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Ann Thorac Surg 2008;86:1815-1819. doi:10.1016/j.athoracsur.2008.07.104
© 2008 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

Distal Aortic Reinterventions After Root Surgery in Marfan Patients

Evaldas Girdauskas, MD*, Thomas Kuntze, MD, Michael A. Borger, MD, PhD, Volkmar Falk, MD, PhD, Friedrich Wilhelm Mohr, MD, PhD

Department of Cardiac Surgery, Heart Center Leipzig, Leipzig, Germany

Accepted for publication July 29, 2008.

* Address correspondence to Dr Girdauskas, Department of Cardiac Surgery, Heart Center Leipzig, Strümpellstrasse 39, Leipzig, 04289, Germany (Email: evagird{at}centras.lt).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: Distal aortic disease may evolve in Marfan patients after aortic root surgery. The aim of this study was to analyze the results of distal aortic reoperations in Marfan patients after proximal aortic surgery.

Methods: A total of 95 Marfan patients (56 male; mean age 34.5 ± 10.9 years) have been followed or operated on at our institution between October 1994 and December 2007. Results of patients who required distal aortic reinterventions after root surgery were collected and analyzed.

Results: Fifteen Marfan patients (9 male; mean age 39.1 ± 7.5 years) underwent distal aortic reinterventions after aortic root surgery. The indications for distal reoperations consisted of dissecting aneurysm after type A dissection surgery in 12 patients (80%) and nondissecting aneurysm in 3 patients (20%). Type A dissection during initial aortic root surgery was the only independent predictor of distal aortic reoperation (hazard ratio 3.8). One patient (6.7%) died perioperatively. Neurologic morbidity consisted of 1 patient with paraplegia and 1 with temporary paraparesis, and no strokes. Two patients died during a mean follow-up of 36.2 ± 25.5 months. Survival was 91.7% ± 1.6% at 1 and 5 years postoperatively. Three patients undergoing reoperative arch procedures required additional interventions on the distal aorta during follow-up.

Conclusions: Distal aortic reoperations in Marfan patients are more common among those presenting with type A dissection. Although technically challenging, such procedures can be performed with good short- and long-term results. Complete aortic arch replacement with an elephant trunk technique, if it can be safely performed, should be considered for Marfan patients presenting with type A dissection.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Aortic root dilatation is a typical vascular lesion in patients with Marfan syndrome. The surgical therapy of proximal aortic disease is well established and produces excellent long-term results, with 10-year survival of approximately 80% [1–3]. Prolonged survival after root surgery has led to an increased number of patients who experience aortic complications beyond the aortic root [4]. Distal aortic disease progression is not uncommon in Marfan patients after aortic root surgery, but the precise incidence is not well defined. A recent analysis of the Euro Heart Survey database [5] showed that the diameter of the distal aorta was greater in patients who had undergone aortic root surgery than in patients without such intervention.

The aim of this report was to analyze the incidence of distal aortic lesions in Marfan patients after aortic root surgery, as well as to review the perioperative and long-term outcomes for the distal aortic reoperations.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
We reviewed our institutional aortic surgery database to identify Marfan patients treated at Heart Center Leipzig between October 1994 and December 2007. A total of 95 patients with Marfan syndrome (56 male; mean age 34.5 ± 10.9 years), defined according to the current Ghent criteria, were treated at our institution over this period (see Table 1). A total of 58 patients (61%) underwent aortic root surgery as the initial procedure, including 27 patients (28%) who were operated on emergently for acute type A aortic dissection. Eighteen patients have not been operated on but are being followed by our surgical outpatient clinic because of small aortic aneurysms or less than severe mitral insufficiency (Table 1).


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  		Table 1 Characteristics of All Marfan Patients Treated and Followed During the Study Period
 
Fifteen Marfan patients required a total of 18 distal aortic reinterventions after root/ascending aortic surgery, and serve as the focus of the current study. Approval of the Ethics Committee of the University Leipzig (Reg. No. 109-2006) for conducting this study was obtained in June 2006. Individual patient consent was waived.

