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Ann Thorac Surg 2006;82:592-596
© 2006 The Society of Thoracic Surgeons


Original article: Cardiovascular

Combined Use of Adamkiewicz Artery Demonstration and Motor-Evoked Potentials in Descending and Thoracoabdominal Repair

Hitoshi Ogino, MDa,*, Hiroaki Sasaki, MDa, Kenji Minatoya, MDa, Hitoshi Matsuda, MDa, Naoaki Yamada, MDb, Soichiro Kitamura, MDa

a Cardiovascular Surgery, National Cardiovascular Center, Suita, Osaka, Japan
b Radiology, National Cardiovascular Center, Suita, Osaka, Japan

Accepted for publication March 3, 2006.

* Address correspondence to Dr Ogino, Department of Cardiovascular Surgery, National Cardiovascular Center, 5-7-1 Fujishirodai, Suita, Osaka 565-8565, Japan (Email: hogino{at}hsp.ncvc.go.jp).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: We retrospectively reviewed the outcome of distal descending aortic and thoracoabdominal aortic repair with preoperative identification of the Adamkiewicz artery by magnetic resonance angiography and intraoperative monitoring of transcranial motor-evoked potentials.

METHODS: We began combined use of demonstration of the Adamkiewicz artery and intraoperative recording of motor-evoked potentials for prevention of spinal cord complications in descending and thoracoabdominal aortic aneurysm repair in 1998. Ninety-two consecutive patients were studied, with descending aneurysm in 53 and thoracoabdominal aneurysm in 39 patients. The repair was performed through a left thoracic or thoracoabdominal incision, using partial cardiopulmonary bypass to prevent spinal cord injury. Magnetic resonance angiography revealed the Adamkiewicz artery in 70.7% of cases. During surgery, spinal cord ischemia was monitored using motor-evoked potentials. Anastomoses were performed using a segmental clamp technique to reduce spinal cord ischemic time. Based on the findings of magnetic resonance angiography and motor-evoked potentials, the Adamkiewicz artery and other relevant intercostals and lumbar arteries were revascularized or preserved, or both.

RESULTS: The mean durations of partial cardiopulmonary bypass, cross-clamping, and surgery, respectively, were 144.4 ± 232.2, 106.0 ± 65.5, and 411.8 ± 170.7 minutes. Three hospital deaths (3.3%) occurred in patients with a thoracoabdominal aortic aneurysm. Motor-evoked potentials changed in 9 patients (9.8%), in 8 (88.9%) of whom they were eventually restored. Although paraplegia developed in 1 patient (1.1%) with a mycotic descending aneurysm, the other patients survived without spinal cord injury.

CONCLUSIONS: Combined visualization of the Adamkiewicz artery and determination of motor-evoked potentials are useful in preventing spinal cord injury in descending and thoracoabdominal aortic repair.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Spinal cord injuries such as paraplegia and paraparesis are still the most devastating complications of surgery for descending thoracic aortic aneurysm (dTAA) or thoracoabdominal aortic aneurysm (TAAA) [1]. Various strategies for protection have been advocated to prevent it, including distal perfusion with left heart bypass [2] or partial cardiopulmonary bypass [3], intraoperative monitoring of spinal cord ischemia with somatosensory-evoked or motor-evoked potentials [4, 5], reattachment of intercostal or lumbar arteries [6, 7], cerebrospinal fluid drainage [8], and epidural cooling [9]. Since 1998, we have used two novel techniques to prevent spinal cord injury. First, using an anatomical approach, the Adamkiewicz artery (AKA) is identified by contrast magnetic resonance angiography (MRA) before surgery [10]. That is followed by a functional approach involving intraoperative monitoring of spinal cord ischemia using transcranial motor-evoked myogenic potentials (MEPs), to prevent spinal cord injury. In the present retrospective study, the efficacy of combined use of preoperative demonstration of the AKA and intraoperative determination of MEPs in preventing spinal cord injury was evaluated.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
This study reviewed the outcome of 92 consecutive patients with dTAA or TAAA between 1998 and 2003. The median age was 67 years (range, 19 to 91). There were 68 males (73.9%) and 24 females. Of the patients, 53 had a dTAA and the other 39 had a TAAA, which was Crawford I in 5 (12.8%), II in 3 (7.7%), III in 27 (69.2%), and IV in 4 cases (10.3%). There were 60 (65.2%) nondissecting and 32 dissecting aneurysms. Fourteen (26.4%) of the patients with a dTAA required redo surgery, as did 19 (48.7%) of the patients with a TAAA. One patient (1.1%) underwent surgery emergently for a ruptured aneurysm. The etiology of aortic lesions was atherosclerotic in 78 patients, Marfan syndrome in 6 patients, degenerative (non-Marfan) in 5 patients, mycotic in 2 patients, and traumatic in 1 patient. All of the aortic dissections were in chronic stage.

