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Ann Thorac Surg 2006;82:1670-1677
© 2006 The Society of Thoracic Surgeons
a Department of Cardiothoracic Surgery, Mount Sinai School of Medicine, New York, New York
b Department of Neurosurgery, Mount Sinai School of Medicine, New York, New York
Accepted for publication May 8, 2006.
* Address correspondence to Dr Etz, Department of Cardiothoracic Surgery, Mount Sinai School of Medicine, One Gustave L. Levy Place, New York, NY 10029. (Email: christian.etz{at}mountsinai.org).
Presented at the Poster Session of the Forty-second Annual Meeting of The Society of Thoracic Surgeons, Chicago, IL, Jan 30–Feb 1, 2006.
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Abstract |
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METHODS: One hundred consecutive patients with intraoperative monitoring of motor evoked potentials (MEP) and somatosensory evoked potentials (SSEP) during TAA/A repair involving serial segmental artery sacrifice (October 2002 to December 2004) were reviewed.
RESULTS: Operative mortality was 6%. The median intensive care unit stay was 2.5 days (IQ range: 1–4 days), and the median hospital stay 10.0 days (IQ range: 8–17 days). Potentials remained unchanged during the course of serial segmental artery sacrifice, or could be returned to baseline levels by anesthetic and blood pressure manipulation, in 99 of 100 cases. An average of 8.0 ± 2.6 segmental artery pairs were sacrificed overall, with an average of 4.5 ± 2.1 segmental pairs sacrificed between T7 and L1, where the artery of Adamkiewicz is presumed to arise. Postoperative paraplegia occurred in 2 patients. In 1, immediate paraplegia was precipitated by an intraoperative dissection, resulting in 6 hours of lower body ischemia. A second ambulatory patient had severe paraparesis albeit normal cerebral function after resuscitation from a respiratory arrest.
CONCLUSIONS: With monitoring of MEP and SSEP, sacrifice—without reimplantation—of as many as 15 intercostal and lumbar arteries during TAA/A repair is safe, resulting in acceptably low rates of immediate and delayed paraplegia. This experience suggests that routine surgical implantation of segmental vessels is not indicated, and that, with evolving understanding of spinal cord perfusion, endovascular repair of the entire thoracic aorta should ultimately be possible without spinal cord injury.
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Introduction |
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In 1993, Svensson and associates [1] described the risk of paraplegia after TAA/A repair in a historic series of 1,509 patients as being 16% overall: according to the Crawford classification, spinal cord injury occurred in 15% of type I aneurysms, 31% of type II, 7% of type III, and 4% of type IV aneurysms. A variety of multimodality approaches has been developed to reduce spinal cord injury secondary to distal aortic surgery [2–4]. It has been assumed that injury arises primarily as a consequence of two mechanisms. The first involves an intraoperative insult: temporary interruption of spinal cord blood supply during the operative procedure of a duration sufficient to irreversibly damage cell bodies and nerve tracts in the spinal cord. The second is postoperative: permanent reduction of the blood supply secondary to sacrifice of critical blood vessels to a level incompatible with spinal cord viability.
Fundamentally, the community of aortic surgeons is divided by their hypothesis as to the cause of postoperative paraplegia. Those who believe that paraplegia is the consequence of chronic hypoperfusion after sacrifice of segmental arteries critical to spinal cord blood supply reimplant segmental arteries, trading prolonged acute cord ischemia for the achievement of arguably superior postoperative perfusion. Believing that the blood supply to the spinal cord depends upon a highly variable collateral system capable of perpetuating sufficient spinal cord perfusion even after radical sacrifice of (almost all) segmental arteries under stable hemodynamic conditions encourages others to forego reimplantation, shortening acute spinal cord ischemia by cutting down aortic cross-clamp time.
Neurophysiologic monitoring–assisted TAA/A repair aims to assess the functional status of the spinal cord during the procedure to guide operative strategy. In theory, it is helpful regardless of one's beliefs concerning the principal cause of paraplegia, since it aids in identifying when acute spinal cord hypoperfusion begins to have a functional impact.
