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Moderate to Deep Hypothermia in Patients Undergoing Thoracoabdominal Aortic Repair
Moderate to Deep Hypothermia in Patients Undergoing Thoracoabdominal Aortic Repair Toshihiro Fukui, and Shuichiro Takanashi, Tokyo, Japan
Background: The aim of this study was to determine early and mid-term outcomes after open repair of thoracoabdominal aortic aneurysm, with moderate to deep hypothermia as part of proximal aortic management. Methods: Between April 2009 and March 2015, 44 patients underwent thoracoabdominal aortic repair by total cardiopulmonary bypass at our institute. Our strategy was to use deep (<25 C) hypothermic circulatory arrest when open proximal anastomosis is necessary (n ¼ 18). Otherwise, proximal anastomosis with an aortic clamp was performed with moderate (25e30 C) hypothermia without circulatory arrest (n ¼ 26). Early and mid-term outcomes were assessed in all patients. Results: In-hospital mortality was observed in 1 patient (2.3%). Stroke was observed in 2 (4.5%) patients and a spinal cord ischemic injury in 4 (9.1%). Renal failure requiring new hemodialysis was observed in 5 patients (11.4%). There were 9 patients (20.5%) with early major adverse events (in-hospital death, stroke, spinal cord ischemic injury, renal failure requiring new hemodialysis, and prolonged intubation). Multivariable logistic regression analysis demonstrated that a history of abdominal aortic aneurysm repair (odds ratio 17.711, 95% confidence interval 1.274e246.426, P ¼ 0.032) was the only independent predictor of early major adverse events. Deep hypothermic circulatory arrest was not an independent predictor of early major adverse events. At 5 years, overall freedom from death was 89.4 ± 6.1%. Conclusion: Moderate to deep hypothermia as a constituent of proximal aortic management was safe and effective in patients undergoing open repair of thoracoabdominal aortic aneurysm.
INTRODUCTION The surgical treatment of thoracoabdominal aortic aneurysm (TAAA) still carries high mortality and morbidity despite improvements in surgical approaches and postoperative management. Hypothermia is considered an effective method for brain and spinal cord protection during open surgical repair for TAAA. Moreover, deep hypothermic circulatory arrest (DHCA) has several benefits
Department of Cardiovascular Surgery, Sakakibara Heart Institute, Tokyo, Japan. Correspondence to: Toshihiro Fukui, MD, Department of Cardiovascular Surgery, Kumamoto University Hospital, 1-1-1 Honjo, Chuo-ku, Kumamoto 860-8556, Japan; E-mail: [email protected] Ann Vasc Surg 2016; 31: 39–45 http://dx.doi.org/10.1016/j.avsg.2015.08.021 Ó 2016 Elsevier Inc. All rights reserved. Manuscript received: June 30, 2015; manuscript accepted: August 21, 2015; published online: November 23, 2015.
including minimal aortic dissection, the elimination of the need for a proximal clamp, a bloodless field, and reduced potential for atheromatous embolization.1 Many investigators have demonstrated the safety and effectiveness of DHCA with favorable outcomes in a large number of patients.1e6 However, there has been a reluctance to use DHCA among other surgeons, largely because of a perception that there is a vastly increased risk of bleeding complications.6 Furthermore, prolonged operation time during cooling and rewarming may be of some concern. We have adopted a modified hypothermic strategy that can be used as a constituent of proximal aortic management. When the proximal aorta could not be clamped or clamping was decided against, DHCA (<25 C) was used during the proximal aortic anastomosis. Otherwise, moderate hypothermia (25e30 C) with a sequential clamp was used. This strategy may have several advantages as regards 39
40 Fukui and Takanashi
neural protection, embolization, and bleeding complications in accord with patients’ conditions. In this study, early and mid-term outcomes were assessed after our modified hypothermic strategy for the surgical repair of TAAA.
PATIENTS AND METHODS Patients Between April 2009 and March 2015, 44 patients underwent TAAA repair using total cardiopulmonary bypass and our modified hypothermic strategy at Sakakibara Heart Institute. Another 5 patients who underwent left heart bypass during the study period were excluded. Preoperative characteristics of all patients are shown in Table I. There were 15 female (34.1%) and 29 male patients (65.9%). Crawford type II or III TAAA was observed in 26 patients (59.1%). There were 18 chronic dissections (40.9%) and 26 degenerative aneurysms (59.1%). Emergent surgery was performed in 6 patients (13.6%) because of rupture. Nineteen patients had undergone previous proximal aortic surgery (Bentall in 2 patients, ascending aorta in 4, total aortic arch in 11, and descending thoracic aorta in 7). No patients had a previously implanted stent graft. The Institutional Review Board approved this retrospective study and waived the need for written consent. Operative Technique Preoperative computed tomography (CT) with contrast enhancement was performed to detect the Adamkiewicz artery in nonemergent patients. Cardiac anesthesiologists placed all spinal drains in the operating room 1 day before the operation in patients undergoing elective surgery. However, spinal drainage was not inserted in patients undergoing emergent surgery and those with technical difficulty. The cerebrospinal pressure was monitored continuously during surgery and the early postoperative period. Cerebrospinal fluid was freely drained with gravity whenever cerebrospinal pressure exceeded 10 mm Hg. In patients without a spinal cord deficit, the drain was removed on postoperative day 2. Intraoperative motor-evoked potentials or somatosensory evoked potentials were not used. Posterolateral incision through the fifth to seventh intercostal space, according to the extent of TAAA, was performed. The diaphragm was incised circumferentially and a retroperitoneal approach was taken without opening the peritoneum.
