Angiographic localization of spinal cord blood supply and its relationship to postoperative paraplegia

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1 Angiographic localization of spinal cord blood supply and its relationship to postoperative paraplegia G. Melville Williams, MD, Bruce A. Perler, MD, James F. Burdick, MD, Floyd A. Osterman, Jr, MD, Sally Mitchell, MD, Dimitri Merine, MD, Benjamin Drenger, MD, Stephen D. Parker, MD, Charles Beattie, MD, and Bruce A. Reitz, MD, Baltimore, Md. Forty-seven patients underwent selective catherization of middle and lower thoracic intercostal and upper lumbar arteries m define the origin of the artery of Adamkiewicz. One patient had significant atheroembolism, and a second had transient lower extremity paresthesias. No other compfications occurred. The origin was found in 26 (55%), and 21 patients underwent thoracoabdominal aneurysm repair with this knowledge. When the critical lumbar or intercostal artery could be included as part of a long proximal or distal anastomosis, all 12 patients could be included as part of a long proximal or distal anastomosis, all 12 patients survived, and one was paralyzed. However, if the aneurysm repair mandated a midgraft anastomosis to intercostal arteries critical to spinal cord perfusion, seven of nine patients either died or were paralyzed (p < 0.05). In the group of 19 patients operated on in whom spinal cord blood supply was not identified three patients had a technically unsuccessful operation; two died, and one was paralyzed. Twelve of 16 patients who had an adequate, but unsuccessful attempt at localization were treated by intercostal "neglect" and survived. Late paresis developed in two patients, but they are walking now. One of the patients who died had multiple systems failure and awakened paraplegic. She had a patent, enlarged, thoracic radlcular artery at T-5 which probably supplied to spinal cord and which was missed angiographicauy. Paralysis was associated with aneurysm extent (group 2 and III B, dissections vs group 1 & 3,p < 0.05). Selective intercostal angiography requires further refinement, but it is safe and offers the promise of understanding the mechanisms and risks of spinal cord complications after repair of extensive thoracoabdominal aneurysms. (J VAse SuRG 1991;13:23-35.) On the basis of detailed anatomic dissections in man, Adamkiewicz ~ challenged the existing concept of spinal cord blood supply in Instead of finding as in animals that every intercostal and lumbar artery provided posterior radicular branches to help supply the anterior and posterior spinal arteries, he demonstrated fewer and larger arteries. The largest of these arteries was named the arteria radiculomedullaries magna, commonly abbreviated to ARMM and known also as the great radicular artery (GRA). From the Departments of Surgery, Radiology (Drs. Osterman, Mitchell, and Merine) and Anesthesia (Drs. Drenger, Parker, and Beattie) The Johns Hopkins Medical Institutions, Baltirnore. Presented at the Forty-fourth Annual Meeting of the Society for Vascular Surgery, Los Angeles, Calif., June 4-6, Reprint requests: G. Melville Williams, MD, Blalock 606, The Johns Hopkins Hospital, 600 N. Wolfe St., Baltimore, MD /6/25611 Most subsequent investigators 24 agree that this branch of an intercostal artery provides the greatest contribution to the anterior spinal artery, which enlarges at the point of its junction with the GRA. Considerable variation exists in the origin of the GRA and lesser radicular arteries normally, and additional anatomic diversity is created by aneurysmal disease. This is so because the development of atherosclerosis or mural thrombus may occlude some originally important intercostal vessels, leaving the spinal cord dependent on unusual and diverse collateral arteries. The importance of these contributions to the spinal cord circulation superimposed on a background of anatomic diversity creates difficult problems for the surgeon managing patients with extensive aneurysmal disease? To reduce the risks of paraplegia associated with the repair of lengthy segments of the aorta, Hollier 6 and McCuUough et al. 7 have applied procedures to preserve spinal cord perfusion during aortic clamp- 23

2 24 Williams et al. Journal of VASCULAR SURGERY Fig. 1. The characteristic appearance on digital subtraction angiography of the GRA (large arrow) joining the anterior spinal artery (small arrow) in the area of lumbar 'enlargement of this artery. Note the presence of numerous collateral vessels and the indistinct origin of the GRA (open arrow) from small tortuous vessels. ing. However, even if the spinal cord were protected well in this stage of the operation, the problem of identifying the source of the GRA remains. Most surgeons find and attach the largest cluster of backbleeding intercostal arteries at the critical zone of T-9 through T-12 hoping to supply the GRA directly or indirectly via collateral vessels. The difficulty with thi s approach is that the surgeon may guess wrong, and the time taken to attach a segment of aorta containing the origin of these vessels of unknown significance robs the liver and kidneys of blood flow. Therefore in attempting to avoid the complication of paraplegia, the surgeon may substitute an even worse problem of uncontrollable bleeding caused by liver ischemia or of renal cortical necrosis. A second approach is to eliminate guesswork by defining before or during surgery the origin of the blood supply to the spinal cord. Svensson et al.8 proposed on the basis of experimental work to inject isolated segments of the aorta with hydrogen monitoring the electrical potentials caused by such injec- tions with platinum electrodes placed anteriorly in the epidural space. Others have used selective angiography before operation. This approach has been feared greatly by vascular surgeons because there are documented instances of paraplegia associated with the intraaortic injection of contrasty However, other studies using less toxic contrast and injection volumes reported no permanent neurologic consequences after the selective injection of intercostal arteries to identify vascular malformations of the human spinal cord. 9'1 Indeed, Kieffer et al.n and Guilmet et al. ~2 have applied selective angiography to define contributions to spinal cord perfusion in patients with extensive aneurysms. Morbidity was rare and related to atheroembolism. Kieffer et al." reported outstanding surgical outcome in patients having the spinal cord completely