Somatosensory evoked potential (SSEP) monitoring alone during surgical cases involving the descending aorta has been associated with an unacceptably high rate of both false positive and false negative predictions of postoperative motor function in the lower limbs [5–7]. These false positives and negatives can occur because SSEPs reflect the integrity of the somatosensory system that lies in the dorsal spinal cord, whereas the neurons critical for motor function are located in more ventral areas of the cord [5].
During the last decade, motor evoked potential (MEP) monitoring has become clinically feasible [8]. Monitoring of MEPs allows for the early detection of spinal cord ischemia and is currently becoming an integral part of spinal cord protective strategies during TAA/A surgery [9–11]. Motor evoked potentials are not suitable for postoperative monitoring, however, so SSEP continue to be used to detect spinal cord dysfunction during the hours immediately after aortic surgery.
We report our experience with monitoring of MEP and SSEP during repair of TAA/A in 100 consecutive patients in whom spinal cord artery reattachment was (with 1 exception) not carried out.
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Material and Methods |
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The underlying disease was atherosclerosis in 45 patients, dissection in 37 patients (34 chronic and 3 acute), and degeneration in 11 patients. Features of Marfan syndrome were present in 7 patients. The average aneurysm diameter measured 68 ± 14 mm. Further patient characteristics, and the risk profile for the group as a whole, are shown in Table 1. Two thirds of the patients were scheduled for the operation owing to enlargement of their known aneurysm. One third were admitted with acute symptoms. Fifteen patients underwent repair of ruptured aneurysms. Of the entire patient group, 66 had elective, 29 had urgent, and 5 underwent emergent procedures. Aneurysm classification and the adjunctive methods utilized to help preserve spinal cord integrity are shown in Table 2.
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Partial cardiopulmonary bypass was used in 34 patients. In these cases, right atrial drainage was established through the common femoral vein and the catheter position controlled by transesophageal echocardiography. Arterial cannulation was performed through a common femoral artery in 30; axillary cannulation or side arms of the graft were used in 2 cases each.
In 17 patients, full cardiopulmonary bypass and deep hypothermic circulatory arrest were utilized. All segmental vessels were sacrificed before bypass, so MEP/SSEP monitoring was possible.
For visceral perfusion, additional catheters were used in 6 patients for the kidneys and in 1 for the superior mesenteric artery. In the remaining patients, a beveled distal anastomosis incorporating the visceral vessels was utilized.
Operative Management
All operations are carried out under at least moderately hypothermic conditions (Table 4). The aneurysm is dissected free from mediastinal tissue. The intercostal and lumbar arteries are dissected and temporarily occluded. If MEP and SSEP remain unchanged, the segmental vessels are sacrificed before opening the aneurysm, to avoid backbleeding and possible steal from the spinal cord circulation. The process of neurophysiologic evaluation and sacrifice of each pair of segmental arteries takes 3 to 5 minutes. If no changes in MEP are noted over the next 10 minutes or so, the next section of the aorta is dissected, 1 to 3 more segmental arteries are occluded, and evoked potentials are once again assessed. This process is repeated until the entire aneurysm has been mobilized. In general—in view its importance in supporting spinal cord perfusion—clamping of the left subclavian artery is avoided, and the internal mammary artery and the superior epigastric axis are preserved. If clamping of the distal aorta is not feasible or is unsafe, the distal anastomosis is done first, and distal perfusion restored after cross clamping of the graft. For the visceral segment, a beveled anastomosis is frequently utilized. If the visceral segment must be replaced circumferentially, the visceral vessels are occluded with a balloon catheter and intermittently perfused with cold blood before they are directly anastomosed to the graft or connected utilizing intervening graft segments (8 to 12 mm Dacron).
Graft Repair
Vascular Dacron grafts (Hemashield; Boston Scientific, Natick, MA; 18 to 28 mm) with as many as three additional side arms were implanted in an end-to-end fashion. The superior mesenteric artery (SMA) was reimplanted in 9, renal arteries in 11, and the celiac in 10 patients. In only 1 patient, an island including intercostal arteries was reimplanted because of extraordinary back bleeding from included intercostals.