Annals of Vascular Surgery
Table I. Preoperative variables Preoperative variables of all patients
All (n ¼ 44)
Age Female gender Crawford extent Type I Type II Type III Type IV Type V Dissection Hypertension Diabetes mellitus Hyperlipidemia Smoking history Marfan syndrome Chronic kidney disease Chronic obstructive pulmonary disease Emergent History of stroke History of proximal aortic surgery History of abdominal aortic surgery
65.6 ± 14.4 15 (34.1%) 3 9 17 8 7 18 42 4 17 29 5 3 2 6 3 19 7
(6.8%) (20.5%) (38.6%) (18.2%) (15.9%) (40.9%) (95.5%) (9.1%) (38.6%) (65.9%) (11.4%) (6.8%) (4.5%) (13.6%) (6.8%) (43.2%) (15.9%)
Arterial cannulation was performed via the left femoral artery in all patients. Additional left axillary arterial or ascending aortic cannulation was performed to prevent embolization to the brain when the preoperative contrast-enhanced CT detected extensive atheromatous plaques in the aorta. Venous cannulation was performed via the left femoral vein. Left heart venting was effected through the left upper pulmonary vein when possible. Our strategy is to use moderate to deep hypothermia during open repair of TAAA for organ protection in all patients. DHCA (<25 C) was applied when open proximal anastomosis was necessary (n ¼ 18). Otherwise, proximal anastomosis with an aortic clamp was performed with moderate (25e30 C) hypothermia without circulatory arrest (n ¼ 26). Open proximal anastomosis was used in situations including no space between aneurysm and left subclavian artery, severe adhesions because of previous proximal aortic operations, vulnerable aortic wall with a dissection, and multiple atheromatous plaques. When open proximal anastomosis was applied, left axillary arterial or ascending aortic perfusion was stopped at the time of aortic incision. Irrespective of proximal management, distal clamping was performed in all patients to perfuse the visceral organs and spinal cord with partial cardiopulmonary bypass. After the anastomosis between the proximal aortic stump and the prosthesis graft, perfusion to the upper body was resumed via a left
Volume 31, February 2016
axillary arterial or ascending aortic cannula in patients undergoing open repair with DHCA. This graft is a 20- to 22-mm Dacron straight tube graft. After completion of the proximal anastomosis in patients undergoing DHCA, they were rewarmed to 25e 30 C. The decision of using DHCA with open proximal anastomosis or moderate hypothermia with proximal clamp was made by preoperative CT and confirmed during operation. Sequential clamping of the descending aorta was performed in all patients. The first clamp was just distal to the proximal aortic anastomosis. The second clamp was applied just above the celiac artery. After opening the descending aorta by removing the first clamp, the major 1 or 2 pairs of intercostal arteries were identified and attached to the side hole of the tube graft. These arteries were generally identified from the preoperative CT. Other minor branches were ligated. Back-bleeding from the intercostal arteries was controlled by inserting 2F balloon-tipped catheters into the ostia to prevent spinal cord ischemia arising from a steal phenomenon. We use the straight tube graft from the proximal anastomosis to the reattachment of intercostal arteries because the handling of a tube graft is satisfactory and the hemostasis is easily confirmed. Perfusion to the intercostal artery was resumed with circulation from the upper body. The 4-branched Dacron graft was anastomosed to the distal end of the tube graft. The third clamp was applied at the infrarenal portion of the aorta, and the abdominal aorta was opened. The celiac, superior mesenteric, and bilateral renal arteries were immediately cannulated and perfused. Celiac and superior mesenteric arteries were perfused with blood by a single roller pump (200 mL/min in total). Bilateral renal arteries were perfused with cold crystalloid solution (250 mL each) intermittently (every 20 min). Each visceral artery was detached individually with a small cuff of aortic wall. The right renal artery, left renal artery, superior mesenteric artery, and celiac artery were anastomosed to the side branches of the prosthetic graft in sequence. Perfusion to each artery was resumed from the upper perfusion sequentially. The major intercostal artery at the level of the celiac artery or superior mesenteric artery was reconstructed using an 8-mm graft interposition when the Adamkiewicz artery was identified. The inferior mesenteric artery was sacrificed in all patients. Final clamping was performed at the distal aorta or bilateral common iliac arteries. At this point, femoral arterial perfusion was stopped and final distal anastomosis was performed. Rewarming was initiated after the reattachment of the intercostal arteries. Cardiopulmonary bypass
Hypothermia in thoracoabdominal repair 41
was discontinued when the bladder temperature reached 35.0 C. Definitions Chronic kidney disease was defined as creatinine level more than 1.5 mg/dL. In-hospital death was defined as death within the same hospitalization period or within 30 days of surgery. Postoperative stroke was defined as the occurrence of a new stroke confirmed by CT. In patients with preoperative stroke, postoperative stroke was defined as a worsening of the neurological deficit with new radiological findings. Spinal cord ischemic injury included permanent paraplegia and paraparesis. Prolonged intubation was defined as a requirement for ventilation longer than 48 hr. Perioperative myocardial infarction was defined as new Q waves on electrocardiography or a peak creatine kinase MB level 5 times the upper limit of normal (25 IU/L). Early major adverse events included inhospital death, stroke, spinal cord ischemic injury, renal failure requiring new hemodialysis, and prolonged intubation. Statistical Analysis All statistical analyses were performed using the StatView 5.0 software package (SAS Institute, Inc., Cary, NC). Continuous variables are reported as mean ± standard deviation. Continuous variables were compared using the ManneWhitney U-test and discrete variables were compared using the c2 test or Fisher’s exact test. Differences were considered significant at P < 0.05. Univariate and multivariate logistic regression analyses were performed to determine the significant predictors of early major adverse events. The variables used for univariate analysis were the clinical variables listed in Table I and DHCA. Variables identified as having a P value of <0.1 on univariate analyses were considered for inclusion in the multivariate model. Actuarial event-free survival curves were estimated by the KaplaneMeier method. The log-rank test was used to assess differences in survival between groups.
RESULTS Early Outcomes The operative data are listed in Table II. The reasons for selecting DHCA were as follows: no space between aneurysm and left subclavian artery in 6 patients, severe adhesions because of previous
42 Fukui and Takanashi
Annals of Vascular Surgery
Table II. Operative and postoperative data Operative and postoperative data of all patients All (n ¼ 44)
Minimal bladder temperature ( C) Cerebrospinal drainage Coronary artery bypass grafting Operation time (min) Cardiopulmonary bypass time (min) 30-Day mortality In-hospital mortality Major adverse events Stroke Spinal cord ischemic injury Renal failure requiring newly hemodialysis Prolonged intubation (>48 hr) Tracheostomy Reexploration for bleeding Low output syndrome Gastrointestinal complications Transfusion of red blood cells (U) Postoperative stay (day)
27.8 ± 4.5 32 (72.7%) 1 (2.3%) 329.1 ± 87.6 118.8 ± 47.2 0 1 (2.3%) 9 (20.5%) 2 (4.5%) 4 (9.1%) 5 (11.4%) 5 (11.4%) 2 (4.5%) 0 0 0 9.9 ± 4.5 28.9 ± 48.5
proximal aortic operations in 6, vulnerable aortic wall with a dissection in 2, and severe atheromatous plaques in 4. Cerebrospinal drainage was inserted preoperatively in 32 patients (72.7%). The reasons of not being feasible for cerebrospinal drainage were emergent operation in 6 patients and technical difficulty in 6. Coronary artery bypass grafting (left internal thoracic artery to left anterior descending artery) was concomitantly performed in 1 patient. There was no 30-day mortality; however, inhospital mortality was observed in 1 patient (2.3%), whose cause of death was stroke. There were 9 patients (20.5%) with early major adverse events in all patients. Of these, spinal cord ischemic injury was observed in 4 patients (9.1%). There was no patient with transient spinal cord ischemic injury in this study. Renal failure requiring new hemodialysis was observed in 5 patients (11.4%); however, they did not need chronic hemodialysis at discharge. There was no patient with low output syndrome. The mean postoperative hospital stay was 28.9 days, with a median of 15 days. Predictors of Early Major Adverse Events On univariate analysis, Crawford type II or III (P ¼ 0.069), chronic kidney disease (P ¼ 0.079), a history of abdominal aortic surgery (P ¼ 0.036), and DHCA (P ¼ 0.090) were selected for further multivariate analysis. Multivariable logistic regression analysis (Table III) demonstrated that a history
of abdominal aortic surgery (P ¼ 0.032) was only independent predictor of early major adverse events. Mid-term Outcome Follow-up was completed in all patients. During the follow-up period (29.1 ± 18.8 months), there were 3 deaths (6.8%) including 1 in-hospital death. The causes of the other 2 deaths were pneumonia at 5.2 months and sudden death at 12.6 months after the operation. The actuarial survival rate at 5 years was 89.4 ± 6.1% in all patients (Fig. 1).