Demographic, clinical, and serial imaging data of this patient subset were analyzed. The indication for secondary surgical procedures in the subgroup of patients with persisting dissection after type A surgery consisted of progressive aneurysmal enlargement of the downstream aorta to greater than 55 mm in 8 patients, a rapidly expanding aneurysm (> 5 mm in 6 months) in 2 patients, and impending aortic rupture in 2 patients. Two patients in the subgroup after elective root surgery had reached a descending aortic diameter of greater than 55 mm, and 1 such patient was operated on for a rapidly expanding aneurysm. We did not observe any acute type B dissection after elective root surgery. The distal aortic reoperation could be performed on an elective basis in most cases (80%).

Surgical Technique
The surgical technique used for distal procedures was dependent on the aortic pathology. Median repeat sternotomy was used for surgical exposure in 4 patients with persistent dissection after type A surgery, who required an arch/proximal descending aortic procedure. Cardiopulmonary bypass (CPB) was established through right axillary perfusion and right femoral venous drainage in all of these patients. The composite valve graft prosthesis was clamped, and antegrade crystalloid cardioplegia was administered. Circulatory arrest was instituted at a rectal temperature of 22oC. Selective antegrade cerebral perfusion at 10 mL · kg–1 · min–1 was performed by clamping the brachiocephalic artery and inserting a perfusion catheter into the left common carotid artery. The left subclavian artery was occluded by a balloon catheter. The head was packed externally in ice during circulatory arrest. The chronically dissected aortic arch and proximal descending aorta were resected, and the intimal membrane was trimmed distally down into the descending aorta. The distal anastomosis was performed using an elephant trunk technique. Reimplantation of the supra-aortic vessels using separate grafts was used only if the arch vessels were found to be dissected. Proximal prosthesis-to-prosthesis anastomosis was performed as the last stage during rewarming. Simultaneous aortic root replacement with a homograft was performed in 1 of these 4 patients because of concomitant aortic valve prosthetic endocarditis (Staphylococcus aureus). Bilateral thoracotomy in the third intercostal space with transverse sternotomy (partial clamshell incision) was used for surgical exposure in 1 Marfan patient with a severe chest deformity.

The remaining 11 patients (8 of them with persistent dissection after type A surgery) were operated on through a left-sided incision, namely, a posterolateral thoracotomy, or a thoracoabdominal incision, depending on the distal extent of aortic replacement. The left femoral vessels were cannulated for CPB in all such patients. Cerebrospinal fluid drainage (introduced in the late 1990s at our institution) was used to minimize the risk of paraplegia, with a goal of keeping the cerebrospinal fluid pressure below 10 cm H2O intraoperatively and postoperatively. Cross-clamping of the proximal descending aorta beneath the left subclavian artery was possible in 9 of these 11 patients. Such patients were operated on under left-side heart bypass and mild hypothermia of 32oC. The intercostal arteries were reimplanted selectively in the lower thoracic to upper lumbar segments in 12 patients. Extent of distal replacement was dependent on the pathology of the diseased aorta and varied from isolated descending aortic replacement to complete thoracoabdominal replacement with bi-iliac anastomoses. Replacement of the abdominal aorta was performed with a second Dacron (C. R. Bard, Haverhill, Pennsylvania) graft under selective perfusion of the visceral organs with cold blood at 1.0 L/min. Distal perfusion was reinstituted through the femoral cannula and the proximal-to-distal prosthetic anastomosis was accomplished as the last stage. Cardiopulmonary bypass was discontinued after reaching a rectal temperature of 35oC.