MEP Monitoring
After induction, volatile anesthetics were discontinued, as were muscle relaxants, and narcotic anesthesia was substituted. Motor evoked potentials were elicited by a train of nine transcranial electrical pulses delivered from a Digitimer D185 cortical stimulator (Welwyn, Garden City, United Kingdom). The stimuli were applied through two disposable corkscrew electrodes (Nicolet Biomedical, Madison, Wisconsin) anchored in the scalp overlying the left and right motor cortices, respectively, approximately 6 to 8 cm lateral from vertex. In response to stimulation, MEPs (composed of compound muscle action potentials) were recorded from the skin over the tibialis anterior (leg) and abductor pollicis (hand) muscles through subdermal needle electrodes. The recordings from the hands permit evaluation of the effects of anesthesia and temperature on the amplitudes of the MEPs. The signals were amplified, filtered, digitized, and saved to hard drive. The stimulation intensity was set to 10% above the level that elicited the maximal MEP amplitude for each patient. A decrease of 50% in amplitude of the leg MEPs in the presence of stable hand MEPs was considered to reflect a lower body ischemic event. In patients in whom hypothermic circulatory arrest was utilized, MEPs were measured during removal of the aneurysm under moderate hypothermia, before deep cooling, and again upon rewarming.
SSEP Monitoring
Somatosensory evoked potentials were elicited by stimulation of the left and right posterior tibial nerves through two surface disk electrodes placed approximately 2.0 cm apart below the medial malleolus at the ankle. Recordings were made from the scalp overlying the somatosensory cortex using subdermal needle electrodes placed approximately 3 to 4 cm behind vertex and referenced to an electrode at FPz on the forehead. A ground electrode was placed on the shoulder. The recorded signals were amplified, filtered, and saved to hard drive. The responses to 200 to 300 stimuli were averaged. Ischemic spinal cord dysfunction was defined as a decrease in SSEP amplitude of more than 50%.
In 99 of 100 cases, MEP and SSEP remained unchanged during the course of serial segmental artery sacrifice, or could be returned to baseline levels (see Fig 1) by anesthetic and blood pressure manipulation, or with increase of distal perfusion during left heart bypass. One patient had loss of SSEP/MEP late intraoperatively (discussed below) and developed paraplegia. Figure 1 shows examples of neurophysiologic recordings from the operating room.
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Postoperative Management
Somatosensory evoked potentials are monitored until the patient awakens. Thereafter, hourly brief neurologic examinations are performed for 72 hours. High normal blood pressures are maintained, aiming for an aortic mean pressure of 80 mm Hg. Drainage is continued for 72 hours, and steroids are tapered over 48 hours.
Statistical Methods
Data were entered in an Excel (Microsoft Corp, Redmond, Washington) spreadsheet and transferred to a SAS file (SAS Institute, Cary, North Carolina) for data description and analysis. Characteristics are described as percentages or as means and standard deviations.
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Results |
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Paraplegia
Postoperative paraplegia occurred in 2 patients. In 1, immediate paraplegia was precipitated by an intraoperative dissection resulting in 6 hours of lower body ischemia. The patient had an atherosclerotic aneurysm (Crawford III) and a longstanding history of peripheral artery disease (after 100 pack-years of smoking). She underwent second-stage completion of an elephant trunk with sacrifice of nine segmental arteries (T6 through L2): SSEP and MEP disappeared after release of the distal clamp and occlusion of both iliac arteries by dissection. Restoration of lower extremity perfusion by stent grafting did not restore neurologic function.
A second patient had severe paraparesis albeit normal cerebral function after resuscitation from a respiratory arrest that occurred 3 weeks postoperatively, after discharge to a rehabilitation facility. The patient had segmental artery sacrifice from T3 to L3.
No patient with fewer than nine intersegmental arteries severed had paraplegia, although 52 patients had nine or more segmental pairs sacrificed. Spinal cord ischemia detected by MEP (1) or SSEP (2) was reversible in 3 patients after adjunctive maneuvers (ie, lightening anesthesia and raising mean arterial blood pressure) were performed to improve perfusion. One patient had preoperative paraplegia that was unaffected by surgery.
Other Complications
The average intensive care unit stay was 4.3 ± 7.3 days, and the mean hospital stay was 16.0 ± 15.2 days. As detailed in Table 5, 4 patients had cardiac complications; 7 patients required prolonged ventilation, with an early tracheostomy in 4 patients; 9 patients had renal complications requiring temporary hemodialysis in 4 cases (none of the patients required chronic dialysis), and 5 patients required reoperation for bleeding.