DISCUSSION This study demonstrated that a modified hypothermic strategy (moderate or deep) with respect to proximal aortic management was safe and effective in patients undergoing open repair of TAAA, with favorable early and mid-term survival rates. Hypothermia has been considered safe and effective for protecting the central nervous system during complex cardiac and vascular surgery. Moreover, DHCA has several benefits including minimal aortic dissection, the elimination of the need for a proximal clamp, a bloodless field, and a reduced potential for the atheromatous embolization.1 Several investigators have reported the usefulness of DHCA in patients undergoing a repair of TAAA. Kouchoukos et al.1 evaluated their 26-year experience using DHCA in patients undergoing TAAA repair. In their analysis, the rates of 30-day mortality, stroke, spinal cord ischemic injury, and new dialysis were 7.8%, 3.7%, 5.3%, and 3.7%, respectively. They described that hypothermia increases ischemic tolerance and allows unhurried aortic reconstruction, and concluded that their results compared favorably with those using alternative open and currently used endovascular and hybrid debranching surgical techniques.3 Fehrenbacher et al.2 reported outcomes after open repair using DHCA in patients with descending thoracic aortic aneurysm and TAAA. Operative mortality was 5.7% (14/245) in selected patients undergoing TAAA repair. Other morbidity rates included 4.5% for stroke, 4.1% for spinal cord ischemic injury, and 2% for new dialysis. They described that the use of open repair with DHCA can visualize the inside of the arch during circulatory arrest, which gives the surgeon the ability to avoid or remove severely atherosclerotic segments, perform endarterectomy of very calcified segments, and assess the need for arch branch bypasses or total arch replacement. Indeed, Fehrenbacher et al. performed total arch replacement concomitantly in 5.5% of the
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Hypothermia in thoracoabdominal repair 43
Table III. Multivariate logistic regression analyses for early major adverse events Variable
Odds ratio
95% Confidence P value interval
History of abdominal 17.711 0.032 aortic surgery Crawford type II or III 9.488 0.111 Deep hypothermic 2.775 0.320 circulatory arrest Chronic kidney 0.873 0.940 disease
1.274e246.426 0.595e151.249 0.371e20.735 0.025e30.321
Fig. 1. KaplaneMeier event-free survival analysis for allcause mortality.
patients. Weiss et al.5 compared DHCA with mild hypothermia without circulatory arrest in patients undergoing descending thoracic aortic and TAAA repair using a propensity score-matching method. In their analysis, significantly lower rates of acute renal failure and liver failure were observed in the DHCA group. However, reports of excellent results after open repair with DHCA in patients with TAAA are limited, and some adverse effects have been reported by other groups. Safi et al.7 reported 21 patients undergoing open repair with DHCA out of 409 patients who underwent repair of descending thoracic aortic aneurysm and TAAA. The reason for selecting DHCA was an inability to gain proximal aortic control because of anatomic or technical difficulty. The outcomes of these patients were not favorable; 30-day mortality, stroke, and spinal cord ischemic injury were observed in 29%, 13%, and 13% of the patients, respectively. Furthermore, the pulmonary complication rate was very high (67%). Safi et al. concluded that the judicious application of this method in rare instances when proximal control is not feasible or there is catastrophic intraoperative bleeding leaves the surgeon with no other option. Coselli et al.8 similarly reported their
results of open repair with DHCA in patients with descending thoracic aortic aneurysm and TAAA. In their institute this technique was used when the location, extent, and severity of disease precluded placement of a proximal aortic clamp. The 30-day mortality, stroke, and renal failure were 21%, 9%, and 15%, respectively. Although these results were not favorable, the incidence of paraplegia was only 1% better than that performed with a non-DHCA technique. Therefore, Coselli et al. concluded that DHCA will continue to play an important role in organ protection, primarily as applied to the spinal cord, in patients at extreme risk of ischemic complications, such as those with Crawford type II aneurysms. In this study, we developed the modified strategy of using hypothermia during proximal aortic management. We agree that hypothermia is effective in reducing the rate of spinal cord ischemic injury and is useful for visceral organ protection. However, it has been suggested that DHCA has disadvantages which include coagulopathy, cold injury to the lung, inflammatory consequences of cardiopulmonary bypass, and retraction injury of the heparinized left lung.8 Moreover, prolonged operation time during cooling and rewarming may be of some concern among surgeons. Our strategy is consistent with the hypothermic strategy. All patients were cooled to at least moderate hypothermia as soon as the cardiopulmonary bypass started. When the proximal aorta could not be clamped or clamping was decided against, then DHCA was used during the proximal aortic anastomosis. Otherwise, proximal clamping with moderate hypothermia was performed. Indeed, in this study, the operation time was longer in patients with DHCA than those without DHCA (379.1 vs. 294.5 min, P ¼ 0.002). However, DHCA was not an independent predictor of early major adverse events with multivariable logistic regression analysis. The potential advantage of our strategy lies in it being easy to switch to DHCA in patients who need open proximal anastomosis during surgery, although not all patients need deep hypothermia. In this study, the rate of renal failure requiring new hemodialysis was high (5 patients, 11.4%). The introduction of hemodialysis takes place early in our institute, following the article by Karvellas et al.9 describing that earlier institution of renal replacement therapy in critically ill patients with acute kidney injury may have a beneficial impact on survival. In our institute, the indications are based on the Risk, Injury, Failure, Loss, and Endstage kidney classification.10 When an increase in serum creatinine by 1.5 times or a urine output <0.5 mL/kg/hr 6 hr is observed, then