revascularized, as only one patient in 20 sustained neurologic injury, which was mild and reversible. Twelve years ago we also began studying patients with particularly extensive aneurysms by selective intercostal artery injection. Our approach deviated from others in two ways. First, we reasoned that the GRA alone was critical to the thoracic "watershed" area of the spinal cord, and catheter manipulations above the area of origin of the GRA (T-7) might do more harm than good. Second, we anticipated that some patients with fusiform aneurysms containing extensive mural thrombus would have occlusions of major intercostal arteries at a pace permitting collateral vessels to develop from the neck. Therefore when we could not locate a major radicular contribution to the anterior spinal artery originating from the aneurysm, we assumed that collateral vessels had developed making it safe to proceed with a simple proximal, visceral-renal, and distal anastomotic repair. This report presents our experience attempting to localize the artery of Adamkiewicz angiographically in 47 patients. Forty of these patients have undergone surgical repair of extensive aneurysms based on the knowledge of whether or not the GRA was identiffed and if so, which intercostal or lumbar artery was its source. MATERIAL AND METHODS Patients The 47 patients comprising this series include 46 who had extensive aneurysms and one who had a tuberculous spinal abscess. The 46 patients with aneurysms were all considered to be at a high risk for paralysis because of the extensiveness of their aneurysmal disease. The mean age was 61.9 years and

3 Volume 13 Number 1 January 1991 Relationship of localization of spinal cord blood supply and paraplegia 25 Fig. 2. A flush injection of the midthoracic aorta in an 81-year-old man. A, The main aneurysm originates at T-10 (open arrow), but a second bulge in the wall of the vessels appears at T-7 (dark arrow). A number of intercostal arteries were identified in the critical zone (small arrows). The one labeled (a) was found to supply the anterior spinal artery. B, This intercostal vessel could have been included in the proximal anastomosis if it were necessary to repair the bleb. Notice the origin is from small vessels, and that collateral vessels are abundant. varied from 29 to 84 years. Twenty-eight men and 18 women participated. Selective catheterization of patent intercostal and lumbar vessels was performed to find which one, if any, contained a branch typical of the GRA. This important artery ascends at least 2 cm and turns to the midline where it joins the anterior spinal artery. The hairpin turn created by the GRA and the anterior spinal artery is characteristic (Fig. 1). We grouped our patients with fusiform aneurysms who were operated on into the four general types proposed by Crawford et al. x3 However, we clarified aneurysm extent a bit more explicitly. Patients with chronic expanding dissecting aneurysms are considered separately. Group 1. Aneurysms of most or all of the descending thoracic aorta and the upper abdominal aorta (extending to the celiac axis)--7 patients. Group 2. Aneurysms of most or all of the descending thoracic and most or all of the abdominal aorta-- 14 patients. Group 3. Aneurysms of the distal half or less (T- 10) of the descending thoracic and variable segments (at least to the renal arteries) of the abdominal aorta-- 11 patients. Group 4. Aneurysm of the entire abdominal aorta--no patients studied. Chronic expanding dissecting aneurysms: DeBakey type HIB. Involvement of all of the den scending thoracic aorta and the renal and visceral portion of abdominal aorta or more--8 patients. Angiographic technique All studies were done in sedated, hydrated patients via retrograde femoral artery catheterization. Flush aortograms were obtained whenever prior aortography failed to delineate filling of intercostal vessels. This allowed us to focus on areas in which these arteries were patent (Fig. 2). Various "shepherdcrooked" or "side winder" catheters were used to engage the orifices of the intercostal and lumbar arteries. Before 1984 when an intercostal orifice was engaged, hand injections of 5 to 10 ml ofdiatrizoate meglumine (Renograffin) or were made and spot films were obtained. Since 1984 we have used nonionic contrast, iohexol (Omnipaque), and digital sub-

4 26 Williams et al. Journal of VASCULAR SURGERY Fig. 3. Demonstration of a successful second attempt. A, Engagement of an intercostal artery at T-10 was possible after graft replacement of the entire abdominal and distal descending thoracic aorta. The numbered grid aids localization on spot films. Note the selective injection of the left T-10 (small arrow) fills T-9 (large arrow) and the anterior spinal artery (open arrow). B, Delayed digital subtraction angiography image of the same catheter injection shows a large posterior collateral (open arrow) and a smaller one (small arrow) join T-10 to T-9. The GRA (dark arrow) arises from T-9 to join the anterior spinal attery (small arrow). traction techniques were used after hand injections into patent intercostal vessels. No attempts were made to engage the intercostal vessels above T-7 to define the location and patency of a higher contribution to the spinal cord. A study was considered successful technically if the GRA was found or if all patent intercostal arteries were studied and the GRA was absent. Five of the 46 patients studied were examined twice. Three patients were considered by the radiologist to have had a technically inadequate and unsuccessful examination on the basis of failing to engage and image all patient intercostal or upper lumbar arteries. These three patients were operated on without additional testing. Surgical technique Before April 1988 none of 22 patients had spinal fluid drainage, 7 intrathecal papaverine, or the monitoring of evoked potentials from epidural (north) electrodes positioned 1 day before surgery. 14'1s Bypass procedures during aortic clamping were carried out according to the choice of the surgeon. Three patients underwent femoral-femoral bypass, eight had left heart bypass, and the remainder underwent simple cross-clamping and repair. After June of 1988, we used all of the above adjunctive measures thought to prevent paralysis, and all 18 patients had bypass of the aneurysm by means of the Biomedicus pump (Biomedicus Eden Prairie, Minn.). All but one patient had spinal cord function monitored with epidural electrodes/4,1s Statistical analysis The Student's t test was used to test the significance of age and sex on outcome. Otherwise, the chi-square test with the Yates correction for small sample size was used to test the null hypothesis. RESULTS LocaliTation of the artery of Adamkiewicz One of the 47 patients studied had a normal aorta and was examined to locate contributions to the anterior spinal artery before orthopedic reconstruction of the midthoracic spine because of tuberculous osteomyelitis. The GRA was readily identified at L-1 on the left. We failed to localize the GRA in 21 patients (46%), and the result was questionable in another who is being followed. In this case the hairpin turn was not as long, abrupt, or as large as in other patients. In 18 of these patients the intercostal

