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Ann Thorac Surg 2004;77:168-176
© 2004 The Society of Thoracic Surgeons
a Division of Cardiac Surgery Baltimore, MD, USA
b Division of Pediatric Cardiology,Baltimore, MD, USA Institute of Genetic Medicine
c Howard Hughes Medical Institute, Johns Hopkins Medical Institutions, Baltimore, Maryland, USA
Accepted for publication July 21, 2003.
* Address reprint requests to Dr Gott, 618 Blalock Building, The Johns Hopkins Hospital, 600 N. Wolfe Street, Baltimore, MD 21287, USA
e-mail: vgott{at}csurg.jhmi.jhu.edu
Presented at the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.
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Abstract |
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 Top Abstract IntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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METHODS: A retrospective clinical review was conducted using hospital charts and office records. Patients or their physicians were contacted for follow-up and recent echocardiograms were obtained and reviewed.
RESULTS: There was no operative or hospital mortality. Twenty-six children had aortic root replacement with a composite graft, 10 patients had replacement with a homograft aortic root, and 14 patients had a David II valve-sparing procedure. Factors related to late morbidity and mortality were analyzed. Long-term results were excellent in the 26 children receiving a composite graft. Twenty-three of these children were New York Heart Association class I (19) or II (4) at study closure. There were 3 late deaths (11, 16, and 17 years postoperative). Seven of 10 children receiving a homograft aortic root are long-term survivors and all 14 children having a valve-sparing procedure are alive. Generally, late results with the David II remodeling procedure have been good although 3 patients developed late aortic insufficiency and two required valve replacement.
CONCLUSIONS: Aortic root replacement in children with aneurysms has low operative risk and good long-term results. Composite grafts in particular carry a low risk of endocarditis, thromboembolism, and hemorrhagic events. Homografts are suitable for small patients but lack durability. Late results with the David II remodeling valve-sparing procedure in children have been compromised by late root dilatation.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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In this study we review our 21-year experience in 50 children who have undergone aortic root replacement using three different operative procedures.
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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Approval for this clinical study was obtained from The Johns Hopkins Institutional Human Research Committee on March 8, 2002.
Operative technique
Twenty-six patients underwent CG replacement by a modified Bentall procedure [1]. Our current operative technique includes complete excision of the aneurysm, direct anastomosis of the mobilized coronary arteries to the Dacron graft, and a full-thickness anastomosis of the distal graft to the transected distal ascending aorta, usually externally reinforced with Teflon felt (Dupont Pharmaceuticals) [2, 3]. All 14 children undergoing a VS operation had the remodeling procedure, as first described by Sarsan and Yacoub [4] and modified by David and Feindel (David II procedure) [5].
Postoperative management
Immediate postoperative care followed standard practice. Long-term management included use of ß-blockers as tolerated to minimize hemodynamic stress on the distal aorta, and in the case of CG patients, sodium warfarin without aspirin to maintain an international normalized ratio (INR) of 2 to 3. If a mechanical mitral prosthesis were also placed, optimal INR was 3 to 3.5. Standard American Heart Association guidelines for antibiotic prophylaxis against prosthetic endocarditis were recommended to all patients.
Statistical methods
Actuarial Survival and Freedom from Reoperation curves were calculated using the Kaplan-Meyer method. Univariate analysis was performed using the Mantel-Cox method and the multivariate analysis by the Cox proportional hazards method. Statistical computations were made using SPSS statistical software (SPSS, Chicago, IL).
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Results |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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Operative results
There were no operative or hospital deaths (Table 1).
The size distribution of aortic root prostheses is illustrated in Figure 1.
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Late results
Composite graft patients.
There were 3 late deaths among the 26 children undergoing CG replacement (Table 1). Patient 1 (EA) underwent CG graft surgery at age 18 for a chronic Type II dissection of the ascending aorta; he had an elephant trunk operation 5 years later for acute dissection of the aortic arch and descending thoracic aorta. One-year later he developed T2 paralysis during the second stage of the elephant trunk procedure, and died 10-years later of cardiorespiratory failure.
Patient 2 (LB) underwent successful repair of a dehisced left coronary artery anastomosis 2 months after CG surgery. He underwent mitral valve replacement 14-years after the CG operation and died 17-years after the original surgery of a suspected arrhythmia. Patient 3 (BL) died of an unknown cause (possible arrhythmia) 11-years after CG graft placement.
Eight of the children undergoing CG surgery also had aortic dissection (Table 2). Seven of these children are long-term survivors (6 patients were New York Heart Association [NYHA] class I, and 1 patient was NYHA class II at closure of the study). The eighth patient in this group (EA) died 16-years after CG surgery and his clinical course is described above.
