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Ann Thorac Surg 2006;82:1679-1687
© 2006 The Society of Thoracic Surgeons
a Department of Cardiovascular Surgery, University Hospital Freiburg, Freiburg, Germany
b Department of Neurosurgery, University Hospital Freiburg, Freiburg, Germany
c Department of Cardiac Surgery, University Heidelberg, Heidelberg, Germany
d Department of Cardiothoracic Surgery, Mount Sinai Medical Center, New York, New York
Accepted for publication May 11, 2006.
* Address correspondence to Dr Weigang, Department of Cardiovascular Surgery, University Hospital Freiburg, Hugstetter Strasse 55, 79106 Freiburg, Germany. (Email: ernst.weigang{at}web.de).
Presented at the Poster Session of the Forty-second Annual Meeting of The Society of Thoracic Surgeons, Chicago, IL, Jan 30Feb 1, 2006.
| Abstract |
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METHODS: Between November 2000 and July 2005, vital parameters and spinal cord function were monitored, including cerebrospinal fluid pressure and transcranial motor-evoked and somatosensory-evoked potentials in 36 stent-graft procedures (31 patients) on the thoracic or thoracoabdominal aorta.
RESULTS: Stent-graft placement was technically successful in all patients. We achieved a survival rate of 100% without neurologic deficit after fast-track extubation. Eleven of 31 patients exhibited changes in evoked potentials during stent-graft deployment. In 12 of 31 patients (including the 11 with evoked potential alterations), cerebrospinal fluid pressure exceeded 15 mm Hg. Cerebrospinal fluid drainage and vital parameter adjustment were executed in those instances. We observed intraoperative evoked potential total recovery in 10 of 11 patients after these interventions.
CONCLUSIONS: Interventions to improve spinal cord perfusion led to total recovery of spinal function in most patients (10/11). Therefore, spinal cord protective measures with motor- and somatosensory-evoked potential monitoring, cerebrospinal fluid drainage, and prevention of hypotension can reduce the incidence of spinal cord ischemia and improve the neurologic outcome of patients undergoing endovascular thoracic or thoracoabdominal aortic repair.
| Introduction |
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After successful reimplantation of the segmental arteries, reperfusion injury can occur as cytotoxic metabolites, formed during aortic clamping, are flushed back [6]. Another mechanism for spinal cord ischemia is a rise in the volume of blood supplied to the brain that occurs during cross-clamping and, in turn, leads to an increase in intracranial pressure (ICP) and a drop in spinal cord perfusion. Different surgical techniques and strategies to protect the spinal cord have been described to reduce the incidence of spinal cord ischemia, including identification and reimplantation of critical segmental arteries, systemic hypothermia, adjunctive pharmacologic therapy, and cerebrospinal fluid (CSF) drainage [7]. Despite these measures, the risk of postoperative neurologic deficits in patients with thoracic or thoracoabdominal aortic open surgical repair remains significant. All in all, the main cause for spinal cord ischemia during open thoracic or thoracoabdominal aortic surgical repair is aortic cross-clamping.
CSF drainage has been used as an adjunct during thoracic or thoracoabdominal aortic open surgical repair over the last 15 years [811]. The rationale is based on animal experiments that suggest that decreasing the CSF pressure during cross-clamping of the aorta enhances spinal cord perfusion and thereby decreases the risk of ischemia-induced paraplegia. Specifically, a decrease in the distal aortic pressure also causes a decrease in the spinal artery pressure. Therefore femorofemoral or left heart bypass is used after the proximal aorta is cross-clamped to improve the distal aortic pressure by increasing the extracorporeal circulatory pump flow. A concomitant rise in the CSF pressure can lead to a spinal cord compartment syndrome [12]. By draining CSF, the pressure is reduced, relieving the compartment syndrome and increasing the perfusion to the spinal cord. This theory is supported in a recent clinical literature review article analyzing a large number of patients from many different institutions undergoing thoracic or thoracoabdominal surgery with and without concomitant CSF drainage [11].
Intraoperative neurophysiologic monitoring is another technique implemented in open thoracic or thoracoabdominal aortic surgery. Here, the functional integrity of the spinal cord can be evaluated by measuring somatosensory-evoked potentials (SSEPs) as well as transcranial motor-evoked potentials (tcMEPs), which exhibit a change upon induced ischemia. Studies have supported the value of this technique in thoracic or thoracoabdominal aortic open surgical repair [1318].