Two patients of the 11 operated on through a left-sided incision required full CPB and deep hypothermic circulatory arrest to replace a chronically dissected distal aortic arch, since the arch was not adequately addressed during the initial procedure. Circulatory arrest was induced at 22°C while the aorta was cross-clamped at the lower descending segment. The lower body was subsequently perfused at 1.0 L/min through the femoral cannula. An open distal hemiarch replacement was accomplished using a Dacron prosthesis with a side-arm graft. Transapical venting was used for left heart decompression and for deairing after completing the aortic arch anastomosis. Perfusion of the upper body was restored through the side-arm graft after careful deairing of the heart and supra-aortic vessels. Distal perfusion through the femoral artery was stopped thereafter, and the cross-clamp on the descending aorta was removed.

Follow-Up and Statistical Analysis
Follow-up was performed for 100% of patients and consisted of a written questionnaire sent to the patients and their family physicians. Serial imaging data obtained during the late postoperative course (echocardiography reports, computed tomography and magnetic resonance images) were obtained from the patients' family physicians and cardiologists.

All statistical analyses were performed with the SPSS version 14.0 (SPSS, Chicago, Illinois). Categorical variables are expressed as percentages, and continuous variables are expressed as mean ± SD throughout the manuscript. Standard definitions were used for patient variables and outcomes. In particular, hospital mortality was defined as death during the same hospitalization. Long-term survival was analyzed with the method of Kaplan-Meier. The Cox regression model was used to analyze the independent risk factors for distal aortic reoperations. All variables were screened in the univariate analysis and considered for clinical relevence before including them in multivariate model.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
The mean interval between root surgery and distal aortic reoperation was 45.1 ± 32.3 months (range, 2 to 120). Three patients required distal reoperations (9.7%) in the group of 31 elective root replacements versus 12 patients (44.4%) in the group of 27 patients after acute type A dissection surgery (p = 0.003). Characteristics of the 15 patients requiring distal aortic reinterventions are summarized in Table 2. The maximal diameter of the descending thoracic aorta at the time of distal reintervention was 56.8 ± 11.6 mm (range, 40 to 82 mm). A total of 5 patients were operated on for distal aortic aneurysm of maximal diameter 50 mm or less because of impending rupture or a rapidly expanding aneurysm. One patient was operated on emergently for a dissecting aneurysm with a luminal diameter of only 40 mm because of sealed aortic rupture in the proximal descending segment.


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  		Table 2 Characteristics of Patients Requiring Distal Aortic Reinterventions After Aortic Root Surgery
 
The duration of CPB or left-side heart bypass was 152.9 ± 52.8 minutes. Cross-clamping of the ascending aorta and cardioplegic arrest was used in 4 patients with a mean time of 98.0 ± 52.6 minutes. Six patients were operated on under circulatory arrest (mean duration, 28.6 ± 17.9 minutes) at a rectal temperature of 21.0° ± 0.8°C. Simultaneous selective antegrade cerebral perfusion was used in all circulatory arrest cases. Distal extent of aortic replacement in the subgroup of patients after type A dissection surgery (n = 12) included aortic arch with elephant trunk anastomosis in 4 patients, and thoracoabdominal aorta in 8 patients (complete replacement to aortic bifurcation with bi-iliac anastomoses). Two descending aortic replacements and 1 thoracoabdominal replacement were required in the subgroup of patients after elective root surgery (n = 3). Selective perfusion of the visceral organs with cold blood was performed in all thoracoabdominal cases.

One patient died while in hospital, corresponding to a mortality rate of 6.7%. The predicted logistic EuroSCORE (European System for Cardiac Operative Risk Evaluation) risk of mortality for the entire patient cohort was 32.0% ± 22.2%. The single patient died after thoracoabdominal surgery for dissecting aortic aneurysm because of massive pulmonary embolism after a prolonged intensive care unit stay of 12 days. The postmortem examination showed an extensive venous thrombosis of the right common iliac vein.