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Comment |
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In the 1980s, SSEP monitoring began to be accepted as a sensitive method for detecting spinal cord injury, and became an established guide to spinal cord protection strategies during TAA/A surgery [12, 13]. But it is the motor neurons within the spinal cord whose functional impairment triggers paraplegia, and compromise of motor neurons can elude SSEP monitoring. Therefore, monitoring of motor neuron integrity would seem to be the next significant step toward finding a strategy to prevent paraplegia [6]. Somatosensory evoked potentials continue to have an important role in the immediate postoperative period, however, as MEPs cannot be carried out readily in unanesthetized patients.
Motor evoked potential monitoring is the most sensitive tool available to assess the functional integrity of motor neurons and guide intraoperative strategies to restore blood supply to this most vulnerable part of the spinal cord, and prevent irreversible ischemic damage [11]. In clinical studies, MEP data appear to show a better correlation with neurologic outcome than SSEP [5, 6, 14], leading contemporary aortic aneurysm surgery to a further reduction in the prevalence of postoperative paraplegia. In 2000, Jacobs and associates [11] reported a significant reduction of neurologic complications—to 2.3%—with the monitoring of MEP in a series of 170 patients with TAA/A, using a reimplantation approach with left heart bypass and cerebrospinal fluid drainage. Van Dongen and colleagues [15] reported a 4.2% rate of postoperative paraplegia in a series of 118 patients, using hypothermia, left heart bypass, and a reimplantation strategy guided by MEP and SSEP monitoring. In 2002, Dong and coworkers [6] reported a 5.4% paraplegia rate in a series of 56 TAA/A operations utilizing MEP and SSEP monitoring with a reimplantation approach. Only 25% of Dong's patients with MEP evidence of spinal cord ischemia showed congruent SSEP changes, and 3 patients with persistent loss of MEP (and recovery of SSEP) suffered paraplegia despite segmental artery reimplantation, underlining the superior sensitivity and specificity of MEP in detection of spinal cord ischemia [6].
The majority of the studies sought to prevent ischemia by reimplantating segmental arteries with particular focus on the area between T7 and L1, believing that paraplegia is the consequence of hypoperfusion after sacrifice of critical spinal cord arteries. Nevertheless, clinical use of MEP has not yet significantly impacted the strategy of reimplantation, as most of the surgeons used an empirical approach rather than a standardized sequence of maneuvers when MEP diminution occurred. But with or without neurophysiologic monitoring and other adjuncts, reimplantation remains the most widespread strategy for preserving spinal cord function. Several studies have demonstrated the arguable superiority of that approach: a recent study by Jacobs and coworkers [16] had 5 cases of paraplegia among 70 type II aneurysms (3 immediate and 2 delayed). LeMaire and associates [17] had earlier reported a series of 1,220 patients operated on by Coselli, using liberal reimplantation of segmental arteries, with an overall paraplegia rate of 4.6%; spinal cord injury occurred in 8.2% of 371 patients with type II aneurysms. In contrast, in 1994 and 1996, paraplegia rates as low as 3% in thoracoabdominal aneurysm repair without intersegmental artery reimplantation were described both in a series of 110 by Acher and colleagues [18], and in 95 consecutive patients by Griepp and associates [19].
According to our current protocol, which uses both MEP and SSEP monitoring, reimplantation was only utilized when all maneuvers involving anesthetic and hemodynamic optimization failed. In 98 of 100 consecutive patients, sacrifice of a total of more than 800 segmental arteries—including radical sacrifice of an average of 4 segmental arteries between T7 and L1—was achieved without persistent intraoperative MEP loss, and therefore without reimplantation. (One patient was already paraplegic preoperatively, and in another, unusually vigorous backbleeding from intercostals prompted empirical reimplantation of a patch of aorta including these arteries). If there were an artery of Adamkiewicz whose integrity was critical for spinal cord function, more than half of these patients should have developed paraplegia. No patient with fewer than nine intersegmental arteries severed had paraplegia. Spinal cord ischemia was reversible in 3 patients after adjunctive maneuvers were performed to improve perfusion, suggesting that spinal cord blood supply is unlikely to depend upon a single segmental artery between T7 and L1. We therefore believe that it is not reasonable to search for a single artery of Adamkiewicz whose preservation will prevent paraplegia. Since the postoperative paraplegia rate in our series was 2%, which is lower than was found in several contemporary series, this suggests that blind reimplantation of as many spinal cord arteries as technically possible may not necessarily be a superior approach.
