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Ann Thorac Surg 1999;67:1038-1043
© 1999 The Society of Thoracic Surgeons


Original Articles

Quick, simple clamping technique in descending thoracic aortic aneurysm repair

Paolo Biglioli, MDa,b, Rita Spirito, MDa,b, Massimo Porqueddu, MDa,b, Marco Agrifoglio, MDa,b, Giulio Pompilio, MDa,b, Alessandro Parolari, MDa,b, Luca Dainese, MDa,b, Erminio Sisillo, MDa,b

a Department of Cardiovascular Surgery, University of Milan, Milan, Italy
b Centro Cardiologico "I Monzino" Foundation - IRCCS, Milan, Italy

Accepted for publication September 28, 1998.

Address reprint requests to Dr Porqueddu, Department of Cardiovascular Surgery, "I Monzino" Foundation IRCCS, Via Parea 4, 20138 Milan, Italy
e-mail: porqueddum{at}lycosmail.com


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. Although significant advances have been made in the surgical treatment of diseases affecting the descending thoracic aorta, paraplegia remains a devastating complication. We propose the quick, simple clamping technique to prevent spinal cord ischemic injury.

Methods. From 1983 to 1998, 143 patients had descending thoracic aorta aneurysm repair. We divided the patients into the following three groups according to the surgical technique used: selective atriodistal bypass was used in group 1 (66 patients); simple clamping technique in group 2 (28 patients); and quick simple clamping technique in group 3 (49 patients). Mean aortic cross clamp time was 39 ± 13 minutes in group 1, 37 ± 11 minutes in group 2, and 17 ± 6 minutes in group 3 (p < 0.01 group 3 versus group 1 and group 2).

Results. The overall incidence of paraplegia was 4.8% (7 patients), 4.5% (3 patients) in group 1, 14.3% (4 patients) in group 2, and 0 in group 3 (p < 0.05 group 3 versus group 2). The overall in-hospital mortality rate was 5.5%. Multivariate logistic regression analysis showed a powerful effect of aortic cross-clamping time as risk factor for both paraplegia (p < 0.008), with an odds ratio of 1.03 per minute, and in-hospital mortality (p < 0.001), with an odds ratio of 2.5 per minute. The mean follow-up time was 65 months with a lower overall mortality rate in group 3 than in group 1 and group 2 (p < 0.05).

Conclusion. In descending thoracic aortic aneurysm repair, spinal cord perfusion can be maintained adequately without reimplantation of segmental vessels or use of atriodistal bypass when the aortic cross-clamp time is short (< 15 to 20 minutes).


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
During the past three decades significant advances have been made in the surgical treatment of diseases affecting the aorta. Despite these important advances paraplegia remains a devastating complication of surgical procedures on the thoracic aorta. The frequency of spinal cord injury ranges from 0.2% after elective repair of an abdominal aortic aneurysm to as high as 40% in an acute rupture involving the descending thoracic aorta. Most surgeons agree that the presence of dissection or the need for an emergency operation because of aneurysm rupture increases the risk for spinal cord injury [14].

The risk of paraplegia after surgical procedures on the thoracic aorta is determined by the interaction of the following factors: the aortic cross-clamp time, the extension of the replaced aortic segment; and the exclusion of critical intercostal arteries [57].

Recent studies on the anatomy and physiology of spinal cord blood supply examined the critical role of the exclusion of a segmental artery (Adamkievicz) as a risk for spinal cord injury; the model of a single anterior spinal artery with multiple interchangeable inputs is more accurate than a model in which any single segmental artery is a prerequisite for adequate spinal cord perfusion [8].


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
We retrospectively reviewed the charts of 143 consecutive patients who had descending aortic aneurysm repair between 1983 and 1998. All patients studied had a descending thoracic aortic aneurysm; no patient with thoracoabdominal aneurysm was included in our patient population. We divided the patients into three groups according to the surgical technique used. Group 1 comprised 66 patients who had selective atriodistal bypass between 1983 and 1994; group 2, 28 patients who had simple clamping between 1983 and 1994; and group 3, 49 patients who had quick, simple clamping between 1995 and 1998. The mechanical support used for selective atriodistal bypass was a centrifugal pump (Biomedicus, Medtronic Inc, Milan, Italy): the left atrium and femoral artery were cannulated.