44 Fukui and Takanashi
hemodialysis is initiated. Such patients are all treated with continuous venovenous hemodiafiltration. Zarbock et al.11 described the advantage of continuous venovenous hemodialysis over intermittent hemodialysis in critically ill patients, including greater hemodynamic and metabolic stability, increased time-averaged dialysis dose, and removal of proinflammatory cytokines. It can also provide better control of fluid balance and solute removal. Owing to early continuous treatments for postoperative renal failure, none of the 4 patients progressed to chronic renal failure. In this study, a history of abdominal aortic surgery was only an independent predictor of early major adverse events. Some investigators demonstrated that a history of abdominal aortic surgery was one of the independent predictors of major complications after thoracoabdominal aortic repair. Schl€ osser et al.12 in their meta-analysis revealed that prior abdominal aortic aneurysm repair was a significant risk factor for neurological deficit and for developing renal failure after TAAA surgery with relative risks of 2.90 (95% confidence interval [CI] 1.26e6.65, P ¼ 0.008) and 3.47 (95% CI 1.74e 6.91, P ¼ 0.0001), respectively. The importance of collateral flow from the infrarenal and pelvic circulation to the spinal cord has been described.13,14 This collateral flow is greatly reduced or eliminated during infrarenal abdominal aortic aneurysm repair, exposing susceptible patients to an increased risk of paraplegia after subsequent TAAA repair. The same mechanism may be the possible reason for a history of abdominal aortic surgery as the only independent predictor of early major adverse events in this study. Mid-term and long-term survival of patients who underwent surgery for TAAA has not been well documented. Kouchoukos et al.1 reported a 5-year survival of 55%, and Fehrenbacher et al.2 reported 69.3% survival in patients with descending thoracic aortic aneurysm and TAAA. However, other analyses including only more recent cases demonstrated favorable mid-term outcomes. Wong et al.15 reported a 2-year survival rate of 79.1% in patients undergoing TAAA repair, Okita et al.16 reported a 5-year survival of 83.6%, and Johns et al.17 reported that 5-year survival was 79.7% in patients younger than 60 years undergoing TAAA repair. Recent intraoperative anesthetic and perfusion techniques and postoperative intensive care management strategies have been improved and have contributed to better outcomes in patients undergoing open repair of TAAA. This study has the following limitations: (1) this is a retrospective observational study; (2) the number
Annals of Vascular Surgery
of patients and the follow-up period of 5 years might not be sufficient to provide definitive results; and (3) because there was no control group, we cannot conclude that moderate to deep hypothermia is superior to traditional techniques in patients undergoing TAAA repair.
CONCLUSIONS A modified hypothermic strategy (moderate or deep) with respect to proximal aortic management was safe and effective in patients undergoing open repair of TAAA, with favorable early and mid-term survival rates. Further studies that include larger sample sizes are needed. REFERENCES 1. Kouchoukos NT, Kulik A, Castner CF. Outcomes after thoracoabdominal aortic aneurysm repair using hypothermic circulatory arrest. J Thorac Cardiovasc Surg 2013;145: S139e41. 2. Fehrenbacher JW, Siderys H, Terry C, et al. Early and late results of descending thoracic and thoracoabdominal aortic aneurysm open repair with deep hypothermia and circulatory arrest. J Thorac Cardiovasc Surg 2010;140:S154e60. 3. Kulik A, Castner CF, Kouchoukos NT. Outcomes after thoracoabdominal aortic aneurysm repair with hypothermic circulatory arrest. J Thorac Cardiovasc Surg 2011;141:953e60. 4. Sundt TM, Fleming MD, Oderich GS, et al. Spinal cord protection during open repair of thoracic and thoracoabdominal aortic aneurysm using profound hypothermia and circulatory arrest. J Am Coll Surg 2011;212:678e83. 5. Weiss AJ, Lin HM, Bischoff MS, et al. A propensity scorematched comparison of deep versus mild hypothermia during thoracoabdominal aortic surgery. J Thorac Cardiovasc Surg 2012;143:186e93. 6. Griepp RB, Di Luozzo G. Hypothermia for aortic surgery. J Thorac Cardiovasc Surg 2013;145:S56e8. 7. Safi HJ, Miller CC 3rd, Subramaniam MH, et al. Thoracic and thoracoabdominal aortic aneurysm repair using cardiopulmonary bypass, profound hypothermia, and circulatory arrest via left side of the chest incision. J Vasc Surg 1998;28:591e8. 8. Coselli JS, Bozinovski J, Cheung C. Hypothermic circulatory arrest: safety and efficacy in the operative treatment of descending and thoracoabdominal aortic aneurysms. Ann Thorac Surg 2008;85:956e63. 9. Karvellas CJ, Farhat MR, Sajjad I, et al. A comparison of early versus late initiation of renal replacement therapy in critically ill patients with acute kidney injury: a systematic review and meta-analysis. Crit Care 2011;15:R72. 10. Hoste EA, Clermont G, Kersten A, et al. RIFLE criteria for acute kidney injury are associated with hospital mortality in critically ill patients: a cohort analysis. Crit Care 2006;10:R73. 11. Zarbock A, Singbartl K, Kellum JA. Evidence-based renal replacement therapy for acute kidney injury. Minerva Anestesiol 2009;75:135e9. 12. Schl€ osser FJ, Mojibian H, Verhagen HJ, et al. Open thoracic or thoracoabdominal aortic aneurysm repair after previous abdominal aortic aneurysm surgery. J Vasc Surg 2008;48: 761e8.
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13. Lombardi JV, Carpenter JP, Pochettino A, et al. Thoracoabdominal aortic aneurysm repair after prior aortic surgery. J Vasc Surg 2003;38:1185e90. 14. Szilagyi DE. A second look at the etiology of spinal cord damage in surgery of the abdominal aorta. J Vasc Surg 1993;17:1111e3. 15. Wong DR, Parenti JL, Green SY, et al. Open repair of thoracoabdominal aortic aneurysm in the modern surgical era:
Hypothermia in thoracoabdominal repair 45
contemporary outcomes in 509 patients. J Am Coll Surg 2011;212:569e79. 16. Okita Y, Omura A, Yamanaka K, et al. Open reconstruction of thoracoabdominal aortic aneurysms. Ann Cardiothorac Surg 2012;1:373e80. 17. Johns N, Jamieson RW, Ceresa C, et al. Contemporary outcomes of open repair of thoracoabdominal aortic aneurysm in young patients. J Cardiothorac Surg 2014;9:195.