The mean intensive care unit length of stay was 7.7 ± 6.9 days. Prolonged length of stay in the intensive care unit (more than 10 days) was required predominantly for pulmonary problems in 4 patients (26.7%). Three patients (20%) required rethoracotomy because of excessive postoperative bleeding. The median time on mechanical ventilation postoperatively was 28.5 hours (range, 3 to 516). Three patients (20%) required temporary tracheostomy for prolonged weaning from the respirator. Acute renal failure requiring hemodialysis occurred in 2 patients (13.3%). Spinal cord injury occurred in 2 patients—paraplegia in the first patient and temporary paraparesis in the second. Both neurologic events had a delayed onset, occurring on the second and third postoperative day after an uneventful initial recovery from general anesthesia. These 2 patients underwent replacement of the entire thoracoabdominal aorta for dissecting aneurysm (namely, persistent dissection after type A surgery). However, only 1 patient had a permanent spinal cord injury of the 11 who underwent replacement of the complete descending or thoracoabdominal aorta, resulting in a paraplegia rate of 9.1%. No patient had postoperative stroke. The postoperative length of hospital stay ranged from 12 to 80 days (mean stay, 26.6 ± 23.6).

Follow-up information was available for all discharged patients, with a mean follow-up period of 36.2 ± 25.5 months (range, 2 to 120). Two patients died during follow-up. The first patient died 70 months after discharge because of extensive stroke. The second patient died 63 months after distal aortic reoperation because of chronic heart failure. The 1- and 5-year survival was 91.7% ± 1.6% at both time intervals.

Three patients required additional interventions on the downstream aorta. All of these patients had initial surgery for acute type A dissection and underwent distal arch/proximal descending aortic procedure at the second stage, with a required replacement of the entire thoracoabdominal aorta performed at the third stage.

A total of 5 variables (of 26 included) reached statistical significance in the univariate model and were analyzed in the Cox regression model for independent risk factors for distal aortic reoperations in the entire cohort of patients undergoing initial aortic root surgery. Aortic dissection at the time of initial surgery was identified as the only significant risk factor (hazard ratio 3.8; Table 3).


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  		Table 3 Cox Regression Analysis of Risk Factors for Distal Aortic Reoperations
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The incidence of aneurysmal dilatation of the distal aorta after proximal aortic surgery is not well defined, but is known to occur not infrequently. It has been reported that 5% to 35% of Marfan patients who underwent proximal aortic surgery will require further operations on the aorta, depending upon the extent of previous surgery and the quality of follow-up [4]. A recent analysis of the Euro Heart Survey database [5] showed that the diameter of the distal aorta was greater in patients who had undergone aortic root surgery than in patients without such an intervention. The most plausible explanation for this finding is a deeper penetrance of cardiovascular manifestations in these Marfan patients, underscoring the need to classify them as a high-risk population for distal aortic events. Moreover, Scharfschwerdt and colleagues [7] found significantly increased wall tension and rate of pressure rise in the residual aorta after prosthetic replacement of the ascending aorta in an in-vitro model, which may also increase the risk of distal aortic surgery.

Known risk factors for late aortic reoperation in Marfan patients include aortic dissection at the time of initial surgery, hypertension, and smoking history [6]. Our study revealed similar findings in that aortic dissection was the initial event in 80% of Marfan patients requiring distal reoperation. Furthermore, distal reinterventions were more commonly required in type A dissection patients than patients who initially underwent elective surgery of the aortic root for aneurysmal disease (44.4% versus 9.7%, p = 0.003; Fig 1). Cox regression analysis identified aortic dissection as the only significant risk factor for distal aortic reoperation in our patient population (hazard ratio 3.8).


Figure 1
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  		Fig 1. Freedom from distal reoperations after aortic root surgery.

