Collateral Network Concept Research Articles

Collateral network concept in 2023.

Extensive thoracoabdominal aortic aneurysm repair can cause spinal cord ischemia which significantly impacts survival and quality of life. Although this complication is uncommon, it is important to recognize the pathophysiology and preventative measures. In the 1990s, Dr. Griepp and colleagues proposed the existence of an extensive collateral network that supports spinal cord perfusion, "the collateral network concept". This includes an interconnecting complex of vessels in the intraspinal, paraspinous, and epidural spaces, and in the paravertebral muscles, involving the intercostal and lumbar segmental arteries as well as the subclavian and hypogastric (iliac) arteries. In this concept, as opposed to the one major segmental input model such as the Adamkiewicz artery, recognition of the importance of multiple inputs to the spinal circulation is paramount to maintaining the spinal blood flow and preventing spinal cord ischemia. In this article, we review the current evidence of the collateral concept and its application in aortic surgery.

Collateral network concept and spinal cord protection.

Collateral network concept and spinal cord protection.

Surgical technique for preservation of extrathoracic collateral networks in thoracoabdominal aortic surgery.

Surgical technique for preservation of extrathoracic collateral networks in thoracoabdominal aortic surgery.

Spinal cord injury in endovascular thoracoabdominal aortic aneurysm repair: prevalence, risk factors and preventive strategies.

Thoracoabdominal aortic aneurysms are among the most challenging pathologic conditions vascular surgeons have to face. Endovascular treatment brought the prospect of being able to treat these complex aneurysms with less invasiveness and recent outcomes already challenge those of open repair. Plus, this technique offers a therapeutic option for patients who had none, due to significant comorbidities limiting open repair. Spinal cord injury is a major complication after complex aneurysm repair that dramatically affects patient's quality of life, even if technical success - aneurysm exclusion from circulation - has been achieved. Several strategies to prevent this terrible outcome have been developed, with remarkable success in narrowing down the number of patients who will suffer this complication. This comprehensive review covers how the standard of care for thoracoabdominal aortic aneurysms has evolved over time, how the understanding of spinal cord perfusion has changed in light of the collateral network concept, the risk factors associated with SCI, and details preventive strategies applied in current practice to lessen even further the frequency of spinal cord injury. Strategies covered go from the traditional adjuncts comprising hemodynamic control, neuroprotective drugs, neuromonitoring and cerebrospinal fluid drainage to emerging and innovative techniques such as near-infrared spectroscopy, two-step repair, minimally-invasive selective segmental artery coil-embolization, temporary aneurysm sac perfusion, and techniques for earlier pelvic and lower limb reperfusion.

Strategies to prevent TEVAR-related spinal cord ischemia.

Spinal cord ischemia remains the Achilles' heel of thoracic and thoracoabdominal diseases management. Great improvements in morbidity and mortality have been obtained with the endovascular approach TEVAR (Thoracic Endovascular Aortic Repair) but this devastating complication continues to severely affect the quality of life, even if the primary success of the procedure - dissection/aneurysm exclusion - has been achieved. Several strategies to deal with this complication have been published in the literature over the time. Knowledge and technology have been evolving from identification of the risk factors associated with spinal cord ischemia, including lessons learned from open surgery, and from developments in the collateral network concept for spinal cord perfusion. In this comprehensive review, the authors cover several topics from the traditional measures comprising haemodynamic control, cerebrospinal drainage and neuroprotective drugs, to the staged-procedures approach, the emerging MISACE (minimally invasive selective segmental artery coil-embolization) and innovative neurologic monitoring such as NIRS (near-infrared spectroscopy) of the collateral network.