The operations on the patients in groups 2 and 3 were performed with the simple clamping technique but with a different surgical approach. At the beginning of our experience (group 2, simple clamping) the intercostal arteries were interrupted after the opening of the aneurysm and sometimes the arteries we believed "critical" were reimplanted.

In the patients in group 3 (quick, simple clamping) the surgical approach evolved into one in which the intercostal arteries were clipped from the outside of the thoracic descending aorta before the aortic cross-clamping, and no intercostal or lumbar arteries were reattached to the graft.

There were no significant differences in the extent of the thoracic aneurysm between the three groups of patients; most of them had an extensive aneurysm involving at least two thirds of the thoracic descending aorta (67% in group 3, 62% in group 2, and 61% in group 1). The preoperative clinical features of the three groups of patients are shown in Table 1.


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Table 1. Preoperative Data

 
There were no significant differences in preoperative risk factors among the three groups of patients except for hypertension (47% in group 1, 25% in group 2, and 16.3% in group 3; p < 0.05 group 1 versus group 2 and group 3).

Operative technique
A catheter was usually inserted between the third and fourth lumbar vertebral space to measure the cerebrospinal pressure and for drainage, if necessary. The patient was positioned in a right lateral decubitus position, and a left posterolateral thoracotomy was done. The superior lobe of the left lung was separated from the anterior part of the aneurysm; the phrenic nerve and the vagal nerve were mobilized to isolate the aneurysm.

In groups 1 and 2 we used a classic surgical approach; in these patients the intercostal arteries were interrupted after the aneurysmectomy, and the arteries believed critical (large size or origin from the low thoracic aorta) were reimplanted on the prosthesis.

To achieve a shorter aortic cross-clamping time we used the following operative strategy (quick, simple clamping) on the patients in group 3.

We isolated the aneurysm in its proximal and ventral portion (Fig 1). The dorsal part of the aneurysm was isolated progressively, and the intercostal arteries were occluded with large clips and sectioned. We then prepared the distal part of the aneurysm and isolated the distal neck (usually through another thoracotomy). The inferior lobe of the left lung was released from the ventral surface of the aneurysm. The distal aneurysm was then mobilized and lifted, to search for the intercostal arteries in order to occlude and to section them. Sometimes it was necessary to make a small incision of the diaphragm.



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Fig 1. Isolation of the proximal and ventral portion of the aneurysm. The superior lobe of the left lung is separated from the anterior part of the aneurysm, and the intercostal arteries are isolated.

 
When the aneurysm was completely mobilized and the aorta was ready to be clamped (Fig 2), the proximal and distal anastomoses were done. The prosthesis of appropriate size was anastomized to the aorta with a continuous suture with careful positioning of the graft inside the aorta. Then the aneurysm was totally removed. The anastomoses were usually reinforced with proximal and distal wrappings and resorcine-formol (Colle Biologique, Saint Etienne, France) glue to decrease the suture line tension.



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Fig 2. The intercostal arteries have been isolated and interrupted with metal clips. The aneurysm is mobilized completely and the aorta is ready to be clamped.

 
In patients with aneurysms involving a large extent of the thoracic aorta, we mobilized the proximal and distal portion of the aneurysm while the central part was not completely isolated (Fig 3). The proximal and distal anastomoses were done between two clamps. After the circulation was restored the aneurysm was opened and the intercostal arteries were sutured from the inside of the aneurysm (Fig 4). Then the prosthesis was wrapped with the aneurysmic wall.



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Fig 3. Only the proximal and the distal ends of the aneurysm are isolated; the intercostal arteries that arise from these parts of the aneurysm are interrupted from the outside of the aorta. The proximal and the distal anastomoses are done between two clamps without removing the aneurysm.