Institutional approval for this study was obtained, and each patient within the study gave informed consent for serving as a subject.

Demonstration of the AKA
We significantly reduce the invasiveness of our procedures with the use of MRA (Fig 1) [10]. The AKA was imaged by contrast MRA using gadolinium dimegulumine (0.3 mmol/kg body weight). Early- and late-phase images were used for differentiation of arteries and veins. Imaging volumes covered the levels between T6 and L3. Diagnosis of the AKA and the anterior spinal artery was made by at least two radiologists using 0.6 mm contiguous sections processed by multiplanar reconstruction. The diagnostic criteria were described in previous reports [10]. In 3 patients of the present series, the AKA was visualized by multidetector computed tomography (MD-CT) scans instead of MRA because MRA was not available (Fig 1). Figure 2 shows the levels of the critical intercostal or lumbar arteries connecting to the AKA, as demonstrated by MRA. Presence of the AKA was demonstrated in the so-called critical zone between T8 and L1, particularly around T9 or T10, in all but 1 patient. The AKA was demonstrated in 65 patients (70.7%). The AKA originated predominantly from the left side intercostal or lumbar arteries in 76.9% of cases. In 18 patients (34.0%) with a dTAA and in 9 patients (23.1%) with a TAAA, the AKA could not be identified by MRA or MD-CT.


Figure 1
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Fig 1. Magnetic resonance angiography demonstrates the Adamkiewicz artery (AKA [large white arrows]) ascending to the anterior midsagittal surface of the spinal cord from the radicular-medullary artery originating from the dorsal branch of the intercostal or lumbar artery. It is continuous with the anterior spinal artery (ASA), with a hairpin turn in the early phase (left). The Adamkiewicz artery (white arrow) can be visualized clearly by multidetector computed tomography scans as well (right).

 

Figure 2
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Fig 2. Levels of critical intercostal or lumbar arteries connecting to the Adamkiewicz artery (AKA), demonstrated by magnetic resonance angiography. The AKA was demonstrated in 65 patients (70.7%). In 18 patients with a descending thoracic aortic aneurysm (hatched bars) and in 9 patients with a thoracoabdominal aortic aneurysm (solid bars), the AKA could not be identified by magnetic resonance angiography or multidetector computed tomography scans. (R = right side; L = left side.)

 
Motor-Evoked Potentials
For functional assessment after the anatomical study, MEPs were monitored during surgery [4, 5]. Under sufficient anesthesia with low doses of fentanyl (0.02 to 4 mg/kg), propofol (4 to 6 mg · kg–1 · h–1), and vecuronium (0.04 mg · kg–1 · h–1), the motor cortex was activated by 600-V transcranial electrical stimulation. The action potentials conducted through the anterior horn motor neurons were recorded from the skin over the upper extremity muscles (as a control), the lower extremity muscles, and the thenar muscle. Monitoring of MEPs is influenced by anesthesia including neuromuscular blockade. Light anesthesia was maintained with a low dose of vecuronium. During cross-clamping, MEP levels were determined every 2 to 5 minutes. A fall in MEP amplitude to less than 25% of the baseline was taken to indicate ischemia of the spinal cord [5].