The interventional aortic repair technique with endovascular stent-graft implantation enhances the general prospects of a positive outcome for these patients [19]. The stent-graft implantation technique itself has several advantages. Aortic cross-clamping is not necessary, and the proximal hypertension with negative effects on cerebrospinal cord perfusion are thus avoided. Distal aortic perfusion remains uninterrupted, guaranteeing a continuous blood flow to the spinal cord. During endovascular stent-graft implantation, segmental arteries were not reimplanted. Thus, this technique is not accompanied by reperfusion injury to the spinal cord. The frequency of neurologic complications with this minimally invasive method appears to be reduced compared with open surgical aortic repair. However, endovascular stent-graft repair of the thoracic or thoracoabdominal aorta is associated with a risk of perioperative spinal cord ischemia occurring in 3% to 12% of patients [2025].
The aim of our study was to evaluate whether adjunctive techniques such as CSF drainage combined with neurophysiologic monitoring (SSEPs and tcMEPs) and prevention of hypotension can reduce the risk of paraplegia and decrease the mortality rate in patients undergoing thoracic or thoracoabdominal stent-graft implantation.
| Material and Methods |
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High-risk patients were defined as 11 with a distinct thoracoabdominal aneurysm of the aorta and 5 with previous open surgical infrarenal aortic replacement. At particularly high risk were 11 patients who received multiple stent-graft implantations and 2 patients who received infrarenal Y-Dacron (Vascutek Ltd, Glasgow, Scotland) prostheses with occlusion of the internal iliac arteries and occlusion of a high number of segment arteries caused by poor collateral flow into the spinal cord.
The university ethics committee reviewed and approved the study (study approval number 108/2001). Full informed consent was obtained from all patients for participation in the study, including stent-graft implantation, neurophysiologic monitoring, placement of a spinal catheter to measure and drain spinal fluid, and data collection with analysis.
Endovascular Stent-Graft Implantation
All patients received preoperative CT or angiography to determine individual aortic anatomy and obtain exact measurements for stent-graft sizing (Fig 1). All stent-graft procedures were performed in the operating room by two cardiovascular surgeons. Endovascular stent-grafts (Talent and Valiant, Medtronic AVE, Minneapolis, MN; TAG Excluder, W. L. Gore and Assoc, Flagstaff, AZ; and Zenith, Cook Group Inc, Bloomington, IN) were placed under fluoroscopic guidance. No branched stent-grafts were used.
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Strategies to Protect the Spinal Cord
We used a set of strategies to protect the spinal cord to improve the neurologic results. Permissive moderate systemic hypothermia (34° to 35°C) by the use of no active warming measures reduces the oxygen demand of the neural tissue (5% per degree Celsius) [29]. Adjustments in the case of change of tcMEPs or SSEPs to guarantee sufficient spinal cord perfusion pressure included the use of noradrenaline to increase the MAP to more than 80 mm Hg. The CVP was reduced to less than 12 mm Hg by use of nitroglycerine and restrictive volume management. In all patients with tcMEP or SSEP changes, CSF pressure was lowered less than 10 mm Hg. In addition, we drained fluid if the ICP exceeded 15 mm Hg, regardless of spinal cord function [30].
Cerebrospinal Fluid Drainage
We inserted a CSF drainage catheter in all patients except those who had recently been prescribed nonaspirin antiplatelet therapy (ie, clopidogrel) and those who were coagulopathic. The CSF drain was routinely inserted by a neurosurgeon the day before surgery, thus minimizing the risk of intrathecal or epidural bleeding with intraoperative and postoperative anticoagulation. Insertion was performed in the usual manner by puncture preferentially between the spinous processes L4/5 at the level of the posterior iliac crest in the left lateral decubitus position with a 14-gauge Tuohy needle. Once the CSF began to flow, a Portex lumbar drain (Portex Ltd, Kent, UK) was inserted 30 cm into the intradural space. Correct placement was checked by observing the spontaneous flow through the catheter and gently aspirating 2 mL of clear CSF with a syringe. The drain was then blocked, secured at the puncture site with sterile dressing, and the distal blocked connector was lead along the right lateral abdomen and chest and secured in the anterior axillary line. The drain was secured with wide tape dressing along its entire course and connected to the external monitoring equipment before surgery began to register the baseline. Intraoperatively, CSF was drained in case the CSF pressure exceeded 15 mm Hg. Other neuroprotective measures included adjusting the MAP and CVP. Routine CSF pressure monitoring was done until the third postoperative day. If CSF pressure exceeded 15 mm Hg, CSF was drained again under pressure control.