Background: The aim of this study was to determine early and mid-term outcomes after open repair of thoracoabdominal aortic aneurysm, with moderate to deep hypothermia as part of proximal aortic management. Methods: Between April 2009 and March 2015, 44 patients underwent thoracoabdominal aortic repair by total cardiopulmonary bypass at our institute. Our strategy was to use deep (<25 C) hypothermic circulatory arrest when open proximal anastomosis is necessary (n ¼ 18). Otherwise, proximal anastomosis with an aortic clamp was performed with moderate (25e30 C) hypothermia without circulatory arrest (n ¼ 26). Early and mid-term outcomes were assessed in all patients. Results: In-hospital mortality was observed in 1 patient (2.3%). Stroke was observed in 2 (4.5%) patients and a spinal cord ischemic injury in 4 (9.1%). Renal failure requiring new hemodialysis was observed in 5 patients (11.4%). There were 9 patients (20.5%) with early major adverse events (in-hospital death, stroke, spinal cord ischemic injury, renal failure requiring new hemodialysis, and prolonged intubation). Multivariable logistic regression analysis demonstrated that a history of abdominal aortic aneurysm repair (odds ratio 17.711, 95% confidence interval 1.274e246.426, P ¼ 0.032) was the only independent predictor of early major adverse events. Deep hypothermic circulatory arrest was not an independent predictor of early major adverse events. At 5 years, overall freedom from death was 89.4 ± 6.1%. Conclusion: Moderate to deep hypothermia as a constituent of proximal aortic management was safe and effective in patients undergoing open repair of thoracoabdominal aortic aneurysm.
INTRODUCTION The surgical treatment of thoracoabdominal aortic aneurysm (TAAA) still carries high mortality and morbidity despite improvements in surgical approaches and postoperative management. Hypothermia is considered an effective method for brain and spinal cord protection during open surgical repair for TAAA. Moreover, deep hypothermic circulatory arrest (DHCA) has several benefits
Department of Cardiovascular Surgery, Sakakibara Heart Institute, Tokyo, Japan. Correspondence to: Toshihiro Fukui, MD, Department of Cardiovascular Surgery, Kumamoto University Hospital, 1-1-1 Honjo, Chuo-ku, Kumamoto 860-8556, Japan; E-mail: [email protected] Ann Vasc Surg 2016; 31: 39–45 http://dx.doi.org/10.1016/j.avsg.2015.08.021 Ó 2016 Elsevier Inc. All rights reserved. Manuscript received: June 30, 2015; manuscript accepted: August 21, 2015; published online: November 23, 2015.
including minimal aortic dissection, the elimination of the need for a proximal clamp, a bloodless field, and reduced potential for atheromatous embolization.1 Many investigators have demonstrated the safety and effectiveness of DHCA with favorable outcomes in a large number of patients.1e6 However, there has been a reluctance to use DHCA among other surgeons, largely because of a perception that there is a vastly increased risk of bleeding complications.6 Furthermore, prolonged operation time during cooling and rewarming may be of some concern. We have adopted a modified hypothermic strategy that can be used as a constituent of proximal aortic management. When the proximal aorta could not be clamped or clamping was decided against, DHCA (<25 C) was used during the proximal aortic anastomosis. Otherwise, moderate hypothermia (25e30 C) with a sequential clamp was used. This strategy may have several advantages as regards 39
40 Fukui and Takanashi
neural protection, embolization, and bleeding complications in accord with patients’ conditions. In this study, early and mid-term outcomes were assessed after our modified hypothermic strategy for the surgical repair of TAAA.
PATIENTS AND METHODS Patients Between April 2009 and March 2015, 44 patients underwent TAAA repair using total cardiopulmonary bypass and our modified hypothermic strategy at Sakakibara Heart Institute. Another 5 patients who underwent left heart bypass during the study period were excluded. Preoperative characteristics of all patients are shown in Table I. There were 15 female (34.1%) and 29 male patients (65.9%). Crawford type II or III TAAA was observed in 26 patients (59.1%). There were 18 chronic dissections (40.9%) and 26 degenerative aneurysms (59.1%). Emergent surgery was performed in 6 patients (13.6%) because of rupture. Nineteen patients had undergone previous proximal aortic surgery (Bentall in 2 patients, ascending aorta in 4, total aortic arch in 11, and descending thoracic aorta in 7). No patients had a previously implanted stent graft. The Institutional Review Board approved this retrospective study and waived the need for written consent. Operative Technique Preoperative computed tomography (CT) with contrast enhancement was performed to detect the Adamkiewicz artery in nonemergent patients. Cardiac anesthesiologists placed all spinal drains in the operating room 1 day before the operation in patients undergoing elective surgery. However, spinal drainage was not inserted in patients undergoing emergent surgery and those with technical difficulty. The cerebrospinal pressure was monitored continuously during surgery and the early postoperative period. Cerebrospinal fluid was freely drained with gravity whenever cerebrospinal pressure exceeded 10 mm Hg. In patients without a spinal cord deficit, the drain was removed on postoperative day 2. Intraoperative motor-evoked potentials or somatosensory evoked potentials were not used. Posterolateral incision through the fifth to seventh intercostal space, according to the extent of TAAA, was performed. The diaphragm was incised circumferentially and a retroperitoneal approach was taken without opening the peritoneum.