5 Volume 13 Number 1 January 1991 Relationship of localization of spinal cord blood supply and paraplegia 27 Fig. 4. Small branch origin of the GRA. A, The GRA (large arrow) originates from at least two small arteries (open arrow). B, Subsequent exposures demonstrate caudal flow in the anterior spinal artery (arrow). We never observed bidirectional flow at the junction of the GRA with the anterior spinal artery. vessels known to be patent by aortic flushing and in the field encompassed by the aneurysm were successfully engaged and studied, but did not contribute to spinal cord blood supply. In the other three instances efforts to locate the GRA were technically unsuccessful, and the study was discontinued before prominent intercostal arteries were examined. The reasons for stopping were one or several of the following: the limits of contrast were exceeded; it was not possible to enter the true or false lumen of an aortic dissection; extensive mural thrombus existed and the risk of continued manipulation was thought dangerous; and the lumen of the aneurysm was so large that the catheters could not be manipulated successfully to engage patent intercostal vessels. The latter reason was responsible for failure in one patient who underwent successful repair of a group 3 aneurysm. The remaining thoracic aorta dilated acutely, and a second search was made above the area of the repair (Fig. 3). The presence of a normal-sized graft allowed sufficient purchase to engage intercostal arteries and demonstrated the origin of the GRA at T-9. In the remaining 26 patients a characteristic contribution to the anterior spinal artery was found. The GRA arose at T-9 to T-12 in 69% of the patients (Table I). Localization was possible in 8 of 11 pa- Table I. Localization of origin of the artery of Adamkiewicz Total 1 T-7 2 T-8 1 T-9 6 T-10 7 T-11 2 T L-I 1 L tients with chronic spontaneous aortic dissections and in 18 of 34 (52%) patients with fusiform aneurysms. Most patients had extensive collateral vessels between the intercostal arteries (Fig. 3). The selective injection of one invariably led to the visualization of an intercostal vessel above or below and of the opposite side. This simplified the identification of the critical blood supply angiographically while also providing some reassurance to the surgeon that inclusion of a more proximal or distal intercostal artery into an anastomosis might suffice to sustain the blood supply to the spinal cord. Patients with chronic type IIIB dissecting aneurysms had a greater number of patent intercostal arteries.

6 28 Williams et al. Journal of VASCULAR SURGERY Table II. Outcome and type of intercostal attachment Dead Alive (paralyzed) Paralyzed Weak Inclusion Separate 2 4 (1) 1 1 ("button") p < 0.05 gery the following day. He died 1 day after operation. No direct or indirect evidence was found incriminating the angiographic study and the aortic rupture. No other patient sustained hemorrhagic, thrombotic, renal, or neurologic complications. The procedure, however, was time consuming requiring 1 to 7 hours. Fig. 5. The best demonstration of an important GRA (small arrow) originating directly from the intercostal artery (large arrow). This patient was treated with spinal fluid drainage, intrathecal papaverine, and atriofemoral bypass, Intercostal ischemic time was 12 minutes. Yet she awoke with paralysis at the T- 11 level, Most GRAs originated from small branches of the posterior branch of the intercostal arteries (Figs. 1, 2, B, and 4). A striking exception is illustrated in Fig. 5, which shows the GRA originating directly from a large intercostal artery. This patient was paraplegic despite the application of all ancillary methods thought useful for the prevention of cord ischemia and a 12-minute intercostal artery anastomotic time. Radiologic technique improved with experience. At times it was possible to direct the catheter tip posteriorly and inject 20 to 30 ml of contrast, which filled numerous intercostal arteries and even the GRA (Fig. 6). Selective angiography caused serious complications in just one recent patient who had a retroperitoneal hematoma, pancreatitis, and a rise in serum creatinine from 2 mg/dl to 4 mg/dl. Although reversible, the complications delayed her operation 3 months. Transient paresthesias developed in another patient's legs without paresis coincident with the injection of Kenograffin into the critical artery. These symptoms resolved in 2 hours. A final patient was asymptomatic immediately after his study, but his 8 cm fusiform (group 3) aneurysm ruptured 2 days later while he was hospitalized awaiting elective sur- Surgical and angiographic correlations Six study patients were not treated surgically. One age 83 years declined surgery and died of rupture 1 week after discharge. Four have chronic type IIIB aortic dissections and are being followed by CT scans. The final patient is scheduled for surgery. The remaining 40 patients provide early information regarding our two major questions. Failure to localize the artery of Adamkiewicz and outcome. Are there adequate collateral vessels to allow for a simplified operation? Three patients in this group of 19 had a technically unsuccessful attempt at catheterizing the intercostal arteries, and all had a poor outcome. In each case the surgeon and radiologist decided against a second angiographic attempt and opted for anastomotic intercostal artery inclusion. One patient died during surgery and two were paralyzed. The 16 patients who had a satisfactory technical attempt that failed to identify the spinal artery were treated without midgraft efforts to attach intercostal arteries (Table II). In this group of patients, 10 survived and are normal neurologically. Three patients, ages 70, 74, and 76 years, died during surgery or in the intensive care unit before neurologic status could be determined. One of these had a ruptured group 3 aneurysm. The fourth death occurred in a patient, age 71 years, who awoke densely paraplegic and died on the third postoperative day. She had two angiographic studies, and the only patent vessels in the "critical area" were at T- 11. These vessels were injected on each occasion and clearly did not supply the anterior spinal artery. At surgery the patient had deterioration of evoked potentials stimulated by epidural electrodes 3 minutes after the aorta at the subclavian origin was damped and lost activity completely 10 to 15 minutes later despite excellent