Surgery
The aneurysm was approached through a left thoracic or thoracoabdominal incision. During aortic cross-clamping, distal aortic perfusion at a pressure above 60 mm Hg was maintained by partial cardiopulmonary bypass consisting of a heparin-coated femorofemoral circuit, with permissive mild hypothermia at 32°C to 34°C. Anastomoses were performed using a "segmental clamp technique" [7] to reduce spinal ischemic time. In cases with extended lesions that included the visceral arteries, visceral perfusion was also performed, using 12F or 14F branched balloon-chipped tubes of the cardiopulmonary bypass circuit [7]. Cerebrospinal fluid drainage was not routinely performed in this series, and was used in only two high-risk patients with Crawford type II TAAA [8].

In each case, a surgical strategy for reconstructing or preserving the relevant intercostal arteries or lumbar arteries was devised, based on the preoperative anatomical assessment of the AKA identified by MRA. Revascularization of the intercostal or lumbar arteries was guided by monitoring of MEPs. Subsequently, the Adamkiewicz artery and other relevant intercostals and lumbar arteries, predominantly those between T8 and L1, were revascularized or preserved by beveling techniques. Especially large intercostals and lumbar arteries with poor backflow were spared. In most cases, the critical intercostal or lumbar arteries and visceral arteries were selectively reconstructed using a graft interposition technique with an 8-mm tube graft; in the remaining 2 patients, en-bloc reconstruction was performed. When critical reduction of amplitude of MEPs was observed, rapid revascularization of the spinal cord blood supply was performed [5]. In addition, distal perfusion flow was increased to increase the distal pressure above 80 mm Hg. The blood pressure of the upper body was also increased with use of catecholamines or transfusion, or both. In all cases, revascularization of the spinal cord was carried out until MEPs were restored.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
The mean durations of partial cardiopulmonary bypass, aortic cross-clamping, and surgery were, respectively, 144.4 ± 232.2, 106.0 ± 65.5, and 411.8 ± 170.7 minutes. There were 3 in-hospital deaths (3.3%), although there was no 30-day mortality. Three elective patients (7.7%) with TAAA died of graft infection, bowel necrosis, or gastrointestinal bleeding. Various complications occurred, including bleeding in 9 cases, stroke in 1, respiratory failure in 9, renal failure in 4, complications of gastrointestinal tract in 6, hepatic failure in 1, sepsis (graft infection) in 2, chylothorax in 4, and wound problems in 7 cases. The mean lengths of ventilatory support, intensive care unit stay, and hospital stay were 17.8 ± 28.2 hours, 4.1 ± 4.3 days, and 30.1 ± 14.3 days. The mean amount of blood transfusion was 2436 ± 3307 mL.

The MEPs changed in a total of 9 patients (9.8%). The MEPs disappeared in 2 patients (3.8%) with dTAA. Among patients with TAAA, the MEPs disappeared in 4 (10.3%), and their amplitude decreased significantly to less than 25% in 3 patients (7.7%). The MEPs were successfully restored by rapid reconstruction of the blood supply to the spinal cord, except in 1 patient in whom paraplegia developed. The duration for restoration of the MEPs was between 5 minutes and 3 hours after revascularization of the spinal cord. In 8 of the 9 patients having the MEPs change, the AKA had been identified preoperatively. In 6 of these 8 patients the MEPs decreased expectedly during ischemia of the AKA, whereas in the other 2 patients they decreased unexpectedly. In 2 of the former 6 patients with a preoperatively identified AKA, the other intercostal arteries close to the AKA were reconstructed because the orifices of the AKA were occluded. In another patient whose AKA was not identified, the MEPs returned after revascularization of the intercostal arteries between T7 and T9.