Annals of Vascular Surgery
Table I. Preoperative variables Preoperative variables of all patients
All (n ¼ 44)
Age Female gender Crawford extent Type I Type II Type III Type IV Type V Dissection Hypertension Diabetes mellitus Hyperlipidemia Smoking history Marfan syndrome Chronic kidney disease Chronic obstructive pulmonary disease Emergent History of stroke History of proximal aortic surgery History of abdominal aortic surgery
65.6 ± 14.4 15 (34.1%) 3 9 17 8 7 18 42 4 17 29 5 3 2 6 3 19 7
(6.8%) (20.5%) (38.6%) (18.2%) (15.9%) (40.9%) (95.5%) (9.1%) (38.6%) (65.9%) (11.4%) (6.8%) (4.5%) (13.6%) (6.8%) (43.2%) (15.9%)
Arterial cannulation was performed via the left femoral artery in all patients. Additional left axillary arterial or ascending aortic cannulation was performed to prevent embolization to the brain when the preoperative contrast-enhanced CT detected extensive atheromatous plaques in the aorta. Venous cannulation was performed via the left femoral vein. Left heart venting was effected through the left upper pulmonary vein when possible. Our strategy is to use moderate to deep hypothermia during open repair of TAAA for organ protection in all patients. DHCA (<25 C) was applied when open proximal anastomosis was necessary (n ¼ 18). Otherwise, proximal anastomosis with an aortic clamp was performed with moderate (25e30 C) hypothermia without circulatory arrest (n ¼ 26). Open proximal anastomosis was used in situations including no space between aneurysm and left subclavian artery, severe adhesions because of previous proximal aortic operations, vulnerable aortic wall with a dissection, and multiple atheromatous plaques. When open proximal anastomosis was applied, left axillary arterial or ascending aortic perfusion was stopped at the time of aortic incision. Irrespective of proximal management, distal clamping was performed in all patients to perfuse the visceral organs and spinal cord with partial cardiopulmonary bypass. After the anastomosis between the proximal aortic stump and the prosthesis graft, perfusion to the upper body was resumed via a left
Volume 31, February 2016
axillary arterial or ascending aortic cannula in patients undergoing open repair with DHCA. This graft is a 20- to 22-mm Dacron straight tube graft. After completion of the proximal anastomosis in patients undergoing DHCA, they were rewarmed to 25e 30 C. The decision of using DHCA with open proximal anastomosis or moderate hypothermia with proximal clamp was made by preoperative CT and confirmed during operation. Sequential clamping of the descending aorta was performed in all patients. The first clamp was just distal to the proximal aortic anastomosis. The second clamp was applied just above the celiac artery. After opening the descending aorta by removing the first clamp, the major 1 or 2 pairs of intercostal arteries were identified and attached to the side hole of the tube graft. These arteries were generally identified from the preoperative CT. Other minor branches were ligated. Back-bleeding from the intercostal arteries was controlled by inserting 2F balloon-tipped catheters into the ostia to prevent spinal cord ischemia arising from a steal phenomenon. We use the straight tube graft from the proximal anastomosis to the reattachment of intercostal arteries because the handling of a tube graft is satisfactory and the hemostasis is easily confirmed. Perfusion to the intercostal artery was resumed with circulation from the upper body. The 4-branched Dacron graft was anastomosed to the distal end of the tube graft. The third clamp was applied at the infrarenal portion of the aorta, and the abdominal aorta was opened. The celiac, superior mesenteric, and bilateral renal arteries were immediately cannulated and perfused. Celiac and superior mesenteric arteries were perfused with blood by a single roller pump (200 mL/min in total). Bilateral renal arteries were perfused with cold crystalloid solution (250 mL each) intermittently (every 20 min). Each visceral artery was detached individually with a small cuff of aortic wall. The right renal artery, left renal artery, superior mesenteric artery, and celiac artery were anastomosed to the side branches of the prosthetic graft in sequence. Perfusion to each artery was resumed from the upper perfusion sequentially. The major intercostal artery at the level of the celiac artery or superior mesenteric artery was reconstructed using an 8-mm graft interposition when the Adamkiewicz artery was identified. The inferior mesenteric artery was sacrificed in all patients. Final clamping was performed at the distal aorta or bilateral common iliac arteries. At this point, femoral arterial perfusion was stopped and final distal anastomosis was performed. Rewarming was initiated after the reattachment of the intercostal arteries. Cardiopulmonary bypass
Hypothermia in thoracoabdominal repair 41
was discontinued when the bladder temperature reached 35.0 C. Definitions Chronic kidney disease was defined as creatinine level more than 1.5 mg/dL. In-hospital death was defined as death within the same hospitalization period or within 30 days of surgery. Postoperative stroke was defined as the occurrence of a new stroke confirmed by CT. In patients with preoperative stroke, postoperative stroke was defined as a worsening of the neurological deficit with new radiological findings. Spinal cord ischemic injury included permanent paraplegia and paraparesis. Prolonged intubation was defined as a requirement for ventilation longer than 48 hr. Perioperative myocardial infarction was defined as new Q waves on electrocardiography or a peak creatine kinase MB level 5 times the upper limit of normal (25 IU/L). Early major adverse events included inhospital death, stroke, spinal cord ischemic injury, renal failure requiring new hemodialysis, and prolonged intubation. Statistical Analysis All statistical analyses were performed using the StatView 5.0 software package (SAS Institute, Inc., Cary, NC). Continuous variables are reported as mean ± standard deviation. Continuous variables were compared using the ManneWhitney U-test and discrete variables were compared using the c2 test or Fisher’s exact test. Differences were considered significant at P < 0.05. Univariate and multivariate logistic regression analyses were performed to determine the significant predictors of early major adverse events. The variables used for univariate analysis were the clinical variables listed in Table I and DHCA. Variables identified as having a P value of <0.1 on univariate analyses were considered for inclusion in the multivariate model. Actuarial event-free survival curves were estimated by the KaplaneMeier method. The log-rank test was used to assess differences in survival between groups.
RESULTS Early Outcomes The operative data are listed in Table II. The reasons for selecting DHCA were as follows: no space between aneurysm and left subclavian artery in 6 patients, severe adhesions because of previous
42 Fukui and Takanashi
Annals of Vascular Surgery
Table II. Operative and postoperative data Operative and postoperative data of all patients All (n ¼ 44)
Minimal bladder temperature ( C) Cerebrospinal drainage Coronary artery bypass grafting Operation time (min) Cardiopulmonary bypass time (min) 30-Day mortality In-hospital mortality Major adverse events Stroke Spinal cord ischemic injury Renal failure requiring newly hemodialysis Prolonged intubation (>48 hr) Tracheostomy Reexploration for bleeding Low output syndrome Gastrointestinal complications Transfusion of red blood cells (U) Postoperative stay (day)
27.8 ± 4.5 32 (72.7%) 1 (2.3%) 329.1 ± 87.6 118.8 ± 47.2 0 1 (2.3%) 9 (20.5%) 2 (4.5%) 4 (9.1%) 5 (11.4%) 5 (11.4%) 2 (4.5%) 0 0 0 9.9 ± 4.5 28.9 ± 48.5
proximal aortic operations in 6, vulnerable aortic wall with a dissection in 2, and severe atheromatous plaques in 4. Cerebrospinal drainage was inserted preoperatively in 32 patients (72.7%). The reasons of not being feasible for cerebrospinal drainage were emergent operation in 6 patients and technical difficulty in 6. Coronary artery bypass grafting (left internal thoracic artery to left anterior descending artery) was concomitantly performed in 1 patient. There was no 30-day mortality; however, inhospital mortality was observed in 1 patient (2.3%), whose cause of death was stroke. There were 9 patients (20.5%) with early major adverse events in all patients. Of these, spinal cord ischemic injury was observed in 4 patients (9.1%). There was no patient with transient spinal cord ischemic injury in this study. Renal failure requiring new hemodialysis was observed in 5 patients (11.4%); however, they did not need chronic hemodialysis at discharge. There was no patient with low output syndrome. The mean postoperative hospital stay was 28.9 days, with a median of 15 days. Predictors of Early Major Adverse Events On univariate analysis, Crawford type II or III (P ¼ 0.069), chronic kidney disease (P ¼ 0.079), a history of abdominal aortic surgery (P ¼ 0.036), and DHCA (P ¼ 0.090) were selected for further multivariate analysis. Multivariable logistic regression analysis (Table III) demonstrated that a history
of abdominal aortic surgery (P ¼ 0.032) was only independent predictor of early major adverse events. Mid-term Outcome Follow-up was completed in all patients. During the follow-up period (29.1 ± 18.8 months), there were 3 deaths (6.8%) including 1 in-hospital death. The causes of the other 2 deaths were pneumonia at 5.2 months and sudden death at 12.6 months after the operation. The actuarial survival rate at 5 years was 89.4 ± 6.1% in all patients (Fig. 1).