Invited Commentary

German researchers have always been very fond of enigmata. They even called one of the most sophisticated encrypting machines ever simply “Enigma.” It was first patented in 1918 and was used widely during the Second World War until its code system was finally broken at Bletchley Park [1Hinsley F.H. Stripp A. Codebreakers: The Inside Story of Bletchley Park. Oxford University Press, Oxford, UK1993Google Scholar]. One enigma still unsolved 70 years later is the blood supply of the spinal cord and its protection during operations on the thoracic or thoracoabdominal aorta. Interestingly enough, the crucial steps to understand both the Enigma machine and spinal cord blood supply were taken by Poles: Marian Rejewski and Albert Adamkiewicz, respectively. Pig models have been used for a long time for further understanding, despite of some basic anatomic differences [2Wadouh F. Arndt C.F. Metzger H. Hartmann M. Wadouh R. Borst H.G. Direct measurements of oxygen tension on the spinal cord surface of pigs after occlusion of the descending aorta.J Thorac Cardovasc Surg. 1985; 89: 787-794PubMed Google Scholar, 3Etz C.D. Kari F.A. Mueller C.S. et al.The collateral network concept: a reassessment of the anatomy of spinal cord perfusion.J Thorac Cardiovasc Surg. 2011; 141: 1020-1028Abstract Full Text Full Text PDF PubMed Scopus (212) Google Scholar]. An academic debate regarding the role of the so-called artery of Adamkiewicz [4Adamkiewicz A. Die Blutgefässe des menschlichen Rückenmarkes I: Die Gefässe der Rückenmarkssubstanz. Sitzungsberichte der kais. Akademie der Wissenschaften zu Wien.Math Naturwissenschaftl Classe. 1881; 84: 469-502Google Scholar, 5Adamkiewicz A. Die Blutgefässe des menschlichen Rückenmarkes II: Die Gefässe der Rückenmarlsoberfläche. Sitzungsberichte der kais. Akademie der Wissenschaften zu Wien.Math Naturwissenschaftl Classe. 1882; 85: 101-130Google Scholar] has been ongoing, including the respective protective approaches derived from the defended opinion [6Wadouh F. Arndt C.F. Oppermann E. Borst H.G. Wadouh R. The mechanism of spinal cord injury after simple and double aortic cross-clamping.J Thorac Cardiovasc Surg. 1986; 92: 121-127PubMed Google Scholar, 7Griepp R.B. Ergin M.A. Galla J.D. et al.Looking for the artery of Adamkiewicz: a quest to minimize paraplegia after operations for aneurysms of the descending thoracic and thoracoabdominal aorta.J Thorac Cardiovasc Surg. 1996; 112: 1202-1215Abstract Full Text Full Text PDF PubMed Scopus (247) Google Scholar, 8Heinemann M.K. Brassel F. Herzog T. Dresler C. Becker H. Borst H.G. The role of spinal angiography in thoracic aortic surgery: myth or reality?.Ann Thorac Surg. 1998; 65: 346-351Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar]. Now, Haldenwang and colleagues have applied the porcine model to simulate modern surgical strategies [9Haldenwang P.L. Prochnow N. Baumann A. et al.Spinal cord ischemia after selective cerebral perfusion in a porcine “frozen elephant trunk” simulation model.Ann Thorac Surg. 2015; 99: 1624-1631Google Scholar]. Given the background of the previous studies, it is not so surprising that the lower (lumbar) regions were more susceptible to ischemic damage even after indirect (selective cerebral) perfusion at moderate hypothermia (28°C). Some perfusion is probably almost always better than none, and the colder the better is still valid for tissue protection. This report nicely shows that even seemingly less invasive techniques such as endovascular stent-grafting are still troubled by one of the most enigmatic enigmata in medicine. Definitive deciphering is still bound to take a while, and it is to be hoped that this group will continue its valuable research. Spinal Cord Ischemia After Selective Cerebral Perfusion in a Porcine “Frozen Elephant Trunk” Simulation ModelThe Annals of Thoracic SurgeryVol. 99Issue 5PreviewThe “frozen elephant trunk” procedure (FET) represents the therapy of choice for extended aortic diseases. The aim of our study was to analyze whether 90 minutes of selective cerebral perfusion (SCP) at 28°C followed by permanent occlusion of the thoracic segmental arteries (TSA) would cause spinal cord ischemia in a porcine model. Full-Text PDF

Significance and function of different spinal collateral compartments following thoracic aortic surgery: immediate versus long-term flow compensation

Iatrogenic paraplegia has been accompanying cardiovascular surgery since its beginning. As a result, surgeons have been developing many theories about the exact mechanisms of this devastating complication. Thus, the impact of single arteries that contribute to the spinal perfusion is one of the most discussed subjects in modern surgery. The subsequent decision of reattachment or the permanent disconnection of these intercostal arteries divides the surgical community. On the one hand, the anatomical or vascular approach pleads for the immediate reimplantation to reconstruct the anatomical situation. On the other hand, the decision of the permanent disconnection aims at avoiding stealing phenomenon away from the spinal vascular network. This spinal collateral network can be described as consisting of three components-the intraspinal and two paraspinal compartments-that feed the nutrient arteries of the spinal cord. The exact functional impact of the different compartments of the collateral network remains poorly understood. In this review, the function of the intraspinal compartment in the context of collateral network principle as an immediate emergency backup system is described. The exact structure and architectural principles of the intraspinal compartment are described. The critical parameters with regard to the risk of postoperative spinal cord ischaemia are the number of anterior radiculomedullary arteries (ARMAs) and the distance between them in relation to the longitudinal extent of aortic disease. The paraspinal network as a sleeping reserve is proposed as the long-term backup system. This sleeping reserve has to be activated by arteriogenic stimuli. These are presented briefly, and prior findings regarding arteriogenesis are discussed in the light of the collateral network concept. Finally, the role of preoperative visualization of the ARMAs in order to evaluate the risk of postoperative paraplegia is emphasized.