7 Volume 13 Number 1 January 1991 Relationship of localization of spinal cord blood supply and paraplegia 29 Table III. Aneurysm extent, type, and outcome Dead Alive (paralyzed) Paraplegic Weak Group Group (1) 3 1 Group IIIB Dissecting 3 2 (1) 2 1 Neurologic injury groups 1 and 3 versus 2 and IIIB p < midthoracic to femoral perfusion by atrial femoral shunt. The T-11 intercostal arteries were in the perfusion field. At the conclusion of the aortic repair, we observed backbleeding from an intercostal vessel at T-5, which was centered in the main body of the aneurysm. This vessel had never been identified angiographically and was excluded during atriofemoral bypass. In retrospect, this intercostal vessel, which was not perfused early or late, probably supplied the spinal cord through a hypertrophied thoracic radicular artery. The two patients suffering paraparesis awoke intact neurologically, but developed weakness after hypotensive episodes occurring the first week. Both are walking now. In summary, when the GILA could not be found after a technically successful search, neurologic outcome was excellent in 10 of 13 and acceptable in 12 of 13 patients. Three patients in this series had the entire descending thoracic aorta and the entire abdominal aorta replaced without attachment of any intercostal or lumbar vessels and are alive and healthy. Two other patients not studied angiographically because of the need for urgent surgical therapy have also survived this extensive repair. Only one in this group of five patients had a "one-stage" operation from subclavian origin to common femoral arteries. Three had the repair in two stages and one in three stages. Successful localization of the artery of Adamkiewicz. Does it help? The characteristic artery of Adamkiewicz (GRA) was identified in 21 patients, In 12 patients the critical intercostal artery or its documented collateralizing neighbor could be incorporated as part of the distal or proximal anastomosis. Ten patients had long slots cut into the posterior aspect of the graft to create a long posterior suture line to include one or two pairs of intercostal arteries. Two patients with chronic expanding dissecting aneurysms underwent extensive removal of the intimal flap from most of the descending thoracic aorta with tailored closure of the aortotomy to achieve a 2 cm diameter lumen thereby preserving all thoracic intercostal arteries. Follow-up CT scans Fig. 6. Demonstration of the posterior aortic flush technique currently used. When direct injection is not technically possible, the catheter tip is positioned posteriorly and a hand injection of 20 ml of contrast made. Note filling of two pairs of intercostal arteries and the GRA (arrow). have shown a stable aortic diameter. In this group of 12 patients treated by extensive anastomotic inclusion of the critical artery or its neighbor, one patient was paralyzed, and all survived: This ~esult is significantly different from the group of patients requiring a separate central anastomosis to restore circulation to the GRA (Table III). Nine patients, five with group 2 aneurysms, and three with type iiib chronic dissecting aneurysms underwent a separate midgraft anastomosis to include one or more pairs of intercostal vessels known to supply' the GRA. Four patients died of repeated intraoperative anastomotic disruptions. One of these lost evoked potentials as the "button" anastomosis was nearly complete and never regained them. One of five survivors was densely paraplegic on awakening, another was paretic, and the third had delayed severe paraplegia. Only two of these nine patients survived intact. The crucial question in this group of patients known to be in jeopardy is the timing of the ischemic event causing paraplegia. Was there ischemic damage caused by the lack of flow during the repair or the did, the intercostal anastomosis fail? Available evidence implicates the first mechanism in two patients and the second in one. The two patients suffering intraoperative spinal cord injury did so after 12 and 15 minutes of aortic occlusion despite all new ad-

8 30 Williams et al. Journal of VASCULAR SURGERY Vertebral a Thyrocervical trunk Art. of Adamkiewiez AORTA---~ Ant. spinal a. ~%--Cord iliac a. spinal a. radicular a. Collaterals Fig. 7. Schematic representation of the arterial supply to the spinal cord. The anterior and posterior spinal arteries originate from branches of the vertebral arteries and have contributions from the thyrocervical and costocervical trunks. The thoracic radicular artery is one of the more constant radicular branches contributing to the anterior spinal artery, particularly when the GILA originates from L-1 or L-2. We have drawn the origin of the GRA or artery of Adamkiewicz originating from a nest of collateral vessels from several intercostal arteries as this has been our observation in patients with aneurysms. The terminal portion of the spinal cord receives input from small branches of the internal iliac and/or middle sacral artery. The anterior and posterior spinal arteries are connected at this point by a circular artery, but are likewise fairly independent. junctive therapeutic measures. Delayed paraplegia occurred in a third patient who awoke intact, became paraplegic, and angiography documented occlusion of the intercostal arteries. Other factors determining outcome Our series is too small for much statistical power, yet there were features that still distinguished high and low risk patients. Thus although the risk of death and spinal cord injury was not significantly different for aneurysm groups in this small series, a comparison of aneurysm groups of lesser extent, 1 and 3, with those, both dissecting and fusiform, involving most of the descending thoracic and abdominal aorta, disclosed a significantly increased risk of paralysis in the latter (p < 0.05) but not