Intraoperative Neurophysiologic Monitoring
Additional neurophysiologic monitoring serves as a control mechanism to identify spinal cord ischemia. It reveals pathologically relevant changes in the functional integrity of neural tissue and makes early intervention possible so that the physiologic situation can be restored.
TcMEPs are induced to observe signal transmittance in the descending neuronal motor pathways. Upon transcranial stimulation of the motor cortex, a motor response occurs in the peripheral muscles (Fig 3, top). SSEPs assess the function of the ascending neuronal sensory pathways. The cerebral response is measured continuously after electrical stimulation of a peripheral nerve (Fig 3, bottom). Both the tcMEP and SSEP monitoring methods assess spinal cord function and have a complementary controlling character: tcMEP recordings reflect the functional integrity of the anterolateral tract, and SSEP recordings the posterior tract of the spinal cord. We used the 10-20 system for electroencephalogram recordings, in which tcMEP stimulation electrodes are attached percutaneously in the area corresponding to the C3/C4 region of the motor cortex, and the SSEP recording electrodes are positioned at Cz/Fz [31]. TcMEP recording electrodes are placed into the anterior tibial muscles and gastrocnemius muscles. SSEP stimulating electrodes are percutaneously inserted lateral and caudal to the malleolus medialis to stimulate the tibial nerve (EWACS and ISIS IOM; inomed, Medizintechnik GmbH, Teningen, Germany) [31].
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After the patient has been anesthetized, a baseline recording is made. The baseline guarantees a correct definition of the patient's preoperative spinal cord function. The basic method to gain SSEP recordings involves signal averaging. Usually, the responses of 200 stimuli are averaged because of the relatively long distance between the recording electrodes and the somatosensory cortex [31]. This removes any "noise" and allows for an interpretable signal. It is important to obtain the baseline recordings before surgery, because interference from technical equipment precludes viable recordings. Furthermore, the comparison between intraoperatively gained potentials and the patient's individual baseline values enables the neurophysiologic monitoring team to assess acute spinal cord function [16, 17].
The sequence and placement of tcMEP and SSEP electrodes follows a careful plan to avoid hindering the anesthetic preparations and to save precious time. The placement of the percutaneous needle electrodes occurs after the patient has been anesthetized and positioned on the operating table. Once placed, the electrodes can provide stable recordings for many hours, even once the intervention has ceased [31]. We stopped recording after the patients were awake.
| Results |
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The 5 patients with acute type B dissection still showed a slight retrograde flow in the false lumen postoperatively that was barely noticeable at discharge. The rate of postoperative complications was also minor in those patients who presented with high perioperative risk in terms of a potential spinal cord ischemia, namely those with an extensive thoracoabdominal aortic aneurysm or those with previous surgery on the abdominal aorta.
We performed neurophysiologic monitoring during endovascular stent-graft implantation in 36 procedures (31 patients). Both tcMEPs and SSEPs remained intraoperatively stable in 20 (65%) of 31 patients. We recorded a loss or changes of evoked potentials (tcMEPs and SSEPs) in 11 patients (35%) (3 CC type I, 3 CC type II, 2 CC type III, 1 CC type IV, 1 descending thoracic aortic aneurysm, 1 acute Stanford type B dissection) immediately after the stent-graft deployment (Table 3). We observed a loss in tcMEPs in 3 patients (10%), with 1 to 2 minutes' latency after stent-graft deployment. Seven patients (23%) showed a drop in tcMEP amplitudes of 50% to 70%. The SSEP amplitudes decreased during the 7 to 12 minutes after the deployment of the stent-grafts in 8 patients (26%) and disappeared briefly in 4 patients (13%). In none of these cases was intraoperative blood loss the reason behind the loss of the evoked potentials. The incidences of neurophysiologic potential decrease in our study were accompanied by decreases in blood pressure (42%) and heart rate (31%). In addition, we recorded an increase in CVP by 76% and in ICP by 112% in those patients. These comparisons are based on each patient's individual preoperative baseline values (preoperative baseline ICP values were 8 to 10 mm Hg). Furthermore, experience has shown that tcMEPs react more sensitively to intraoperatively implemented interventions than do the SSEPs. SSEPs respond with delayed alterations in amplitude, latency, and recovery after changes in the tcMEP.