 


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Fig 4. After the circulation has been restored the aneurysm is opened completely and the intercostal arteries are sutured from the inside of the aorta.

 
There were no significant differences between groups 1 and 2 in aortic cross-clamp time (39 ± 13 versus 37 ± 11 minutes). In group 3 we achieved a significantly shorter mean aortic cross-clamp time (17 ± 6 minutes; p < 0.01 group 3 versus group 1 and group 2).

Statistical method
Univariate ({chi}2 and Fisher exact test) and multivariate (stepwise logistic regression) analyses were used to detect preoperative and intraoperative clinical predictors of early morbidity and mortality. Survival curves were estimated by the Kaplan-Meyer method; differences in survival rates between the groups were analyzed using the log rank test. The stepwise Cox regression model was used to predict late mortality.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
The incidence of paraplegia was 4.8% overall, 4.5% in group 1, 14.3% in group 2, and 0 in group 3. There was no significant difference between group 1 and group 2; the difference between group 3 and group 2 was significant (p < 0.05) (Table 2).


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Table 2. Postoperative Complications

 
The most common postoperative complications were myocardial infarction, respiratory failure, acute renal failure, and bleeding. Only the incidence of respiratory failure was significantly different between group 1 (15.1%) and group 2 (3.6%) and group 3 (2%) (Table 2).

There were no significant differences in reoperation for bleeding among the three groups, but patients in groups 2 and 1 required transfusion with more packed red blood cells and fresh frozen plasma than those in group 3.

Multivariate logistic regression analysis found a powerful effect of aortic cross-clamping time as a risk factor for paraplegia (p < 0.008) with an odds ratio of 1.03 per minute. Other factors correlated to neurologic events were preoperative renal failure (p < 0.05) and emergency operation (p = 0.02). Multivariate analysis found no other risk factors as important influences on the rate of paraplegia, including age, sex, presence of diabetes, hypertension, and previous coronary artery bypass grafting.

Multivariate logistic regression analysis also found a significant effect of aortic cross-clamp time as risk factor for respiratory failure (p < 0.006) with an odds ratio of 1.06 per minute. History of chronic obstructive broncopneumopathy (p < 0.05) and emergency operation (p < 0.02) were also risk factors for respiratory failure (Table 3).


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Table 3. Stepwise Logistic Regression Analysis

 
We had an overall in-hospital mortality rate of 5.5%. There was no significant difference between group 1 (9.8%) and group 2 (7.1%). In group 3 (49 patients) there were no in-hospital deaths.

Multivariate logistic regression analysis found a significant effect of aortic cross-clamp time for in-hospital mortality (p < 0.001) with an odds ratio of 2.5 per minute. Other preoperative risk factors for in-hospital mortality were age (p < 0.03), with an odds ratio of 1.08 per year, and female sex (p < 0.04).

The causes of in-hospital death were pulmonary embolism (0.7%), multiorgan failure (2.1%), mesenteric ischemia (0.7%), and stroke (2.1%). There were no significant differences between groups 1 and 2.

The mean follow-up time was 65 months. Cumulative survival at 60 months after the operation was 80.2% for group 1 and 79.3% for group 2; there was no significant difference in the overall mortality rate between groups 1 and 2.

Group 3 cumulative survival at 48 months after the operation was 97.5%; there is a significant difference in overall mortality rate of the group 3 versus group 1 and group 2 (log rank p < 0.05) (Fig 5). Cox regression analysis of risk factors for late mortality identified age more than 70 years as a predictor of late mortality (p = 0.05).



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Fig 5. Overall survival curve.

 

    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
There are different protective techniques used to reduce the risk of spinal cord injury during operations on the descending thoracic aorta. Short aortic cross-clamp time, intercostal artery reimplantation, distal aortic perfusion, cerebrospinal fluid drainage, drugs, and cardiopulmonary bypass with or without hypothermia are all potential adjuncts that might decrease the incidence of postoperative paraplegia.