of death. Adjunctive therapy applied since June of 1988 resulted in a higher rate of survival with normal spinal cord function, as 14 of 18 patients survived intact compared to 9 of 22 (p < 0.05). Neither patient age nor sex was associated significantly with either mortality rate or spinal cord injury in this small series. DISCUSSION The studies reported raised more questions than the two we posed, as answers must be qualified and based on an understanding of spinal cord circulation. Thus much is known (Fig. 7). The major arterial vessels of the spinal cord are a single anterior spinal artery and two smaller posterior spinal arteries. These longitudinal arteries originate from branches of the vertebral arteries with important contributions from the costocervical and thyrocervical trunks. Spinal cord perfusion is ultimately dependent on these arteries that receive additional vital contributions from branches of the intercostal and lumbar arteries. The largest contribution is the GRA, which arises as a direct or indirect branch of lower intercostal or upper lumbar arteries (Table I). Complexity is created by variable contributions from other radicular branches joining the anterior spinal artery. Dommisse 2 found that some human cadavers contained 17 radicular contributions, and others only had two. It is obvious that no surgeon could attach 17 intercostal-lumbar arteries or even the mean of eight found in autopsy specimens. 2 Therefore the fact that few patients are paraplegic after extensive aortic surgery indicates that the abnormality necessitating aortic repairs causes significant deviations from the normal semisegrnental spinal circulatory system. Clinical experience is very instructive regarding the importance of radicular branches (Fig. 8). The upper thoracic segment of the descending thoracic aorta extending from the subclavian artery to T-8 is commonly replaced, with paraplegia occurring in just 3% of patients despite anatomic dissections demonstrating a higher frequency of a significant radicular branch (thoracic radicular artery) originating from the upper thoracic intercostal arteries at T When the entire descending thoracic aorta is replaced, the risk of paraplegia increases to 9%, le as the thoracic radicular artery is likely to be sacrificed and the GRA threatened. The risk of paraplegia is again increased at least threefold when repairs are extended to most or all of

9 Volume 13 Number 1 Janua~ 1991 Relationship of localization of spinal cord blood supply and paraplegia 31 t Fig. 8. Schematic representation of the risk of spinal cord injury associated with the repair of various segments of the descending thoracic and abdominal aorta. The risk of paraplegia from clinical reports is associated with the length of the aortic segment requiring repair and the risk of injury to the GRA. the thoracic and abdominal aorta further threatening the GRA. 6"HJs Conversely, when replacement is limited to most of the abdominal aorta and the very most distal portion of the thoracic aorta, the risk of paraplegia again falls to 3%. ~3 The available evidence implicates the GILA as the most significant vessel requiring preservation to preserve spinal cord function. The important message from clinical experience is that the arterial supply to the spinal cord is adaptable. Relatively short segments of the diseased aorta may be replaced with low risk. However, extensive repairs of both the thoracic and the abdominal aorta entail a high risk because important contributions to the anterior spinal artery are likely to exist somewhere in the body of the aneurysm. Patients with extensive spontaneous dissecting aneurysm of the descending thoracic aorta inevitably have a higher risk of paraplegia. We suggest this is because a greater proportion of the intercostal vessels are patent, and there is less chance of adaptation and the formation of collaterals. There are at least three possible collateral pathways for the provision of spinal cord blood supply when the intercostal arteries are occluded by mural thrombus. The most significant of these may be anastomoses between the intercostal and lumbar arteries (Figs. 1, 2, B, and 4). Anastomotic channels exist posterior to the vertebrae through posterior muscular branches, between the vertebral body and the dura and through the substance of the vertebral bodies themselves. Lazorthes et al.2 concludes "From the occiput to the sacrum, horizontal anastomoses unite the vertebral branches of the cerebral, thoracic, and lumbar arteries, and vertical anastomoses unite the posterior muscular branches of these arteries." The second possible adaptive mechanism may be enlargement and continuity of the anterior spinal artery itself. Doppman et al.17 have demonstrated that the usually tenuous lower cervical and upper thoracic anterior spinal artery is capable of enlarging greatly to form a cervical to thoracic collateral spanning the area of an aortic coarctation. Thus enlargement of the anterior spinal artery is possible in man but has yet to be demonstrated in patients with aneurysms. Even greater speculation exists about the significance of the third collateral system, which depends on the branches of the internal lilac or middle sacral artery to perfuse the terminal Portion of the spinal cord and cauda equina) The fact that the internal iliac vessels are diseased or sacrificed so commonly without neurologic symptoms suggests that this system is normally of minor importance. We could find no reports of hypertrophy of this system in disease states. Whereas there is no clear evidence favoring any of these mechanisms as dominant, compelling evidence exists that one or more are operable in some patients. How else could one explain the observation that five