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An increase in blood pressure was obtained through noradrenaline infusion; a decrease in central venous pressure was achieved with nitroglycerin infusion. Owing to intraoperative interventions, full recovery of tcMEP and SSEP values was achieved in 10 (91%) of the 11 patients with an intraoperative loss or change in evoked potentials. In 1 patient (9%) with total loss of tcMEPs and SSEPs, the evoked potentials recovered slightly after our interventions. No neurologic deficit was detected after fast-track extubation in the operating room. A temporary paraparesis developed at home 3 weeks after the stent-graft procedure in 1 patient whose potentials had been intraoperatively stable.
| Comment |
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Endovascular stent-graft repair of the thoracic or thoracoabdominal aorta has shown a promising reduction in perioperative morbidity and mortality rates owing to the procedure's advantagesit has less influence on patient perfusion physiologycompared with open surgical aortic repair techniques [30]. Aortic cross-clamping is not necessary during stent-graft placement, thereby avoiding the proximal hypertension and the negative effects on spinal cord perfusion associated with open surgical aortic repair methods. The distal aortic perfusion remains uninterrupted, guaranteeing a continuous blood flow to the spinal cord. Reperfusion injury during open surgical aortic replacement can only occur when, after successful segmental artery reimplantation, cytotoxic metabolites that formed during cross-clamping are flushed [6]. The risk of reperfusion injury of the spinal cord by over-stenting segmental arteries during stent-graft placement is low. Unfortunately, however, the risk of spinal cord ischemia remains in 3% to 12% of patients who undergo thoracic or thoracoabdominal stent-graft placement [2025].
Stent-graft implantation in the thoracic or thoracoabdominal position might have drawbacks vis-à-vis spinal cord perfusion owing to an occlusion of segmental arteries. Surprisingly, over-stenting and occluding of large segments of segmental arteries lead to a low incidence of spinal cord ischemia. One possible explanation is an uninterrupted distal aortic perfusion guaranteeing a continuous collateral blood flow to the spinal cord. Consequently, this risk factor appears to be less important than the overall advantages of this procedure, particularly when stent-graft procedures are performed on patients with chronic atherosclerotic aneurysm compared with acute aortic dissection, because collaterals develop with time and are able to compensate. Many studies have underlined the importance of these individual collateral arterial networks supplying the spinal cord in patients undergoing thoracic or thoracoabdominal endovascular stent-graft repair [20, 32, 33].
Endoluminal stent-grafting restricts maneuverability in case of permanent loss of evoked potentials, despite all of our neuroprotective measures. Endovascular stent-graft implantation may still be preferable to open thoracoabdominal repair, however, because it lowers the rate of paraplegia and mortality [20, 21, 36]. A few case reports have been published on this subject [3739]. According to our experience, endovascular stent-graft implantation lowers both the rate of neurologic complications and mortality compared with open surgical procedures involving the prosthetic replacement of the thoracoabdominal aorta [16]. This correlates with our low incidence of changes in SSEPs and tcMEPs during the stent-graft procedures.
Yet, more patients presented with changes during intraoperative neurophysiologic monitoring than there were postoperative neurologic complications. Only 1 (3%) of our 31 patients had a delayed postoperative neurologic deficit; this corresponds with published reports [2025]. One can assume that a temporary spinal cord malperfusion occurs during the over-stenting of the segmental arteries during stent-graft implantation that triggers obvious changes during neurophysiologic monitoring. By taking additional neuroprotective measures (MAP > 80 mm Hg, CVP < 12 mm Hg, ICP < 15 mm Hg), one can counter the malperfusion, and collateral flow into the spinal cord is improved.