Clinically, the clamp and go technique was the first method used to repair aneurysms of the thoracic aorta. Svensson and colleagues [3] determined that the aortic cross-clamp time was an independent predictor of paraplegia of paraparesis. A literature review from 1988 to 1998 reports a range in the incidence of paraplegia which was closely related to aortic cross-clamp time as an independent risk factor for spinal cord damage. A spinal cord ischemic time greater than 30 minutes has been considered a critical event regardless of the spinal cord protective techniques employed [9, 10].

Although the clamp and go technique has been used successfully in many patients, those studies confirmed the need for additional protective measures when aortic cross-clamp time is greater than 30 minutes. Different techniques have been advocated for perfusing the distal aorta in retrograde fashion, including passive shunts, roller pumps, centrifugal pumps, or total cardiopulmonary bypass to increase distal perfusion beyond the aortic clamp [1114]. The fundamental premise of these techniques has been that increasing the distal aortic perfusion pressure will result in increased blood flow to the entire spinal cord and thus decrease spinal cord ischemic injury during aortic cross-clamping.

Centrifugal pumps have the potential advantage of maintaining aortic distal perfusion while avoiding the problems related to systemic heparinization, with the use of the roller pumps, and the inability to regulate the flow to the distal aorta, with the use of the Gott shunt.

Unfortunately, these distal aortic perfusion techniques do not protect the spinal cord in all patients. In fact, perfusion techniques simply provide blood flow to the distal aorta, and if the artery supplying the anterior spinal artery arises from the excluded segment of the aorta, the spinal cord remains ischemic despite excellent distal aortic perfusion.

The cause of postoperative neurologic deficits (paraplegia and paraparesis) after otherwise successful descending thoracic aorta replacement is multifactorial. The approaches that have been attempted previously by different surgical groups (deep hypothermia and circulatory arrest, intercostal artery reimplantation, cerebrospinal fluid drainage, and distal circulatory support) could not completely eliminate the occurrence of this complication.

Our experience was with a population of patients with aneurysms of the descending thoracic aorta. Most of them had an extensive aneurysm involving more than two thirds of the descending thoracic aorta. In most patients, the collateral circulation of the spinal cord is usually adequate to perfuse the cord even if the blood supply from the intercostal arteries is interrupted. When the interruption of the blood supply from the intercostal arteries is done (by external clipping or intra-aneurysmal suture of the intercostal branches) the critical factor of this operation is the duration of the aortic cross-clamp time.

One limitation of our study is that it was a retrospective review of a consecutive series of patients operated on between 1983 and 1998. In the past 15 years there has been a general improvement in anesthesia and increased awareness of the physiology of spinal cord perfusion. These factors might be related to the incidence of postoperative paraplegia. However, the results obtained in group 3 are so impressive and the reduction of the aortic cross-clamp time so significant that we consider the ischemic time the most critical factor related to spinal cord ischemic injury.

Irrespective of the mechanism, a decrease in spinal cord blood flow results in spinal cord ischemia. At normothermia, mitochondrial oxidative phosphorylation stops after 3 to 4 minutes, resulting in depletion of adenosine triphosphate and failure of the adenosine triphosphate-dependent membrane pumps that regulate intracellular calcium homeostasis [15]. The increasing level of intracellular calcium results in production of free radicals and release of neurotoxic amino acid, with a progressive loss of membrane integrity, DNA damage, and intracellular edema leading to reversible or irreversible cellular injury. The occurrence of hyperemia during reperfusion also contributes to cellular damage [1618].

According to recent surgical experience reported by Griepp and colleagues [8], we believe that spinal cord supply does not depend on a single artery or even on a small number of critical intersegmental vessels: our preliminary results showed that spinal cord perfusion can be maintained adequately without reimplantation of segmental vessels.