10 32 Williams et al. Journal of VASCULAR SURGERY of our patients had replacement of the entire descending thoracic and abdominal aorta without attachment of a single intercostal or lumbar vessel and are completely normal neurologically? One of these patients had such severe aneurysmal and occlusive disease that the repair had to terminate at the common femoral arteries at one stage. Is it possible to answer the two questions we posed and confirm the safety of spinal cord angiography? The latter issue is readily answered as modern contrast agents injected by hand prove to bc harmless to the spinal cord. The major risk of the procedure appears to be atheroembolism produced by catheter manipulation. The answer to our question of the safety of neglecting intercostal arteries when the GRA cannot be found is a qualified yes. The qualifications are two. First, a negative test must include the study of all patent potential sources for the GRA. The presumption of collateral vessels from a more superior or inferior source is dangerous when the studies are incomplete. Second, when the GRA cannot be identified in the lower thoracic and upper lumbar areas, less common contributions to spinal cord blood supply should be sought for they may become dominant, as was the case in one of our patients. Excluding such technical failures, 10 of 12 surviving patients treated by intercostal neglect were normal neurologically, and the remaining two are walking now. Yet is it reasonable to assume that all studies will be technically successful? Significant obstacles include the failure to identify and hence to study all patent intercostal arteries because some may be obscured by contrast in the body of large aneurysms; the inability to engage and study arteries known to be present; and the risk of atheroembolism. In the future, techniques providing positive evidence for collateral flow should be developed. For example, selective injections of the costocervical or thyrocervical vessels may define a continuous and large anterior spinal artery in some patients. This may be better grounds for neglecting intercostal vessels than our current approach depending on complicated negative evidence. The second question of whether knowledge about the location of a patent GRA can help surgical management, is also answered with a qualified yes. However, at this point, knowing the origin of the GRA is just the first step in the prevention of spinal cord ischemia. Our studies showed if the critical intercostal or lumbar artery or its collaterizing neighbor can be included in either the proximal or the distal anastomosis, the risk of ischemic injury was significandy less than when a separate midgraft anastomosis was required. This finding is best explained by the existence of abundant intercostal collateral vessels (Fig. 8). When an aneurysm repair must extend from T-8 to the terminal aorta and the GRA is found to arise from T-10, perfusion is apt to be maintained through more superior, patent intercostal vessels during the period of aortic clamping. Further, the inclusion of these vessels into the anastomosis provides a rapid and durable method of attachment. Conversely, when the critical intercostal vessel requires a separate anastomosis for attachment to the graft, spinal cord ischemia is more likely to occur during aortic clamping because the distance between these critical vessels and the collateral vessels above and below is greater. Additionally, the anastomosis of the aortic button containing these intercostal arteries to the graft is more cumbersome and tenuous. Irretrievable ischemic injury may occur within minutes and did so in three of our patients needing central graft attachment of the intercostal arteries despite spinal fluid drainage and intrathecal papaverine. Thus a group of patients undergoing repairs of group 2 aneurysms arc so critically dependent on contributions from the GILA that other methods for the protection of spinal cord must be developed to prevent ischemic injury. ~8,19 It is probably presumptuous to define categories of increasing risk of paraplegia based on anatomic studies, clinical reports, and our small early experience in spinal angiography. However, we believe there is merit in forming a hypothesis that there are four different risk categories. Patients at greatest risk are those having group 2 aneuryms and a large patent GILA arising directly from a large intercostal branch at the center of the aneurysm. We predict that patients with this anatomy are at high risk for becoming paraplegic during aortic clamping. A second category is defined as patients with equally extensive aneurysms, but whose GRA is smaller and originates from much smaller branches of the intercostal or lumbar arteries. We suggest that this group of patients may withstand aortic clamping, but not anastomotic failure. The third category of patients comprise those without an identifiable GRA arising from the aneurysm after a thorough technically successful anglographic study. The fourth category, consists of patients with less extensive aneurysms and the GRA identified but originating close enough to the normal aorta to permit an inclusion anastomosis. Careful studies must be encouraged to confirm or modify these categories, for they imply that greater success will be achieved only by altering our approaches to repairs of extensive thoracoabdominal aneurysms.

11 Volume 13 Number 1 Janua~ 1991 Relationship of localization of spinal cord blood supply and paraplegia 33 REFERENCES 1. Adamkiewicz A. Die Blutgefasse des Menschlichen Kfickemmarkes: I. Die Gefasse der Rtickenmarksubstanz. Sitz Akad Wiss Wien Math Natur Klass 1882;84: Dommisse GF. The blood supply of the spinal cord: a critical vascular zone in spinal surgery. J Bone Joint Surg 1975;56B: Lazorthes G, Gouaze A, Zadeh JO, Santini JJ, Lazorthes Y, Burdin P. Arterial vascularisation of the spinal cord. Recent studies of the anastomotic substitution pathways. J Neurosurg 1971;35: Crock MV, Yoshisawa M. Vascular supply of the vertebral column and the spinal cord. Berlin, New York: Springer Verlag, Szilagyi DE, Hageman JH, Smith RF, Elliott JP. Spinal cord damage in surgery of the abdominal aorta. Surgery 1978;83: Hollier LH. Protecting the brain and spinal cord. J VASC SURG 1989;5: McCuUough JL, Hollier LH, Nugent M. Paraplegia after aortic occlusion: influence of cerebrospinal fluid drainage. J VASC SURG 1988;7: Svensson LG, Patel V, Coselli JS, Crawford ES. Prelimina~ report of localization of spinal cord blood supply by hydrogen during aortic operations. Ann Thorac Surg 1990;49: DiChiro G, Doppman J, Ommaya AK. Selective arteriography of arteriovenous aneurysms of the spinal cord. Radiology 1967;88: Doppman JL, DiChiro G, Ommaya AK. Selective arteriography of the spinal cord. St. Louis: Warren H. Green, Inc., i 1. Kieffer E, Richard T, Chiras J, Godet G, Cormier E. Preoperative spinal cord arteriography in aneurysmal disease of the descending thoracic and thoraco-abdominal aorta: preliminary results in 45 patients. Ann Vasc Surg 1987;3: RichardT, Guilmet D, Bical O, et al. La protection medullaire au cours de la chirurgie de l'aorte thoracique et thoracoabdominale. In: Kieffer E, ed. Chirurgie de l'aorte Thoracique Descendante et Thoraco-Abdominale Paris. Paris: L'Expansion Scientifique, 1986: Crawford ES, Crawford JL, Sail HJ, et al. Thoracoabdominal aortic aneurysms: preoperative and intraoperative factors determining immediate and long-term results of operations in 605 patients. J VASC SURG 1986;3: Beric A, Dimitrijevic MR, Sharkey PC, Sherwood AM. Cortical potentials evoked by epidural stimulation of the cervical and thoracic spinal cord in man. Electroencephaiogr Clin Neurophysiol 1986;65: North RB, Drenger B, Beattie C, et al. Spinal cord stimulation evoked potential monitoring during thoracoabdominal aneurysm surgery: technical note, preliminary results, and review of the literature. J Neurosurg (In press). 