 
Based on our findings and those of other investigators, we recommend strongly considering complete aortic arch replacement with an elephant trunk anastomosis during the initial type A dissection surgery in Marfan patients, provided that the surgeon believes that it can be safely performed. Such a recommendation has also been made by other authors [8–10]. The main advantage of such an approach is avoidance of repeat sternotomy for distal aortic reintervention and simplification of the secondary procedure on the downstream aorta by clamping of elephant trunk and using left-heart bypass with mild hypothermia. The main disadvantage of this technique is the increased circulatory arrest time and increased surgical complexity of the initial operation, especially because of the relatively small sized proximal descending aorta that exists in many Marfan patients with type A dissection. However, the development of axillary cannulation and selective antegrade cerebral perfusion has significantly decreased the risk of stroke during such complex arch surgery [11, 12].

Marfan patients with acute type A dissection tend to be younger than other acute dissection patients and will therefore survive longer after successful surgery. The longer life expectancy and well-recognized aortopathy of Marfan patients predisposes them to future distal aortic events. In addition, these patients can have complex anatomy with an elongated and enlarged thoracoabdominal aorta, as well as severe chest deformities. Such issues make distal aortic reinterventions a technically challenging procedure requiring complex decision making and significant expertise in vascular surgery.

We therefore believe a more radical approach may be justified for Marfan patients presenting with acute type A dissection to reduce the associated morbidity and mortality during subsequent thoracoabdominal surgery. For acute type A dissection in patients without suspected Marfan syndrome, however, we do not advocate preventive replacement of the complete aortic arch. We prefer to perform hemiarch replacement in such patients and reserve complete arch replacement for those patients with an entry site tear in the arch.

Our current report shows that distal aortic reoperations can be performed with good short- and long-term results in Marfan patients. Our observed hospital mortality rate of 6.7% and our 5-year survival rate of 91.7% ± 1.6% are comparable to results from other aortic surgery centers [4, 11]. We believe our favorable results also support the strategy of early elective surgical intervention when the diameter of the dissected distal aorta exceeds 4.5 to 5.5 cm [12]. Kalkat and colleagues [13] advocate a change in luminal expansion rate accompanied by an increased fractional size of the false lumen as additional criterion to recommend surgery in asymptomatic patients. We believe all Marfan patients after surgery should undergo regular aortic computed tomography scanning to detect the progression of distal aortic disease at an early stage.

Spinal cord injury after distal aortic intervention remains the most worrisome complication of this procedure, despite the use of several protective measures (namely, prophylactic cerebrospinal fluid drainage, distal aortic perfusion, hypothermia, and selective reimplantation of intercostals). LeMaire and associates [14] reported a 5% paraplegia/paraparesis incidence after 81 thoracoabdominal aortic repairs in Marfan patients, a rate that compares very favorably to the literature. Both affected patients in our series awoke uneventfully from general anesthesia and spinal complications developed during the next 72 hours postoperatively. One patient suffered hypotension after reintubation directly before paraplegia ensued. The hypotensive episode presumably caused the compromised spinal circulation to become clinically evident. We therefore recommend, as does the group at Mount Sinai [15], that aggressive management and correction of perioperative hypotension should be performed in such patients. The intercostal arteries were not reimplanted in the patient with complete paraplegia because most of intercostal arteries originated from the false lumen and were found to be thrombosed intraoperatively.

We agree with other authors that interventional endovascular treatment of distal aortic lesions is not a viable option for Marfan patients because of their extensive and aggressive aortopathy [14]. One exception is Marfan patients in whom an existing aortic graft can be used for proximal and distal landing zones (for example, focal pseudoaneurysm) [1].

In conclusion, our results suggest that distal aortic reoperations can be performed for Marfan patients with good short- and long-term results. Aortic dissection during the initial surgical procedure could be identified as the only significant risk factor for distal aortic reoperations. Consideration should be given to complete aortic arch replacement in the setting of acute type A dissection in Marfan patients, with the goals of avoiding repeat sternotomy and of facilitating subsequent thoracoabdominal reinterventions.