In only 1 patient, an 85-year-old man with a mycotic descending aortic aneurysm, did paraplegia develop. In this patient, preoperative MRA demonstrated that the first lumbar artery (L1) was the AKA. The aorta between T9 and T10 involved by the mycotic aneurysm was replaced using an aortic allograft with preservation of the T8 and T11 intercostal arteries. The MEPs disappeared after completion of the repair, and never returned. The aortic cross-clamping time was 80 minutes. Despite subsequent cerebrospinal fluid drainage, the patient had paraplegia due to spinal cord infarction between T7 and T9. Figure 3 shows the reconstruction or preservation of the intercostal or lumbar arteries. The Adamkiewicz artery and other relevant intercostals and lumbar arteries, predominantly those between T8 and L1, were revascularized or preserved by beveling techniques.


Figure 3
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Fig 3. Reconstruction (light bars) or preservation (dark bars) of the intercostal or lumbar arteries (large numbers). The Adamkiewicz artery and other relevant intercostals and lumbar arteries, predominantly those between T8 and L1, were revascularized or preserved, or both, by beveling techniques. Especially large intercostals and lumbar arteries with poor backflow were spared. (R = right side; L = left side.) The small numbers show the levels of the critical intercostal or lumbar arteries connecting to the Adamkiewicz artery, demonstrated by magnetic resonance angiography (Fig 2).

 

    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
The findings of this retrospective study suggest that the combination of the preoperative anatomical approach of demonstrating the AKA by MRA followed by intraoperative functional test using MEPs is useful for preventing spinal cord injury. The information obtained from the anatomical assessment provides a "map" of the relevant intercostal or lumbar artery suitable for reconstruction or preservation of the blood supply to the spinal cord, while the subsequent functional monitoring provides a precise and real-time guide ensuring spinal cord safety without ischemic deficits and without delays during surgery.

Preoperative knowledge of the target arteries requiring reconstruction or preservation is greatly advantageous. The usefulness of preoperative identification of the AKA by selective spinal angiography has been proposed by other groups, in Europe [11–13]. However, selective angiography is invasive and time-consuming, and carries the risk of serious spinal cord injury due to embolization and bleeding. Yamada and colleagues [10] from our institution were the first to demonstrate the feasibility of preoperative detection of the AKA using noninvasive contrast MRA. Yoshioka and colleagues [14] then also succeeded in visualizing the AKA by similar techniques using MRA. They developed a new technique of MD-CT to demonstrate the AKA and the collateral arteries to the spinal artery [15]. Demonstration by MD-CT is less time-consuming than contrast MRA and can enables visualization of the origin of the intercostal artery connecting to the AKA more clearly, with three-dimensional views. However, MD-CT has the disadvantages of not excluding the influence of the spine on the image of the AKA and lack of accurate differentiation of the AKA from the anterior radicular vein which has a similar hairpin curve. The contrast medium needed for MD-CT carries the risk of allergic response or adverse effects on the kidney; therefore, MRA is still our current modality for AKA demonstration.

Preoperative AKA identification aids preoperative planning of surgical strategy. The safest segmental cross-clamp site can easily be determined, as can the appropriate range of aortic lesion to be replaced or target vessels to be vascularized, based on preoperative anatomical assessment of the AKA. However, brief ischemia of the spinal cord due to cross-clamping the aorta involving key vessels is inevitable during surgery. In 9 of our patients, MEPs changed during the temporary interruption of spinal cord blood supply by aortic cross-clamping. In 8 of these 9 patients, excluding the paraplegic patient, they were restored by rapid revascularization of the spinal cord. Without preoperative identification of the AKA, the MEPs might have changed at higher frequencies, possibly resulting in a higher incidence of spinal cord complications.

