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Ann Thorac Surg 2007;83:S865-S869
© 2007 The Society of Thoracic Surgeons

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Supplement

Spinal Cord Perfusion and Protection During Descending Thoracic and Thoracoabdominal Aortic Surgery: The Collateral Network Concept

Department of Cardiothoracic Surgery, Mount Sinai School of Medicine, New York, New York

^_* Address correspondence to Dr Griepp, Mt Sinai Medical Center, Cardiothoracic Surgery, 1 Gustave Levy Place, New York, NY 10029. (Email: ebgriepp{at}aol.com).

Presented at Aortic Surgery Symposium X, New York, NY, April 27–28, 2006.

	Abstract

Top Abstract Introduction Collateral Network Concept Minimizing the Effect of... Clinical Implications of the... Monitoring Spinal Cord Function Current Practice Implications for Endovascular... References

 
In the last two decades, as an increasing number of patients with descending thoracic and thoracoabdominal aneurysms are being diagnosed and treated, a more sophisticated understanding of spinal cord perfusion has become important in the attempt to minimize the frequency of spinal cord injury. The synthesis of information from laboratory studies and clinical experience has led to the collateral network concept, a framework for understanding spinal cord perfusion and thereby improving spinal cord protection during treatment of aneurysmal disease of the aorta distal to the left subclavian artery. Application of principles based on the collateral network concept has resulted in falling rates of spinal cord injury, which now approach 1% in descending thoracic aneurysm resection and less than 10% in extensive thoracoabdominal resections. These accomplishments suggest that, with further investigation, routine sacrifice of segmental aortic branches can be carried out in a way that will allow surgical and endovascular therapy of extensive distal aortic aneurysms without neurologic injury.

	Introduction

Top Abstract Introduction Collateral Network Concept Minimizing the Effect of... Clinical Implications of the... Monitoring Spinal Cord Function Current Practice Implications for Endovascular... References

 
Interest in the blood supply of the spinal cord dates back at least 130 years to the seminal anatomic studies of Adamkiewicz and the publication of his monograph [1]. He described the anterior and posterior spinal arteries, their anastomoses, and the major inputs into the blood supply of the spinal cord. The major cephalic inputs into spinal cord blood supply include the vertebral arteries and other branches of the subclavian and carotid arteries that reach the cord in its upper portion. The input to the central cord is from multiple segmental branches (the intercostal and lumbar arteries), including a large branch in the lower thoracic or upper abdominal aorta now designated as the artery of Adamkiewicz. The distal spinal cord and cauda equina are supplied primarily from the hypogastric arteries and their branches.

In the 1970s, in a series of dissections and vessel injections, Lazorthes and colleagues [2] expanded the observations of Adamkiewicz, detailing more precisely the multiple vessels contributing to spinal cord blood supply. They also described the multiple anastomotic pathways outside the spinal canal, including the peri-vertebral vessels and a rich collateral pathway involving the paraspinous muscles.

	Collateral Network Concept

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In the last two decades, as resection of the descending thoracic and thoracoabdominal aorta has become an important surgical discipline, a better appreciation and understanding of the anatomy and physiology of the spinal cord blood supply has emerged. A unifying hypothesis resulting from numerous laboratory and clinical observations is the collateral network concept, which can be characterized as follows:

1 There exists an axial network of small arteries in the spinal canal, in the perivertebral tissues, and in the paraspinous muscles that anastomose with one another and with the nutrient arteries of the spinal cord.

2 Inputs into this network include not only the segmental vessels but also the subclavian arteries and the hypogastric arteries and their branches.

3 This network can increase cord nutrient flow from one source when another is reduced. Contrariwise, cord nutrient flow can be reduced if an alternate low resistance pathway is opened; that is, steal can occur. Examples of steal include back bleeding of intercostals into an open excluded aortic segment or unperfused iliac or visceral vessels secondary to aortic cross-clamping, and pharmacologically induced arteriovenous shunting such as that resulting from use of nitroprusside.

The importance of extrasegmental vessels for inflow into the spinal cord has been demonstrated in a number of laboratory studies. Christiansson and colleagues [3] demonstrated that oxygen tension in the intrathecal space could be maintained in a viable range without development of progressive intrathecal acidosis after ligating all segmental arteries in the pig. Clamping the subclavian arteries in addition, however, resulted in a decrease of PO ₂ to zero and prompt appearance of acidosis.

Using motor evoked potentials (MEP) to monitor spinal cord function, Strauch and colleagues [4] showed in the pig that the number of segmental vessels that could safely be ligated was decreased substantially if either the subclavian or the median sacral artery—which corresponds to the hypogastric artery in man—were ligated. Biglioli and colleagues [5] have demonstrated the collateral network in man with cadaver dye injections.