We were able to demonstrate in our study that the evoked potentials (SSEPs and tcMEPs) recovered during our neuroprotective measures. One might therefore consider some of these measurements as false-positives. It is certainly true that paraplegia would not have developed in all of these patients, but we are convinced that all of them had some degree of temporary spinal cord ischemia. These measurements do not permit the distinction between mild and severe forms of spinal cord ischemia; therefore, it is mandatory to act immediately if any sign of spinal cord ischemia is suspected. The measures we propose to improve spinal cord perfusion are relatively easy to perform, are associated with low morbidity, and can safely be administered to all patients showing signs of spinal cord ischemia, even when paraplegia would not ultimately develop in all of them.
Evoked potentials are a valuable tool for monitoring intraoperative spinal cord function, which allows the interdisciplinary team to assess any potential ischemic incident and act accordingly to minimize the risk of postoperative neurologic complications. The study of Cheung and colleagues [22] has suggested a potential value of SSEPs combined with CSF drainage in thoracic stent-graft repair.
A distinction must be made regarding the relevance and prognostic value of tcMEP loss compared with a SSEP loss [13]. The tcMEPs allow insight into spinal cord function within several minutes after an intervention. Also, the tcMEPs can be remeasured after only a short interim. The SSEPs, on the other hand, gradually deteriorate and exhibit a retarded restoration period and an impending long-term loss, even after an intervention to counteract any potential malperfusion. Both types of evoked potentials gauge different anatomic spinal cord structures having a different vascular supply.
Given these differences between tcMEPs and SSEPs, we conclude that measuring tcMEP has greater prognostic value than measuring SSEP, also because tcMEPs directly assess the integrity of the motor pathways. This allows the detection of impending motor deficit, which is more important for the postoperative outcome than sensory deficits. Despite the SSEP limitation, we recommend implementation of both of these monitoring methods, because SSEPs provide additional safety as well as more diagnostic advantages. Moreover, the reversibility of changed potentials coinciding with an uneventful neurologic outcome stresses the fact that neurophysiologic monitoring is able to detect an impending deficit at a reversible stage. Based upon our positive results, we would like to expand Cheung and colleagues' [22] thesis and recommend the routine implementation of tcMEP, SSEP, and CSF pressure monitoring for all thoracic or thoracoabdominal stent-graft implantations.
CSF drainage is an additional tool to minimize spinal cord ischemia. Our experiences during open surgical thoracic or thoracoabdominal repair have shown that this intervention is followed by a recovery of evoked potentials and consequently has a positive effect on the neurologic outcome of our patients [16, 17]. We therefore also decrease ICP to less than 15 mm Hg during thoracic or thoracoabdominal stent-graft implantation.
We insert the CSF drain at least 12 hours before surgery for two main reasons. First, it is necessary to register a baseline of the patient's individual CSF pressure under healthy conditions; only then can an aberrance of pressure in a pathologic situation be reliably detected and it permits a controlled insertion versus a late insertion only in case of neurologic complication. Second, an early insertion (at a time when the patient is without anticoagulation) can reliably decrease the risk of hazardous complications such as a spinal intrathecal or epidural hemorrhage with possible consecutive neurologic deficits, as our and other data show [16, 17, 34, 35]. In addition, we did not detect any problems with infections and consecutive meningitis using this strategy.
We took other neuroprotective measures in addition to CSF drainage, such as adjusting the MAP and CVP. The combination of various neuroprotective measures based on actual spinal cord function (measured via evoked potentials) is more differentiated than using only continuous nonpressure-adapted CSF drainage because it lowers the risk of CSF drainage-induced complications, such as headaches.
From these results we conclude that monitoring the neurophysiologic functions of patients undergoing thoracic or thoracoabdominal aortic endovascular stent-graft implantation is a valid method to detect spinal cord malperfusion and serves as a guideline for therapeutic spinal cord protective interventions. At our institution, neurophysiologic monitoring has become routine during thoracic and thoracoabdominal aortic repair because it is easy to implement and does not hinder perioperative and intraoperative activity [31]. Loss of tcMEP and SSEP is associated with spinal cord ischemia [14]. Most of these patients have a higher risk for paraplegia or death than patients without tcMEP or SSEP loss [16, 40]. By raising MAP and reducing central venous and CSF pressure, spinal cord perfusion is presumably improved and recovery of tcMEP and SSEP can be achieved. These spinal cord protective measures lower the incidence of spinal cord ischemia and improve the neurologic outcome of patients undergoing endovascular thoracic and thoracoabdominal aortic repair.
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