16. Livesay JJ, Cooley DA, Ventemiglia RA, et al. Surgical experience in descending thoracic aneurysmectomy with and without adjuncts to avoid ischemia. Ann Thorac Surg 1985; 39: Doppman JL, DiChiro G, Glancy DL. Collateral circulation through dilated spinal cord arteries in aortic coarctation and extraspinal arteriovenous shunts. Chn Radiol 1969;20: Coles JG, Wilson GJ, Sima AF, et al. Intraoperative management of thoracic aortic aneurysm: experimental evaluation of perfusion cooling of the spinal cord. J Thorac Cardiovasc Surg 1983;85: Colon R, Frazier OH, Cooley DA, McAllister HA. Hypothermic regional perfusion for protection of the spinal cord during periods of ischemia. Ann Thorac Surg 1987;43: DISCUSSION Dr. Larry Hollier (New Orleans, La.). Paraplegia after thoracoabdominal aneurysm repair has been unpredictable and unpreventable despite the use of various adjunctive treatments. Intercostal artery reimplantation, however, from my viewpoint, remains vitally important in some patients. In my own practice I have always routinely attempted to reimplant all intercostal arteries if technically feasible. More recently, we have used cerebrospinal fluid drainage in addition to intercostal reimplantation. The additional use of cerebrospinal fluid drainage did not decrease the incidence of combined neurologic deficit as compared to routine reimplantation of intercostal vessels alone. However, in the cerebrospinal fluid drainage group, we saw no paraplegia, and no patient awoke with a deficit, but late onset paraparesis developed in three patients. However, the cohort of patients at high risk was small, and no aneurysms dissected in this group. Paraplegia and paraparesis appear to be the result of the interdependent variables of (1) the severity of spinal cord ischemia during cross-clamping, (2) the metabolic activity of the spinal cord neurons during ischemia, and (3) the postischemic reperfusion injury of oxygen-derived free radicals and of both direct and complement-mediated leukocyte injury. The critical element, however, is ischemia. Prolonged clamp times with inadequate collateral flow or failure to reimplant critical intercostal arteries will resuk in paraplegia. Preoperative identification of the critical intercostal arteries can facilitate rapid intercostal reimplantation and thus reduce cord ischemia time. This paper by Williams et al. supports the validity of this concept. Despite this technique, however, some ischemia is inevitable, and if enough metabolic byproducts are produced, reperfusion injury can lead to paraplegia or delayed onset paraparesis. If we hope to prevent paraplegia in humans, we should perhaps attempt to intervene in all three phases of injury at each operation: reducing cord ischemia, decreasing the

12 34 Williams et al. Journal of VASCULAR SURGERY metabolic activity of the cord, and minimizing reperfusion injury. I would like to ask the authors if such adjunctive therapy (lowering neuronal metabolic rate and inhibiting reperfusion injury) have been attempted during surgery. Also, in a significant number of patients one may be unable to angiographically identify the characteristic spinal arteries. In these patients, would you consider routine reimplantation of all patent intercostal arteries, or would you consider the use of deep hypothermia and circulatory arrest to increase safe ischemia time? Dr. Edward Kieffer (Paris, France). We have used preoperative spinal cord arteriography for the last 5 years in 112 patients undergoing elective surgery for aneurysms of the lower descending thoracic and thoracoabdominal aorta. We reported our early experience with our first 52 patients in 1989, in Annals of Vascular Surgery. I agree will Dr. Williams that preoperative spinal cord arteriography is a major advance in the management of these patients, and I share most of his conclusions. I would like, however, to stress a few differences in our experience. First, the artery of Adamkiewicz was visualized in 97 of 112 patients, or 86% in our series as opposed to 61% in his series. The reason for this important difference is not quite clear to me, and I would like to ask Dr. Williams to comment on that. Second, we have had two neurologic complications that were directly attributable to the arteriogram. One patient had an aortic dissection manifested 3 weeks earlier by transient paraparesis, which recurred after spinal cord arteriography. Another patient, whose aneurysm was diagnosed after blue toe syndrome and renal failure, had a shower of atheromatous emboli after prolonged and unsuccessful attempts at spinal cord arteriography. He died a few days later with ischemia of the lower extremities, renal failure, and paraplegia. Spinal cord arteriography cannot, therefore, be considered completely safe. We feel that the recent history of spinal cord ischemia or clinical microembolism should contraindicate, at least temporarily, spinal cord arteriography. Third, we have had no technical problems with separate reattachment of critical vessels in the mid portion of the aneurysm. We agree, however, that performance of this anastomosis increases the period of visceral ischemia. Fourth, I strongly feel that patients in whom critical arteries cannot be visualized are at high risk for postoperative neurologic complications. Fifth, Dr. Williams has not fully addressed the problem of the patency of these reattached arteries, and I wonder if he would comment on that. Did he perform routine postoperative arteriography on patients surviving the operations? Dr. Lars Svensson (Houston, Texas). The maportance of determining the spinal cord blood supply and reattaching it is clearly one of the important principles in trying to prevent paraplegia. The other principles include preventing ischemia during the period of aortic crossclamping, which is dependent on the extent of aneurysm, the available collateral vessels, and