Das zweizeitige Vorgehen zur Reduktion der spinalen Ischämie bei der Ausschaltung thorakoabdomineller Aortenaneurysmen - eine Übersicht

The spinal cord is particularly susceptible to ischaemic injury following repair of extensive descending thoracic and thoracoabdominal aortic aneurysms (TAAA). For the past decade, the Mount Sinai group in New York has intensively studied the anatomy of the extensive vascular network surrounding the spinal cord, as well as its dynamic morphology in response to decreased blood pressure and flow. Along with clinical data, experimental findings gave rise to the Collateral Network Concept, by which spinal cord injury in open TAAA repair can be significantly reduced. With the more recent widespread use of endovascular repair, strategies to prevent ischaemic spinal cord damage after extensive segmental artery sacrifice/occlusion are still evolving. The hypothesis that dividing extensive aneurysm repair into two steps may mitigate the impact of diminished blood flow to the collateral network has led to a recently conducted series of staged repair experiments. By exploiting the resources of the collateral network, spinal cord injury could be minimised in staged open, as well as in staged hybrid repair and seems equally adoptable for endovascular procedures. The contribution presented herein provides an overview of clinical and experimental studies on the staged approach. Furthermore, it briefly assesses the anatomic rationale for the collateral network concept.

Staged approach for spinal cord protection in hybrid thoracoabdominal aortic aneurysm repair.

At present, there are three available options for surgical thoracoabdominal aortic aneurysm (TAAA) repair: conventional open surgery, total endovascular repair, and a hybrid approach, involving conventional surgical and endovascular techniques. Each modality has a different risk/benefit profile, requiring careful patient selection. Spinal cord injury (SCI) due to compromised blood supply following extensive segmental artery (SA) sacrifice is a daunting complication observed with all three approaches. A thorough understanding of the response of the spinal cord vasculature to SA sacrifice is essential to minimize the incidence of SCI after open or endovascular repair of TAAA. For over a decade, perioperative spinal cord protection during TAAA repair has been investigated in Dr. Griepp’s laboratory at The Mount Sinai Hospital in New York. Clinical and experimental work have provided insight into the anatomy of the extensive vascular network surrounding the spinal cord, and its dynamic response to SA sacrifice. This new understanding of spinal cord perfusion has been termed the Collateral Network Concept (CNC) (1).

Open surgical repair of thoracoabdominal aneurysms - the Massachusetts General Hospital experience.

The modern era of surgical management of thoracoabdominal aneurysms (TAA) began with the pioneering work of E. Stanley Crawford (1); this benchmark series reported an operative mortality of 10% with an incidence of spinal cord ischemia (SCI) of 16%, some 50% of which were total paraplegia. Over a 20 year period until 2006, TAA repair at our institution (2) was predominantly performed using a simplified clamp and sew approach in accordance with Dr. Crawford’s teachings which emphasized operative expediency and technical efficiency (2). Management of TAA during this time was typically performed without use of distal perfusion techniques. Adjunct use included routine cerebrospinal fluid (CSF) drainage (3,4), aggressive intercostal re-implantation (3,5,6), regional hypothermia for spinal cord protection (7,8), infusion of hypothermic renal preservation fluid for prevention of renal failure, and in-line mesenteric shunting (9) to reduce complications resulting from visceral ischemia. Using this approach we achieved favorable results with an overall operative mortality of 8% (6% elective and 13% urgent) with significant SCI in 8% of patients (2). Largely driven by the apparent failure of epidural cooling to drive SCI to less than 5%, we modified operative management of TAA in recent years in an effort to further reduce spinal cord complications. As our experience has shown (10) that patients with type IV TAA can safely be managed with a simplified clamp/sew approach with favorable results, this evolution in operative strategy has been exclusively implemented in management of patients with extents I-III TAA. In essence the rationale exploited the collateral network concept (11-13): we adopted routine use of distal aortic perfusion (DAP) via left atrial to femoral bypass to support the collateral circulation to the spinal cord during the period of aortic cross clamp application. Additionally, intra-operative motor evoked potential (MEP) monitoring (14,15) has afforded the ability to dynamically assess spinal cord ischemia during aneurysm reconstruction. As a result, we have abandoned aggressive intercostal re-implantation in favor of a selective MEP driven re-implantation strategy. Clinical outcomes resulting from this evolution in operative strategy for extents I-III TAA have recently been published and are further highlighted herein (16).

