explained, and all were associated with transient or long-term neurological sequelae. Finally, the impact of SEP monitoring was not limited to concurrent operations, but also contributed to improvement of subsequent surgical strategy.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 References
 

  1. De Mol B., Hamerlijnck R., Boezman E., Vermeulen F.E.E. Prevention of spinal cord ischemia in surgery of thoraco-abdominal aneurysm: the Biomedicus pump, the recording of somatosensory evoked potentials and the impact on surgical strategy. Eur J Cardiothorac Surg 1990;4:658-664.[Abstract]
  2. Guerit J.M., Verhelst R., Rubay J., et al. The use of somatosensory evoked potentials to determine the optimal degree of hypothermia during circulatory arrest. J Card Surg 1994;9:596-603.[Medline]
  3. Davis L.K. Hypothermia: physiology and clinical use. In: Gravlee G.P., Davis R.F., eds. Cardiopulmonary bypass: principles and practice. Baltimore: Utley, Williams & Wilkins, 1993:40.
  4. Wood M., Shand D.G., Wood A.J. The sympathetic response to profound hypothermia and circulatory arrest in infants. Can Anaesth Soc J 1980;27:124-132.
  5. Greeley W.J., Ungerleider R.M., Smith L.R., et al. The effects of deep hypothermic cardiopulmonary bypass and total circulatory arrest on blood flow in infants and children. J Thorac Cardiovasc Surg 1989;97:737-745.[Abstract]
  6. Svensson L.G., Crawford E.S., Hess K.R., et al. Deep hypothermia with circulatory arrest: determinants of stroke and early mortality in 656 patients. J Thorac Cardiovasc Surg 1993;106:19-31.[Abstract]
  7. Crawford E.S., Svensson L.G., Coselli J.S., et al. Surgical treatment of aneurysm and or dissection of the ascending aorta, and transverse aortic arch: factors influencing survival in 717 patients. J Thorac Cardiovasc Surg 1989;98:659-674.[Abstract]
  8. Hickey P.R., Anderson N.P. Deep hypothermic arrest: a review of pathophysiology and clinical experience as a basis for anesthetic management. J Cardiovasc Anesth 1987;1:137-155.[Medline]
  9. John ER, Pricheps LS, Chabot RJ, et al. Monitoring brain function during cardiovascular surgery: hypoperfusion vs microembolism as the major cause of neurological damage during cardiopulmonary bypass. In: Refsum, Hulg, Rasmussen, eds. Heart and brain, brain and heart. Berlin: Springer Verlag, 1989:405–21.
  10. Brillman J. CNS complications in coronary artery bypass graft surgery. Neurologic Clinics 1993;11:475-495.[Medline]
  11. Pugsley W., Klinger L., Paschalis C., et al. The impact of microemboli during cardiopulmonary bypass on neuropsychological functioning. Stroke 1994;25:1393-1399.[Abstract]
  12. Moody D.M., Bell M.A., Challa V.R., et al. Brain microemboli during cardiac surgery or aortography. Ann Neurol 1990;28:477-486.[Medline]
  13. Taylor K. Brain damage during cardiopulmonary bypass. In: Kawashima, Takamoto, eds Amsterdam: Elsevier, 1997:3–13.
  14. Guerit J.M., Verhelst R., Rubay J., et al. Multilevel somatosensory evoked potentials (SEPs) for spinal cord monitoring in descending thoracic and thoracoabdominal aortic surgery. Eur J Cardio Thorac Surg 1996;10:93-104.[Abstract]



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This Article
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Robert A. Dion
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