the length of time of cross-clamping. I think that a possible way of avoiding some of the problems of spinal angiography would be to localize the spinal cord blood supply during surgery. We have developed a technique whereby we insert under local anesthetic a catheter with a platinum electrode alongside the spinal cord. During aortic cross-clamping we divide the aorta into segments and inject hydrogen in solution into the occluded segments. By this technique we can determine which vessels supply the spinal cord. We can also insert hydrogen into the atriofemoral bypass pump to determine whether the pump is perfusing the spinal cord. At the end of the procedure we can test the vessels that have been reattached to see whether they are still patent and supplying the spinal cord--whether the reattachment was successful. We have been using this technique in patients with an average testing time during cross-clamping of 6 minutes, and we have found the information gained to valuable. I have three questions for Dr. Williams. First, in the clinical context how are you determining which of those vessels you identify as supplying the spinal cord should be reattached? Second, how do you reattach and prevent tearing of the reattached Carrel patch, particularly in the presence of dissection and especially in patients with Manfar syndrome? Third, did you perform postoperative arteriography to confirm successful reattachment of the identified vessels? We found postoperative angiography very enlightening in our studies using hydrogen for identification of the spinal cord blood supply since we observed occlusion of some reattached vessels. Dr. Williams. We have not tried to lower the metabolic rate of the spinal cord, but I think this is something that might well be the next step, particularly in the difficult group of patients requiring midgraft reattachrnent. To answer Dr. Kieffer and Dr. Hollier's question asking what should be done if you cannot find the blood supply--ignore it or reimplant it haphazardly, I would say this is perhaps a point of contention between us. It is clear that in many cases if you look at a CT scan, there is a thick peel of mural thrombus, and on aortic flush injections you see only two pairs of intercostal arteries. If you can successfully inject both of those, our assumption is that the blood supply is coming from the vertebral artery completely. This, in fact, worked in seven of ten patients. I think if we knew for sure which aortic segment supplied the spinal cord, this would certainly be another adjunct confirming the importance of the intercostal arteries originating from that segment. The problem with angiography is the problem of technical proficiency in cannulating these vessels, and we must rely on the angiographers and also tell them when to stop. Dr. Kieffer mentioned two complications, which were both reported in his paper. He has almost doubled the number of studies now, so he has learned that by not studying patients who have embolic showers to begin with,

13 Volume 13 Number 1 January 1991 Relationship of localization of spinal cord blood supply and paraplegia 35 you avoid problems subsequently. I assume from his report that he has had no complications confirming our experience in his last 50 patients. We have not done routine angiography of the intercostal vessels. I think probably only a quarter of the patients have had that. We have always used the hand-held Doppler held over the edge of the rib to make certain that the intercostal artery that we have implanted is in fact flowing. This, in fact, was not the case in one patient with a button anastomosis, and this required revision. I think all of the operative adjuncts that Drs. Svensson and Crawford have applied are very helpful, particularly as they tell us more about the mechanisms of these injuries. When we can define when this injury occurs and how it occurs, then I think we can further divide patients into groups of risk and use even more extraordinary techniques such as hypothermic arrest in the treatment of some of these terrible problems. THE E. J. WYLIE TRAVELING FELLOWSHIP OF THE EDUCATIONAL FOUNDATION OF THE SOCIETY FOR VASCULAR SURGERY The Educational Foundation of the Society for Vascular Surgery (with financial assistance from W. L. Gore & Associates, Inc.) has established an E. J. Wylie Traveling Fellowship. The purpose of the fellowship is to enable young surgeons to visit centers of excellence in vascular surgery in the United States and abroad. The benefits of educational travel for the maintenance and enhancement of excellence in the practice of vascular surgery are obvious. To be considered for selection a candidate must: 1. Be younger than 40 years of age at the time the traveling fellowship is awarded 2. Have completed a postgraduate vascular training program or have considerable experience in vascular surgery supplemental to general surgical training 3. Be committed to an academic career in vascular surgery and have obtained an academic appointment in a medical school or freestanding clinic devoted to excellence in medical education 4. Have a demonstrated record of success in pursuing clinical or basic science research sufficient to assure academic excellence in his or her pursuit of a career in vascular surgery Selection will be made without regard to the candidate's geographic location. A candidate submitting documentation for consideration for selection must furnish an upto-date curriculum vitae and a list of publications, research projects, current research support, and a list of the centers that he or she wishes to visit. Three letters of recommendation are required, including one from the Division Head and another from the Chairman of the Department of Surgery of the institution in which the candidate holds a faculty appointment. A 500-word essay describing the objectives of the candidate's travel plans and linking these to his or her career goals must be appended. The Travel Fellowship Award is $10,000, granted to one person for use during a time limit and for expenses of travel, research, and clerical help. Application for the Fellowship award shall be made in a letter containing the information and documents as detailed. The deadline for receiving applications is March 1, Letter of nomination or intent should be directed to: Ronald J. Stoney, M.D., F.A.C.S. Chairman, E. J. Wylie Traveling Fellowship Committee Division of Vascular Surgery University of California Medical Center 505 Parnassus Ave., M-488 San Francisco, CA 94143