The potential flow away from the spinal cord—steal—was documented by Christiansson and colleagues [3], who demonstrated retrograde flow of intercostal vessels into the distal aorta after aortic cross-clamping. It is an almost invariable clinical observation that opening an excluded segment of thoracic and thoracoabdominal aorta will reveal very substantial back bleeding from intercostal arteries into the open aortic segment.

Measures to minimize steal have been clinically demonstrated to contribute to the prevention of spinal cord ischemia and are considered to be an important aspect of safe thoracoabdominal aortic resection in the experience of a number of surgical groups. Borst and colleagues [6] introduced the idea of preventing steal by rapidly inserting occlusive pegs into back-bleeding intercostal arteries after opening the aneurysm. Acher and Wynn [7] emphasized the importance of prompt intraaortic ligation of back-bleeding segmental vessels. Cambria and colleagues [8] prevented back bleeding with the use of balloons and tourniquets. And we, for the past 13 years, have clamped and divided segmental vessels entering the aorta in the segment to be excised before cross-clamping or opening the aorta [9].

In our most recently reported series of 100 cases of thoracic and thoracoabdominal aortic resection, in which segmental vessels were ligated before opening the aorta, the incidence of paraplegia was 2% [10]. Of these patients, 32 had descending thoracic aneurysms, and 68 had thoracoabdominal aneurysms. The extent of segmental artery sacrifice, corresponding to the extent of the aneurysm, is shown in Fig 1, which indicates those who died and the 2 patients who sustained postoperative paraplegia. An average of 8.0 ± 2.5 segmental artery pairs were sacrificed, including an average of 4.5 ± 2.1 segmental pairs between T7 and L1 (shaded area), where the artery of Adamkiewicz is presumed to arise.

View larger version (55K): [in this window] [in a new window]   Fig 1. This figure displays, in chronologic order, the extent of segmental artery sacrifice in each of 100 patients operated on from October 2002 to December 2004. *The patients who died. **Patients who sustained paraplegia. The shaded area corresponds to segmental pairs between T7 and L1. (Reprinted from Etz CD, et al. Thoracic and thoracoabdominal aneurysm repair: is reimplantation of spinal cord arteries a waste of time? Ann Thorac Surg 2006;82:1670–7 [10], with permission.)

	Minimizing the Effect of Unavoidable Intraoperative Temporary Spinal Cord Ischemia

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Moderate passive hypothermia (32° to 34°C) has been found to be clinically effective by a number of surgeons, and we have documented in our laboratory that a reduction in temperature of only 5°C increases the tolerable ischemic interval in the pig from 20 to 50 minutes, a 2.5-fold increase [13]. Longer ischemic intervals can be tolerated at lower temperatures, as evidenced by Kouchoukos and colleagues’ [14] experience with profound hypothermic circulatory arrest for the treatment of thoracoabdominal aortic aneurysm as well as experience with selective cerebral perfusion for arch replacement, where ischemic intervals to the lower body of up to 2 hours at temperatures of 15°C result in routine survival of normal spinal cord function [15]. Almost all aortic surgeons now use at least moderate hypothermia for resection of descending thoracic and thoracoabdominal aneurysms. In addition, a few surgeons have found regional cooling of the spinal cord by infusion of cold saline into the intrathecal space to be effective [8].

	Clinical Implications of the Collateral Network Concept

Top Abstract Introduction Collateral Network Concept Minimizing the Effect of... Clinical Implications of the... Monitoring Spinal Cord Function Current Practice Implications for Endovascular... References

 
It has become evident that careful attention to perfusion variables is important to provide adequate blood flow based on the collateral network. This is critical to postoperative care after aneurysm resection. Arterial pressures in the high physiologic range have been adopted by almost all aortic surgeons. In addition, reduction of resistance to flow in the spinal cord is optimized with drainage of cerebrospinal fluid (CSF) to maintain an intrathecal pressure of 10 cm H₂O or less [16].

Experimental observations suggest that maintenance of adequate spinal cord blood flow is especially critical in the early postoperative period after aneurysm resection when the spinal cord is recovering from its intraoperative ischemic insult. We have demonstrated in the animal laboratory the tremendous capacity of the normal blood supply to the cord to dilate in response to ischemic stress. Increases in spinal cord blood flow up to eightfold can be demonstrated after restoration of perfusion after 20 minutes of normothermic cross-clamping.