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Milewicz DM, Dietz HC, Miller DC. Treatment of aortic disease in patients with Marfan syndrome Circulation 2005;111:e150-e157.[Free Full Text]
  2. Gott VL, Cameron DE, Alejo DE, et al. Aortic root replacement in 271 Marfan patients: a 24-year experience Ann Thorac Surg 2002;73:438-443.[Abstract/Free Full Text]
  3. de Oliveira NC, David TE, Ivanov J, et al. Results of surgery of aortic root aneurysm in patients with Marfan syndrome J Thorac Cardiovasc Surg 2003;125:789-796.[Abstract/Free Full Text]
  4. Carrel T, Beyeler L, Schnyder A, et al. Reoperations and late adverse outcome in Marfan patients following cardiovascular surgery Eur J Cardiothorac Surg 2004;25:671-675.[Abstract/Free Full Text]
  5. Engelfriet PM, Boersma E, Tijssen JG, Bouma BJ, Mulder BJ. Beyond the root: dilatation of the distal aorta in Marfan's syndrome Heart 2006;92:1238-1243.[Abstract/Free Full Text]
  6. Finkbohner R, Johnston D, Crawford ES, Coselli J, Milewicz DM. Marfan syndrome. Long-term survival and complications after aortic aneurysm repair. Circulation 1995;91:728-733.[Abstract/Free Full Text]
  7. Scharfschwerdt M, Sievers HH, Greggersen J, Hanke T, Misfeld M. Prosthetic replacement of the ascending aorta increases wall tension in the residual aorta Ann Thorac Surg 2007;83:954-957.[Abstract/Free Full Text]
  8. Bachet J, Larrazet F, Goudot B, et al. When should the aortic arch be replaced in Marfan patients? Ann Thorac Surg 2007;83(Suppl):774-779.
  9. Tagusari O, Ogino H, Kobayashi J, et al. Should the transverse aortic arch be replaced simultaneously with aortic root replacement for annuloaortic ectasia in Marfan syndrome? J Thorac Cardiovasc Surg 2004;127:1373-1380.[Abstract/Free Full Text]
  10. Itoh T, Ohtsubo S, Natsuaki M, et al. Influence of acute aortic dissection on long-term results of aortic root reconstruction in patients with Marfan's syndrome Kyobu Geka 1998;51(Suppl):651-655.[Medline]
  11. Svensson LG, Blackstone EH, Rajeswaran J, et al. Does the arterial cannulation site for circulatory arrest influence stroke risk? Ann Thorac Surg 2004;78:1274-1284.[Abstract/Free Full Text]
  12. Bakhtiary F, Dogan S, Zierer A, et al. Antegrade cerebral perfusion for acute type A aortic dissection in 120 consecutive patients Ann Thorac Surg 2008;85:465-469.[Abstract/Free Full Text]
  13. Kalkat MS, Rahman I, Kotidis K, Davies B, Bonser RS. Presentation and outcome of Marfan's syndrome patients with dissection and thoracoabdominal aortic aneurysm Eur J Cardiothorac Surg 2007;32:250-254.[Abstract/Free Full Text]
  14. LeMaire SA, Carter SA, Volguina IV, et al. Spectrum of aortic operations in 300 patients with confirmed or suspected Marfan syndrome Ann Thorac Surg 2006;81:2063-2078.[Abstract/Free Full Text]
  15. Etz CD, Luehr M, Kari FA, et al. Paraplegia after extensive thoracic and thoracoabdominal aortic aneurysm repair: does critical spinal cord ischemia occur postoperatively? J Thorac Cardiovasc Surg 2008;135:324-330.[Abstract/Free Full Text]

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Invited Commentary
Duke Cameron
Ann. Thorac. Surg. 2008 86: 1819-1820. [Extract] [Full Text] [PDF]



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Ann. Thorac. Surg., December 1, 2008; 86(6): 1819 - 1820.
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