DISCUSSION This study demonstrated that a modified hypothermic strategy (moderate or deep) with respect to proximal aortic management was safe and effective in patients undergoing open repair of TAAA, with favorable early and mid-term survival rates. Hypothermia has been considered safe and effective for protecting the central nervous system during complex cardiac and vascular surgery. Moreover, DHCA has several benefits including minimal aortic dissection, the elimination of the need for a proximal clamp, a bloodless field, and a reduced potential for the atheromatous embolization.1 Several investigators have reported the usefulness of DHCA in patients undergoing a repair of TAAA. Kouchoukos et al.1 evaluated their 26-year experience using DHCA in patients undergoing TAAA repair. In their analysis, the rates of 30-day mortality, stroke, spinal cord ischemic injury, and new dialysis were 7.8%, 3.7%, 5.3%, and 3.7%, respectively. They described that hypothermia increases ischemic tolerance and allows unhurried aortic reconstruction, and concluded that their results compared favorably with those using alternative open and currently used endovascular and hybrid debranching surgical techniques.3 Fehrenbacher et al.2 reported outcomes after open repair using DHCA in patients with descending thoracic aortic aneurysm and TAAA. Operative mortality was 5.7% (14/245) in selected patients undergoing TAAA repair. Other morbidity rates included 4.5% for stroke, 4.1% for spinal cord ischemic injury, and 2% for new dialysis. They described that the use of open repair with DHCA can visualize the inside of the arch during circulatory arrest, which gives the surgeon the ability to avoid or remove severely atherosclerotic segments, perform endarterectomy of very calcified segments, and assess the need for arch branch bypasses or total arch replacement. Indeed, Fehrenbacher et al. performed total arch replacement concomitantly in 5.5% of the
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Hypothermia in thoracoabdominal repair 43
Table III. Multivariate logistic regression analyses for early major adverse events Variable
Odds ratio
95% Confidence P value interval
History of abdominal 17.711 0.032 aortic surgery Crawford type II or III 9.488 0.111 Deep hypothermic 2.775 0.320 circulatory arrest Chronic kidney 0.873 0.940 disease
1.274e246.426 0.595e151.249 0.371e20.735 0.025e30.321
Fig. 1. KaplaneMeier event-free survival analysis for allcause mortality.
patients. Weiss et al.5 compared DHCA with mild hypothermia without circulatory arrest in patients undergoing descending thoracic aortic and TAAA repair using a propensity score-matching method. In their analysis, significantly lower rates of acute renal failure and liver failure were observed in the DHCA group. However, reports of excellent results after open repair with DHCA in patients with TAAA are limited, and some adverse effects have been reported by other groups. Safi et al.7 reported 21 patients undergoing open repair with DHCA out of 409 patients who underwent repair of descending thoracic aortic aneurysm and TAAA. The reason for selecting DHCA was an inability to gain proximal aortic control because of anatomic or technical difficulty. The outcomes of these patients were not favorable; 30-day mortality, stroke, and spinal cord ischemic injury were observed in 29%, 13%, and 13% of the patients, respectively. Furthermore, the pulmonary complication rate was very high (67%). Safi et al. concluded that the judicious application of this method in rare instances when proximal control is not feasible or there is catastrophic intraoperative bleeding leaves the surgeon with no other option. Coselli et al.8 similarly reported their
results of open repair with DHCA in patients with descending thoracic aortic aneurysm and TAAA. In their institute this technique was used when the location, extent, and severity of disease precluded placement of a proximal aortic clamp. The 30-day mortality, stroke, and renal failure were 21%, 9%, and 15%, respectively. Although these results were not favorable, the incidence of paraplegia was only 1% better than that performed with a non-DHCA technique. Therefore, Coselli et al. concluded that DHCA will continue to play an important role in organ protection, primarily as applied to the spinal cord, in patients at extreme risk of ischemic complications, such as those with Crawford type II aneurysms. In this study, we developed the modified strategy of using hypothermia during proximal aortic management. We agree that hypothermia is effective in reducing the rate of spinal cord ischemic injury and is useful for visceral organ protection. However, it has been suggested that DHCA has disadvantages which include coagulopathy, cold injury to the lung, inflammatory consequences of cardiopulmonary bypass, and retraction injury of the heparinized left lung.8 Moreover, prolonged operation time during cooling and rewarming may be of some concern among surgeons. Our strategy is consistent with the hypothermic strategy. All patients were cooled to at least moderate hypothermia as soon as the cardiopulmonary bypass started. When the proximal aorta could not be clamped or clamping was decided against, then DHCA was used during the proximal aortic anastomosis. Otherwise, proximal clamping with moderate hypothermia was performed. Indeed, in this study, the operation time was longer in patients with DHCA than those without DHCA (379.1 vs. 294.5 min, P ¼ 0.002). However, DHCA was not an independent predictor of early major adverse events with multivariable logistic regression analysis. The potential advantage of our strategy lies in it being easy to switch to DHCA in patients who need open proximal anastomosis during surgery, although not all patients need deep hypothermia. In this study, the rate of renal failure requiring new hemodialysis was high (5 patients, 11.4%). The introduction of hemodialysis takes place early in our institute, following the article by Karvellas et al.9 describing that earlier institution of renal replacement therapy in critically ill patients with acute kidney injury may have a beneficial impact on survival. In our institute, the indications are based on the Risk, Injury, Failure, Loss, and Endstage kidney classification.10 When an increase in serum creatinine by 1.5 times or a urine output <0.5 mL/kg/hr 6 hr is observed, then