If the normal physiologic response to intraoperative spinal cord ischemia involves a period of marked hyperemia during recovery, the absence of segmental artery contribution to the blood supply of the spinal cord after aneurysm resection poses an especially daunting challenge, rendering the cord particularly vulnerable to additional ischemia in the initial postoperative hours and days during which the collateral circulation is providing the major portion of spinal cord perfusion. Maximization and stability of hemodynamic parameters is mandatory during this vulnerable postoperative interval, including continued CSF drainage. Monitoring of spinal cord function to detect onset of potentially reversible delayed paraplegia should be continued initially by means of evoked potential monitoring and then by assessing functional status directly.

The recognition that an important source of blood supply to the spinal cord comes from the hypogastric arteries provides a physiologic explanation for the clinical observation that perfusion of the distal aorta—particularly the hypogastrics—reduces the rate of paraplegia after thoracoabdominal resection. Two recent publications have documented the efficacy of distal perfusion in reducing paraplegia following resection of extensive thoracoabdominal aortic aneurysms [17, 18].

	Monitoring Spinal Cord Function

Top Abstract Introduction Collateral Network Concept Minimizing the Effect of... Clinical Implications of the... Monitoring Spinal Cord Function Current Practice Implications for Endovascular... References

 
Surgeons who use monitoring of spinal cord function during the resection of thoracic and thoracoabdominal aneurysms believe it reduces the risk of neurologic injury, although it has not yet reached the threshold of standard practice. Somatosensory evoked potentials (SSEP) monitoring has been routine in several centers since the early 1990s [19]. Although they monitor sensory and not motor pathways, and usually do not respond as quickly to cord ischemia as MEPs and SSEPs can be used postoperatively until the patient is fully awake.

In the last decade, a number of investigators have concluded that to provide a sensitive and rapidly responsive indication of spinal cord ischemia during the surgical procedure, MEP monitoring should be used [10, 20]. In most cases, cord ischemia, detected by MEPs or SSEPs or both, during the surgical procedure can be corrected with manipulation of the hemodynamics, particularly by raising the arterial pressure. Some surgeons have also found that MEP monitoring coupled with provocative maneuvers to induce spinal cord ischemia is effective in identifying segmental vessels that may be of critical importance in providing inflow into the collateral network [20].

	Current Practice

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Current strategies for avoiding spinal cord injury are based on the recognition of the dual causes of spinal cord injury resulting from resection of thoracic and thoracoabdominal aneurysms: unavoidable intervals of temporary cord ischemia during surgical procedures, and more permanent injury and lasting ischemia resulting from the failure to provide an adequate blood supply to the cord in the perioperative and postoperative period. Our understanding of spinal cord ischemia has been enhanced by an appreciation of the collateral network concept of spinal cord blood supply and recognition of the unequivocal protective effects of hypothermia on neural tissue.

A consensus is gradually emerging on optimal surgical technique for spinal cord protection. The various approaches can be divided into two groups: techniques that are widely used and whose efficacy is based on unequivocal laboratory or clinical data, and other techniques that are used by a number of experienced surgeons although their efficacy has not been unequivocally demonstrated in the laboratory or in prospective clinical studies.

The first group of techniques includes use of distal perfusion, as much hypothermia as is consistent with the conduct of the operative procedure, prevention of steal from the collateral network, and maximization of perfusion parameters.

Distal perfusion can be provided with or without an oxygenator. Commonly, inflow into the bypass circuit is through the pulmonary vein, or through the right atrium accessed from the femoral vein with echo-guided wire-directed cannulation. Inflow into the distal aorta is most commonly from the femoral artery, but also can be directly into the distal aorta or into the side branch of a graft after performing an open distal anastomosis. Monitoring of lower body blood pressure is necessary to optimize cord perfusion. Surprisingly large flow rates are frequently needed—as high as 3 or 3.5 liters even at moderately hypothermic levels—if mean arterial pressure is to be maintained at 80 to 100 mm Hg.

Passive hypothermia has been found to be very safe, notwithstanding the concern that ventricular fibrillation would be a frequent complication [21]. There is widespread acceptance that a body temperature of 32°C is perfectly safe, and we have found temperatures as low as 29°C to be free of cardiac complications. In a number of surgical situations, profound hypothermia with cardiopulmonary bypass—to enable an open proximal anastomosis to the aortic arch—provides superb cord protection, and as has been noted, intervals of up to 2 hours of cord ischemia are probably well tolerated under these circumstances. As surgeons become comfortable with the use of profound hypothermia, this technique, as advocated by Kouchoukos and colleagues, will probably be used in an increasing number of thoracoabdominal resections.