However, preoperative demonstration of the AKA cannot prevent all spinal cord injury. Some arteries requiring reconstruction or preservation might lie elsewhere, apart from the identified AKA. Identification of superior and middle dorsal arteries representing important collateral pathways to the spinal cord was also addressed in a previous report [13]. In fact, we had 1 patient in whom paraplegia developed owing to spinal cord infarction between T7 and T9. Although the aortic zone replaced was between T9 and T10, and distant from the L1 artery identified as the AKA by MRA, the patient had paraplegia. Postoperative MRA revealed numerous collateral arteries connecting to the AKA and originating from the occluded 11th intercostal arteries. The 11th intercostal arteries were preserved but eventually occluded, presumably because they were close to the suture line, and the aorta had severe calcification. In some other patients, we encountered change in MEPs by aortic cross-clamping of other vessels, even distant from the origin of the AKA.

These findings suggest the existence of a complex network of blood supply to the spinal cord, including sources from the intercostal or lumbar arteries as well as the left vertebral artery, the internal thoracic artery, and the internal iliac arteries [13, 16]. It is also difficult to intraoperatively identify which artery is principally responsible for spinal cord ischemia, since aneurysms including the orifices of intercostal or lumbar arteries are generally elongated longitudinally [13]. In patients with atherosclerotic aneurysms, most intercostal or lumbar arteries are liable to be occluded [5]. Thus, preoperative demonstration of the AKA, if performed alone, cannot prevent all spinal cord injury.

Monitoring of MEPs can provide important, precise information on adequate blood supply to the spinal cord in real time during surgery [4, 5]. The efficacy of MEP monitoring has been much discussed. However, MEP monitoring is influenced by peripheral ischemia, anesthesia including neuromuscular blockade, and systemic hypothermia. It also is unable to prevent all spinal cord complications [4, 5]. Therefore, together with monitoring of the MEPs, it is advantageous to use a map of the target vessel connecting to the spinal cord demonstrated by MRA, to obtain more reliable protection for the spinal cord. Combined use of these modalities is superior to separate use of them. With significant change in MEPs, rapid revascularization of the spinal cord should be performed, even for other intercostal arteries apart from the AKA. Even if the identified AKA has already been reconstructed, revascularization of the other relevant arteries should be carried out until MEPs are restored.

Kawaharada and colleagues [17] have published similar reports on the usefulness of preoperative identification of the AKA by MRA, after ours. In their study, the AKA was detected at a higher rate (83%) than ours (70.7%). In our attempts at demonstration of the AKA, clear identification was achieved in 50% of cases. In 20% of cases, an artery appearing to be the AKA was visualized without clear identification. In the remaining 30% of cases, no artery resembling the AKA was visualized. Their surgical strategy also differs from ours. They reconstructed only the target artery identified as the origin of the AKA, and stated that 11% of their 120 patients had two AKAs. In some of their patients without preoperative identification of the AKA, paraplegia developed, although selected patients whose AKA had been detected did not have spinal cord injury. In our experience, occlusion of the orifice of the preoperatively identified AKA, which was also demonstrated by MRA, sometimes occurred. In these circumstances, we vascularized other relevant arteries close to the occluded AKA (Fig 3). We believe that it is unwise to reconstruct only the target intercostal or lumbar arteries connecting to the AKA [13].

Limitations
The anatomical approach we have described still suffers from problems such as absence of identification of the major AKA artery in approximately 30% of patients, difficulty of intraoperative identification of the AKA demonstrated by preoperative MRA, and imperfect detection of the artery supplying blood to the spinal cord—in sum, incomplete understanding of the overall blood supply [10]. The number of patients involved in this study, particularly patients with Crawford I or II TAAA, was small, because two- or three-staged repair had been our surgical strategy before 1998. With a larger number of Crawford I or II patients, the incidence of spinal cord injury might have been a little higher than in the present study.

We conclude that preoperative noninvasive identification of the Adamkiewicz artery by MRA, followed by intraoperative functional assessment by MEPs, reduces the risk of spinal cord injury in descending and thoracoabdominal aortic repair.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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