44 Fukui and Takanashi
hemodialysis is initiated. Such patients are all treated with continuous venovenous hemodiafiltration. Zarbock et al.11 described the advantage of continuous venovenous hemodialysis over intermittent hemodialysis in critically ill patients, including greater hemodynamic and metabolic stability, increased time-averaged dialysis dose, and removal of proinflammatory cytokines. It can also provide better control of fluid balance and solute removal. Owing to early continuous treatments for postoperative renal failure, none of the 4 patients progressed to chronic renal failure. In this study, a history of abdominal aortic surgery was only an independent predictor of early major adverse events. Some investigators demonstrated that a history of abdominal aortic surgery was one of the independent predictors of major complications after thoracoabdominal aortic repair. Schl€ osser et al.12 in their meta-analysis revealed that prior abdominal aortic aneurysm repair was a significant risk factor for neurological deficit and for developing renal failure after TAAA surgery with relative risks of 2.90 (95% confidence interval [CI] 1.26e6.65, P ¼ 0.008) and 3.47 (95% CI 1.74e 6.91, P ¼ 0.0001), respectively. The importance of collateral flow from the infrarenal and pelvic circulation to the spinal cord has been described.13,14 This collateral flow is greatly reduced or eliminated during infrarenal abdominal aortic aneurysm repair, exposing susceptible patients to an increased risk of paraplegia after subsequent TAAA repair. The same mechanism may be the possible reason for a history of abdominal aortic surgery as the only independent predictor of early major adverse events in this study. Mid-term and long-term survival of patients who underwent surgery for TAAA has not been well documented. Kouchoukos et al.1 reported a 5-year survival of 55%, and Fehrenbacher et al.2 reported 69.3% survival in patients with descending thoracic aortic aneurysm and TAAA. However, other analyses including only more recent cases demonstrated favorable mid-term outcomes. Wong et al.15 reported a 2-year survival rate of 79.1% in patients undergoing TAAA repair, Okita et al.16 reported a 5-year survival of 83.6%, and Johns et al.17 reported that 5-year survival was 79.7% in patients younger than 60 years undergoing TAAA repair. Recent intraoperative anesthetic and perfusion techniques and postoperative intensive care management strategies have been improved and have contributed to better outcomes in patients undergoing open repair of TAAA. This study has the following limitations: (1) this is a retrospective observational study; (2) the number
Annals of Vascular Surgery
of patients and the follow-up period of 5 years might not be sufficient to provide definitive results; and (3) because there was no control group, we cannot conclude that moderate to deep hypothermia is superior to traditional techniques in patients undergoing TAAA repair.
CONCLUSIONS A modified hypothermic strategy (moderate or deep) with respect to proximal aortic management was safe and effective in patients undergoing open repair of TAAA, with favorable early and mid-term survival rates. Further studies that include larger sample sizes are needed. REFERENCES 1. Kouchoukos NT, Kulik A, Castner CF. Outcomes after thoracoabdominal aortic aneurysm repair using hypothermic circulatory arrest. J Thorac Cardiovasc Surg 2013;145: S139e41. 2. Fehrenbacher JW, Siderys H, Terry C, et al. Early and late results of descending thoracic and thoracoabdominal aortic aneurysm open repair with deep hypothermia and circulatory arrest. J Thorac Cardiovasc Surg 2010;140:S154e60. 3. Kulik A, Castner CF, Kouchoukos NT. Outcomes after thoracoabdominal aortic aneurysm repair with hypothermic circulatory arrest. J Thorac Cardiovasc Surg 2011;141:953e60. 4. Sundt TM, Fleming MD, Oderich GS, et al. Spinal cord protection during open repair of thoracic and thoracoabdominal aortic aneurysm using profound hypothermia and circulatory arrest. J Am Coll Surg 2011;212:678e83. 5. Weiss AJ, Lin HM, Bischoff MS, et al. A propensity scorematched comparison of deep versus mild hypothermia during thoracoabdominal aortic surgery. J Thorac Cardiovasc Surg 2012;143:186e93. 6. Griepp RB, Di Luozzo G. Hypothermia for aortic surgery. J Thorac Cardiovasc Surg 2013;145:S56e8. 7. Safi HJ, Miller CC 3rd, Subramaniam MH, et al. Thoracic and thoracoabdominal aortic aneurysm repair using cardiopulmonary bypass, profound hypothermia, and circulatory arrest via left side of the chest incision. J Vasc Surg 1998;28:591e8. 8. Coselli JS, Bozinovski J, Cheung C. Hypothermic circulatory arrest: safety and efficacy in the operative treatment of descending and thoracoabdominal aortic aneurysms. Ann Thorac Surg 2008;85:956e63. 9. Karvellas CJ, Farhat MR, Sajjad I, et al. A comparison of early versus late initiation of renal replacement therapy in critically ill patients with acute kidney injury: a systematic review and meta-analysis. Crit Care 2011;15:R72. 10. Hoste EA, Clermont G, Kersten A, et al. RIFLE criteria for acute kidney injury are associated with hospital mortality in critically ill patients: a cohort analysis. Crit Care 2006;10:R73. 11. Zarbock A, Singbartl K, Kellum JA. Evidence-based renal replacement therapy for acute kidney injury. Minerva Anestesiol 2009;75:135e9. 12. Schl€ osser FJ, Mojibian H, Verhagen HJ, et al. Open thoracic or thoracoabdominal aortic aneurysm repair after previous abdominal aortic aneurysm surgery. J Vasc Surg 2008;48: 761e8.
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13. Lombardi JV, Carpenter JP, Pochettino A, et al. Thoracoabdominal aortic aneurysm repair after prior aortic surgery. J Vasc Surg 2003;38:1185e90. 14. Szilagyi DE. A second look at the etiology of spinal cord damage in surgery of the abdominal aorta. J Vasc Surg 1993;17:1111e3. 15. Wong DR, Parenti JL, Green SY, et al. Open repair of thoracoabdominal aortic aneurysm in the modern surgical era:
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contemporary outcomes in 509 patients. J Am Coll Surg 2011;212:569e79. 16. Okita Y, Omura A, Yamanaka K, et al. Open reconstruction of thoracoabdominal aortic aneurysms. Ann Cardiothorac Surg 2012;1:373e80. 17. Johns N, Jamieson RW, Ceresa C, et al. Contemporary outcomes of open repair of thoracoabdominal aortic aneurysm in young patients. J Cardiothorac Surg 2014;9:195.