Our operative strategy for avoiding paraplegia may owe much of its success to its effectiveness in avoiding backbleeding through intercostal and lumbar arteries, and thus preventing steal from the collateral circulation to the spinal cord. With our technique, intraoperative steal is prevented by sacrificing the segmental arteries before opening the aneurysm. Acher, who also has a very low incidence of paraplegia without segmental artery reimplantation, oversews the segmental arteries immediately after incising the aneurysm, thereby also limiting backbleeding and radically reducing steal.
Available clinical data, particularly on the evoked potential response to cross-clamping, indicate that grey matter perfusion varies considerably even among patients with equivalent TAA extent. Factors such as development of the anterior spinal cord artery, and the particulars of collateral circulation, are likely to account for this variability, and cannot be influenced by reimplantation, particularly when individual intercostal aortic ostia are already occluded. We monitor MEPs to try to identify critical individual intercostals for reimplantation, but have not found any. Attempts to identify and reimplant segmental arteries may jeopardize motor neuron integrity by increasing intraoperative spinal cord ischemia by prolonging aortic crossclamp duration.
Jacobs and coworkers [20] reported that increasing distal perfusion to physiologic levels during left heart bypass can correct MEPs in 27% of the patients with intraoperative MEP loss, underlining the presence of an efficient network of collaterals capable of providing sufficient perfusion to the cord under physiologic conditions. We postulate that an adequate cord blood supply based on a network of natural vessels is present at the end of the operation in patients with intact MEPs [20].
The advantage of segmental artery reimplantation clearly is to establish a redundant blood supply, which should provide protection against the inadequacy of a marginal collateral network in the face of perioperative instability, which therefore may pose less of a threat to cord viability. But reimplantation has the disadvantage of removing a stimulus to the growth of the collateral network, leaving cord viability dependent upon vascular grafts, which may thrombose. Without reimplantation, although this collateral network is marginal, normal compensatory mechanisms should result in its augmentation over time. Until such augmentation occurs, however, avoidance of postoperative hypotension and spinal cord edema seem to be the most effective strategies for preventing deficits in the acute postoperative interval [4]. If delayed paraplegia occurs in patients who have no reimplanted segmental arteries, it is more likely to be functional rather than anatomic (thrombosis), and should therefore be easier to treat (by raising blood pressure and using cerebrospinal fluid drainage). Risk factors compromising the collateral network—such as atherosclerosis—may have an impact on the occurrence of paraplegia: both cases in our cohort were octogenarians with severe generalized atherosclerosis and sacrifice of at least nine segmental arteries.
From this surgical experience of extensive aneurysm resection without segmental artery reimplantation, one would anticipate that, with suitable precautions, endovascular repair of the entire thoracic aorta should be possible without spinal cord injury. The experience with these 100 cases suggests that serial sacrifice of almost all intersegmental pairs—gradually, over a period of time during the operative procedure, and in a way which prevents any backbleeding and steal from the collateral network—is safe. With physiologic monitoring to guide surgical segmental artery sacrifice, it is possible to modify the operative strategy to accommodate loss of those arteries which threaten function, as reflected by diminution in MEP or SSEP.
Endovascular stent grafting precipitates simultaneous occlusion of intersegmental arteries, which may result in a more severe insult. It is possible that physiologic monitoring, combined with endovascular techniques to reduce steal, can help diminish the incidence of spinal cord injury after endovascular TAA/A repair. We hope that further improvements in understanding the dynamics and patterns of adaptation of the collateral circulation will enable marked reduction of paraplegia rates with endovascular repair in the near future.
In conclusion, this experience suggests that routine surgical implantation of segmental vessels is not indicated. There is still much to learn concerning the anatomy and physiology of spinal cord blood supply if paraplegia is to be eliminated as a complication of TAA/A repair, but recent advances suggest that such a goal is achievable.
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