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Tex Heart Inst J. 2010; 37(6): 672–674.
PMCID: PMC3014112

The Collateral Network Concept

Minimizing Paraplegia Secondary to Thoracoabdominal Aortic Aneurysm Resection
Joseph S. Coselli, MD, Section Editor

In the quest to minimize the occurrence of spinal cord injury (SCI) secondary to resection of descending thoracic and thoracoabdominal aortic aneurysms (TAAA), we have undertaken a reevaluation of the anatomy and physiology of the circulation to the spinal cord. To this end, we have performed descriptive and morphometric anatomic studies in pigs, both in the native state and at various times after extensive segmental artery (SA) ligation.1,2 We have also monitored the pressure in the distal stump of lumbar arteries after extensive SA resection using various experimental protocols in pigs, and have monitored distal lumbar artery pressure in patients during and after extensive TAAA resection.3,4

These anatomic and physiologic studies have shown unequivocally the existence of an extensive collateral network of vessels that supply the spinal cord, as well as the adjacent paraspinous muscles. This network has been revealed as a dynamic entity that adapts to the elimination of direct SA input—resulting from simulated experimental or clinical aneurysm resection—by a process of remodeling to maintain spinal cord viability and to guard against the development of subsequent SCI. We have termed this new understanding of the spinal cord blood supply and its adaptations the Collateral Network Concept.

Anatomic Studies

Vascular casts of the collateral network that supplies the spinal cord in young pigs—obtained via aortic infusions of methylmethacrylate—have revealed that the anterior spinal artery and a series of interconnected epidural arcades constitute only a small fraction of the total volume of the massive collateral network that includes the SAs. Most of the vessels lie within and supply the paravertebral muscles, as shown in Figure 1.1 After experimental SA ligation, there is an early increase in the size of the anterior spinal artery—likely due to vasodilation—followed by a definite increase in the number and density and size of small arterioles, as well as a change in their orientation. These changes enable flow from both cranial and caudal directions—from the subclavian and hypogastric arteries—to the area of the spinal cord that has been deprived of direct SA input.

figure 16FF1
Fig. 1 Anatomy of the collateral network: A) dorsal view and B) axial view of a pair of segmental vessels at L1; the spinous process of the vertebra has been removed.

Pressure Monitoring

After serial ligation of all the SAs—the intercostal and lumbar arteries from T4 to L5—the pressures in the collateral network can be monitored using a catheter in the distal stump of a ligated SA (Fig. 2).2

figure 16FF2
Fig. 2 Collateral network pressure (CNP) measured in L1. The significant diminution of the drop in collateral network pressure when the segmental arteries are taken in 2 stages, compared with a single stage, is evident in both graphs.

If all the SAs are serially ligated during a single procedure, the collateral network pressure falls to about 35% of baseline; then it begins to recover within 24 to 48 hours, reliably reaching baseline levels 5 days after SA ligation. Approximately 50% of the pigs will exhibit paraplegia or paraparesis after such extensive SA ligation in a single stage.

If SA ligation of equivalent extent is carried out in 2 stages 7 days apart, however, the drop in the collateral network pressure is much less pronounced, and the recovery of this pressure to baseline levels is more rapid. This correlates with much better functional recovery: evidence of spinal cord ischemia is rare. Avoidance of SCI after a 2-stage protocol is dramatically better than after extensive single-stage SA ligation, regardless of whether the 1st-stage ligation was thoracic or lumbar.

Insertion of a catheter to measure collateral network pressure in patients during TAAA resection has also proved feasible (Fig. 3),5 and such monitoring is valuable postoperatively to prevent the development of SCI. Several clinical studies have shown that an accurate evaluation of spinal cord perfusion pressure must take into account the level of systemic arterial pressure that has prevailed before surgery, and also the cerebrospinal fluid pressure or central venous pressure. Patients with antecedent hypertension require a higher perfusion pressure than do normotensive patients, and a high central venous pressure is a risk factor for the development of spinal cord ischemia.5

figure 16FF3
Fig. 3 Technique for placement of an L1 catheter to measure collateral network pressure in a patient at the time of thoracoabdominal resection. When the catheter is withdrawn postoperatively, the silastic ligatures close the vessel.

Clinical Implications of the Collateral Network Concept

The studies documenting the presence and responsiveness of the collateral vascular network surrounding the spinal cord have provided additional evidence to reaffirm a number of recommendations to minimize paraplegia secondary to extensive resection of descending thoracic aneurysms and TAAAs. The Collateral Network Concept reaffirms the importance of the integrity of the hypogastric and subclavian arteries when extensive SA sacrifice is likely to be required. The importance of maintaining high systemic pressure and low cerebrospinal fluid pressure and central venous pressure intraoperatively and postoperatively is justified by their impact upon the directly measured collateral network pressure. Scrupulous intraoperative attention to maintaining perfusion pressure in the aorta proximal and distal to the resected aortic segment is important, as is preventing steal from back-bleeding of open SAs. It is also important to maintain stable postoperative hemodynamics from the time of surgery until restoration of the preoperative collateral network pressure secondary to vasodilation and remodeling of the vascular network; this requires a maximum of 72 to 120 hours after extensive SA resection.

Mitigating the impact of reduced SA inflow by dividing extensive aneurysm resection into 2 stages reduces the incidence of spinal cord ischemia both experimentally and clinically. The fact that paraplegia is very uncommon if extensive aneurysm resection is divided into 2 stages—without reimplantation of any intercostal or lumbar arteries—makes the use of endografts for extensive aneurysm repair seem increasingly realistic in the future.

Footnotes

Address for reprints: Randall B. Griepp, MD, Department of Cardiothoracic Surgery, Mount Sinai School of Medicine, Annenberg 7–54, Box 1028, One Gustav Levy Place, New York, NY 10029

E-mail: gro.ianistnuom@ppeirG.lladnaR

Presented at the Joint Session of the Denton A. Cooley Cardiovascular Surgical Society and the Michael E. DeBakey International Surgical Society; Austin, Texas, 10–13 June 2010

References

1. Etz CD, Kari FA, Mueller CS, Silovitz D, Brenner R, Lin HM, Griepp RB. The collateral network concept: a reassessment of the anatomy of spinal cord perfusion. J Thorac Cardiovasc Surg. In press. [PMC free article] [PubMed]
2. Etz CD, Kari FA, Mueller CS, Brenner R, Lin HM, Griepp RB. Remodeling of the arterial collateral network after segmental artery sacrifice. J Thorac Cardiovasc Surg. In press. [PMC free article] [PubMed]
3. Etz CD, Di Luozzo G, Zoli S, Lazala R, Plestis KA, Bodian CA, Griepp RB. Direct spinal cord perfusion pressure monitoring in extensive distal aortic aneurysm repair. Ann Thorac Surg 2009;87(6):1764–74. [PubMed]
4. Etz CD, Zoli S, Mueller CS, Bodian CA, Di Luozzo G, Lazala R, et al. Staged repair significantly reduces paraplegia rate after extensive thoracoabdominal aortic aneurysm repair. J Thorac Cardiovasc Surg 2010;139(6);1464–72. [PubMed]
5. Etz CD, Zoli S, Bischoff MS, Bodian CA, Di Luozzo G, Griepp RB. Measuring the collateral collateral network pressure to minimize paraplegia risk in thoracoabdominal aneurysm resection. J Thorac Cardiovasc Surg. In press. [PubMed]

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