Our surgical experience supports this hypothesis: even if the pattern and the features of the spinal cord supply varies in humans, the reduction in cross-clamp time is the most effective measure to prevent perioperative paraplegia. For this reason, further study will be to determine the most suitable surgical approaches (eg, operative technique, surgical material such as needles, suture threads, surgical team training) to obtain a shorter aortic cross-clamp time.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Mauney M.C., Blackbourne L.H., Lagenberg S.E., et al. Prevention of spinal cord injury after repair of the thoracic or thoracoabdominal aorta. Ann Thorac Surg 1995;59:245-252.[Abstract/Free Full Text]
  2. Gharagozloo F., Larson J., Dausmann M.J. Spinal cord protection during surgical procedures on the descending thoracic and thoracoabdominal aorta. Chest 1996;109:799-809.[Free Full Text]
  3. Svensson L.G., Crawford E.S., Hess K.R., Coselli J.S., Safi H.J. Experience with 1509 patients undergoing thoracoabdominal aortic operation. J Vasc Surg 1993;17:357-368.[Medline]
  4. Coselli J.S., LeMaire S.A., Figueiredo L.P., et al. Paraplegia after thoracoabdominal aortic aneurysm repair: is dissection a risk factor. Ann Thorac Surg 1997;63:28-36.[Abstract/Free Full Text]
  5. Svensson L.G., Rickards E., Coull A., et al. Relationship of spinal cord blood flow to vascular anatomy during thoracic aortic cross clamping and shunting. J Thorac Cardiovasc Surg 1986;91:71-78.[Abstract]
  6. Svensson L.G., Patel V., Robinson M.F., et al. Influence of preservation or perfusion of intraoperatively identified spinal cord blood supply on spinal motor evoked potentials and paraplegia after aortic surgery. J Vasc Surg 1988;9:135-144.
  7. Crawford E.S., Crawford J.L., Safi H.J., et al. Thoracoabdominal aortic aneurysms: preoperative and intraoperative factors determining immediate and long term results of operations in 605 patients. J Vasc Surg 1986;3:389-404.[Medline]
  8. Griepp 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;112:1202-1215.[Abstract/Free Full Text]
  9. Livesay J.L., Cooley D.A., Ventemiglia R.A., et al. Surgical experience in descending thoracic aneurysmectomy with and without adjuncts to avoid ischemia. Ann Thorac Surg 1995;39:37-46.[Abstract]
  10. Katz N.M., Blackstone E.H., Kirklin J., et al. Incremental risk factors for spinal cord injury following operation for acute traumatic transection. J Thorac Cardiovasc Surg 1981;81:669-674.[Abstract]
  11. Ergin M.A., Galla J.D., Lansman S.L., et al. Distal perfusion methods for surgery of descending aorta. Thorac Cardiovasc Surg 1991;3:293-299.
  12. Verdant A., Page A., Cossette R., et al. Surgery of the descending thoracic aorta: spinal cord protection with the Gott shunt. Ann Thorac Surg 1988;46:147-154.[Abstract]
  13. Crawford E.S., Coselli J.S., Safi H.J., et al. Partial cardiopulmonary bypass, hypothermic circulatory arrest and posterolateral exposure for thoracic aortic aneurysm operation. J Thorac Cardiovasc Surg 1987;94:824-827.[Abstract]
  14. Kouchoukos N.T., Wareing T.H., Izumoto H., et al. Elective hypothermic cardiopulmonary bypass and circulatory arrest for spinal cord protection during operations on the thoracoabdominal aorta. J Thorac Cardiovasc Surg 1990;99:659-664.[Abstract]
  15. Krause G.S., White B.C., Aust S.D., et al. Brain cell death following ischemia and reperfusion: a proposed biochemical sequence. Crit Care Med 1988;16:714-726.[Medline]
  16. Rothman S. Synaptic release of excitatory amino acid neurotransmitter mediates anoxic neuronal death. J Neurosci 1984;4:1884-1891.[Abstract]
  17. Schittek A., Bennik G.B., Cooley D.A., et al. Spinal cord protection with intravenous nimodipine: a functional and morphologic evaluation. J Thorac Cardiovasc Surg 1992;104:1100-1105.[Abstract]
  18. Giulian D., Robertson C. Inhibition of mononuclear phagocytes reduces ischemic injury in the spinal cord. Ann Neurol 1990;27:33-34.[Medline]

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