The prevention of steal from the collateral network that supplies the spinal cord can be achieved from within the open aorta by occluding the segmental vessels with pegs, balloons, or tourniquets, oversewing back-bleeding vessels promptly, or clipping the vessels externally. Steal into the distal circulation is prevented by distal perfusion.

Perfusion through the collateral network is undoubtedly enhanced by high perfusion pressures. Most surgeons now insist that mean arterial pressures be maintained at least at 80 mm Hg and perhaps as high as 90 to 100 mm Hg during the operative procedure, with possible exceptions during periods of clamping a friable aorta. Oxygen delivery is maximized with maintenance of normal hematocrit levels and careful attention to ventilation so that PO ₂ is normal. CSF drainage has been demonstrated in several prospective studies to add significantly to spinal cord protection and is used by most surgeons intraoperatively and postoperatively to minimize resistance to inflow of blood into the intrathecal space [16].

The techniques for spinal cord protection in the second group are widely used, although their efficacy has never been convincingly demonstrated in clinical studies. This category includes the use of drugs, principally corticosteroids, mannitol, and naloxone.

Intraoperative spinal cord monitoring with SSEP and MEP is thought by many surgeons to represent a substantial advance in the resection of thoracic and thoracoabdominal aortic aneurysms and is currently the only technique that allows detection of intraoperative spinal cord ischemia in time to treat it. Nonetheless, there have been no prospective studies demonstrating its efficacy in reducing the incidence of spinal cord injury.

Finally, most aortic surgeons believe that routine implantation of segmental vessels will reduce the incidence of spinal cord injury. This would appear to be physiologically sensible; however, implantation of segmental vessels may complicate the operative procedure and lengthen the period of unavoidable intraoperative ischemia. Thus, a second group of aortic surgeons believe that implantation of segmental vessels has not been convincingly demonstrated to be beneficial.

	Implications for Endovascular Treatment

Top Abstract Introduction Collateral Network Concept Minimizing the Effect of... Clinical Implications of the... Monitoring Spinal Cord Function Current Practice Implications for Endovascular... References

 
It seems quite clear that for the foreseeable future, endovascular treatment of thoracic and thoracoabdominal aortic aneurysms will usually preclude segmental vessels within the stented segment from contributing to spinal cord blood supply. In patients treated with endovascular grafts, there are probably other factors that cause spinal cord injury in addition to the threats to spinal cord viability posed by open surgical resection. This may account for paraplegia rates that appear to be no lower after endovascular repair than after open resection of aneurysms of comparable extent.

Stent grafts result in sudden complete occlusion of a large number of segmental vessels, and this occurs at relatively normothermic temperatures. A unique threat is the risk of dislodging thrombotic or atheromatous debris into segmental vessels, resulting in distal embolization to small end vessels within the cord, where the opportunity for collateralization does not exist. Finally, steal from the collateral network via retrograde flow via segmental vessels into visceral vessels communicating with the excluded aneurysmal sac—for example, the celiac axis—could theoretically also cause cord ischemia.

These additional possible mechanisms of spinal cord injury may at present be offsetting the obvious benefits of endovascular procedures, such as the absence of any significant period of aortic occlusion and reduction of hemodynamic instability both during the procedure and in the postoperative period. A recent review found a 2.7% incidence of spinal cord injury after endovascular repair of all or a portion of the descending thoracic aorta, which is certainly no better—and perhaps worse—than current results of open aneurysm resection in experienced hands [22].

In summary, we have improved our understanding of spinal cord perfusion and protection substantially within the last decade. The application of techniques that have evolved empirically, but whose mechanisms of action are becoming understandable in terms of the collateral network concept, has had a major impact on rates of neurologic injury. Paraplegia/paraparesis rates are approaching 1% for descending thoracic aneurysm resection and 5% to 10% for thoracoabdominal aneurysm resection in contemporary series. It seems quite conceivable, with continuing evolution of knowledge and technology, that routine sacrifice of all intercostal and lumbar vessels will be possible without spinal cord injury. This is an essential requirement for endovascular therapy of the thoracic and thoracoabdominal aorta to achieve its full potential.

	References

Top Abstract Introduction Collateral Network Concept Minimizing the Effect of... Clinical Implications of the... Monitoring Spinal Cord Function Current Practice Implications for Endovascular... References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Randall B. Griepp Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Griepp, R. B. Articles by Griepp, E. B. Search for Related Content PubMed PubMed Citation Articles by Griepp, R. B. Articles by Griepp, E. B. Related Collections Great vessels