The collateral network concept: Remodeling of the arterial collateral network after experimental segmental artery sacrifice

A comprehensive strategy to prevent paraplegia after open surgical or endovascular repair of thoracoabdominal aortic aneurysms requires a thorough understanding of the response of the collateral network to extensive segmental artery sacrifice. Ten Yorkshire pigs underwent perfusion with a low-viscosity acrylic resin. With the use of cardiopulmonary bypass, 2 animals each were perfused in the native state and immediately, 6 hours, 24 hours, and 5 days after sacrifice of all segmental arteries (T4-L5). After digestion of surrounding tissue, the vascular cast of the collateral network underwent analysis of arterial and arteriolar diameters and the density and spatial orientation of the vasculature using light and scanning electron microscopy. Within 24 hours, the diameter of the anterior spinal artery had increased significantly, and within 5 days the anterior spinal artery and the epidural arterial network had enlarged in diameter by 80% to 100% (P < .0001). By 5 days, the density of the intramuscular paraspinous vessels had increased (P < .0001), a shift of size distribution from small to larger arterioles was seen (P = .0002), and a significant realignment of arterioles parallel to the spinal cord had occurred (P = .0005). Within 5 days after segmental artery occlusion, profound anatomic alterations in the intraspinal and paraspinous arteries and arterioles occurred, providing the anatomic substrate for preservation of spinal cord blood flow via collateral pathways.

The collateral network concept: A reassessment of the anatomy of spinal cord perfusion

Prevention of paraplegia after repair of thoracoabdominal aortic aneurysm requires understanding the anatomy and physiology of the spinal cord blood supply. Recent laboratory studies and clinical observations suggest that a robust collateral network must exist to explain preservation of spinal cord perfusion when segmental vessels are interrupted. An anatomic study was undertaken. Twelve juvenile Yorkshire pigs underwent aortic cannulation and infusion of a low-viscosity acrylic resin at physiologic pressures. After curing of the resin and digestion of all organic tissue, the anatomy of the blood supply to the spinal cord was studied grossly and with light and electron microscopy. All vascular structures at least 8 μm in diameter were preserved. Thoracic and lumbar segmental arteries give rise not only to the anterior spinal artery but to an extensive paraspinous network feeding the erector spinae, iliopsoas, and associated muscles. The anterior spinal artery, mean diameter 134 ± 20 μm, is connected at multiple points to repetitive circular epidural arteries with mean diameters of 150 ± 26 μm. The capacity of the paraspinous muscular network is 25-fold the capacity of the circular epidural arterial network and anterior spinal artery combined. Extensive arterial collateralization is apparent between the intraspinal and paraspinous networks, and within each network. Only 75% of all segmental arteries provide direct anterior spinal artery-supplying branches. The anterior spinal artery is only one component of an extensive paraspinous and intraspinal collateral vascular network. This network provides an anatomic explanation of the physiological resiliency of spinal cord perfusion when segmental arteries are sacrificed during thoracoabdominal aortic aneurysm repair.

Paraparesis after Thoracic Stent-Graft Relining for an Unrecognized Type III Endoleak

We examined the reasons for missing a type III endoleak on conventional imaging and the pathophysiology of paraparesis after relining this stent graft. A 46-year-old man was treated with a thoracic stent graft for thoracic rupture of a chronic type B thoracoabdominal dissection with aneurysm formation. In a second intervention, retrograde revascularization of the visceral and renal arteries was performed in combination with insertion of an abdominal stent graft. After initial shrinkage of the aneurysmal sac, the thoracic aortic diameter started increasing again. Consecutive three-phase helical computed tomographic scans did not reveal any endoleak. Because of unbearable back pain, an open surgical exploration was performed. This showed a type III endoleak. Relining of the thoracic stent graft was performed, but paraparesis developed. In patients with unexplained increase of the aneurysmal sac contrast-enhanced magnetic resonance imaging could help to illuminate the underlying endoleak. The collateral network concept can explain spinal cord injury by even minor hemodynamic changes.

The collateral network concept – the anatomy of the intraspinal and paraspinal vasculature in the pig

The collateral network concept – the anatomy of the intraspinal and paraspinal vasculature in the pig

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

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.