Eight of 26 children undergoing CG placement also had mitral valve surgery (Table 3). Two of these patients had concomitant mitral repair, and 2 patients had concomitant mitral valve replacement. The remaining 4 patients had mitral valve replacement, either before [1] or after [3] CG surgery. Seven of these children undergoing mitral valve surgery and CG placement were NYHA class I or II at study closure. Patient 8 in Table 3 (LB) died of a suspected arrhythmia 17 years after CG surgery and is discussed above.
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Homograft root patients.
Ten children underwent replacement of the aneurysmal aortic root with a cryopreserved aortic root homograft (Table 4).
Five of these patients required early operation primarily because of severe mitral insufficiency. Three of these children had concomitant mitral valve repair at the time of HR placement, while 2 patients had an earlier mitral repair. Of the latter two, mitral valve replacement was eventually necessary, one at the time of HR replacement and one 6.6-years after HR surgery. Two of 5 children having mitral valve surgery are now 13- and 15-years after HR surgery; 3 children died 0.3-, 4-, and 5-years after HR and mitral valve surgery. Patient 8 had mitral valve repair at 1.3 years of age and mitral valve replacement at the time of HR placement. Four months after this operation, the child died suddenly at home. Patients 9 and 10 required early mitral valve repair (and HR placement) because of severe mitral regurgitation. These 2 children lived 4 and 5 years, respectively, but died suddenly of suspected arrhythmia. At autopsy, both children had massive biventricular cardiomegaly.
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Valve-sparing root replacement patients.
All 14 children who had valve-sparing procedures are alive. All were operated on after May 1997 and underwent a David II remodeling procedure. During the same time (1997 to 2002), 2 children had composite grafts and 2 had homograft root replacement. Thus, since 1997, 78% of our patients have had a valve-sparing procedure. Figure 2
depicts postoperative echocardiographic findings in the 14 VS children.
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Although 11 of 14 children have only 0 to 1+ AI, all 8 children who are 2 to 5 years postoperative have aortic root dilatation greater than the 99th percentile for normal-range root diameter based on body surface area (BSA).
Late morbidity in all patients.
Aside from late aortic dissection in 4 children (Table 2) and left coronary dehiscence in 1 patient, there have been no other significant late complications or morbidity in children having CG replacement.
There have been no episodes of thromboembolism among the 44 long-term survivors. One HR patient had a late episode of endocarditis, successfully treated with antibiotics.
Statistical analysis of late results in all three operative groups.
Figure 3
depicts actuarial survival for all 50 patients. Survival was 93% at 5 and 10 years, 87% at 15 years, and 61% at 20 years. Survival in the CG group at 5, 10, 15, and 20 years was 100%, 100%, 82%, and 65%. Survival in the HR group at 5, 10, and 15 years was 79%, 66%, and 66%. Survival has been 100% in the VS group at 5 years.
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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Late results with composite grafts have been surprisingly good. Even in children as young as 6 years old there were no episodes of thromboembolism or hemorrhage. The only late procedure-related or prosthesis-related complication among the CG patients was dehiscence of the left coronary artery anastomosis 2-months postoperatively. With modification of our surgical technique (reimplantation of both coronary arteries onto the composite graft with Teflon felt "lifesaver" reinforcement rather than the classic Bentall technique), this problem has not recurred.
On the other hand, durability of homografts in children has been disappointing. Homografts were used mainly in young children with severe mitral insufficiency. Before our first pediatric valve-sparing procedure in May 1997, the homograft was an attractive option in very young children because it eliminated the need for anticoagulants. However, a high incidence of late failure secondary to aortic valve calcification led to reoperations in most patients; those reoperations to replace the degenerated homografts were technically demanding, but fortunately successful in all. We now believe that the only indication for a homograft is the rare instance of a small aortic root (< 18 mm) in a patient unsuitable for a valve-sparing operation.
The valve-sparing operation has become our procedure of choice over the last 5 years (Fig 5). Only 4 children during this time period had a procedure other than a VS operation, usually because of severe AI, aortic dissection, or the need for a concomitant mitral valve replacement with a mechanical prosthesis. Results with this procedure have been encouraging, although the follow-up has been considerably shorter when compared with the CG and homograft patients.
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David introduced his reimplantation procedure (David I) because of his concern about recurrent root dilatation with Yacoub's original remodeling procedure [5]. After several years of successful use of the David I, he introduced the David II remodeling procedure because of reports of aortic leaflet damage from impingement against the Dacron graft with the David I procedure. More recently, David returned to his reimplantation procedure [7]. To avoid the potential problem of leaflet damage with the reimplantation procedure, David modified the sleeve graft by creating aortic sinuses in the graft. This was achieved by plicating the graft at the levels of the aortic annulus and sinotubular junction. In a more recent report [8], David reported that 8-year freedom from moderate/severe AI was 55% ± 6% with the remodeling technique and 90% ± 6% with the reimplantation technique. He also reported exclusive use of the reimplantation technique (with neoaortic sinuses in the sleeve graft) over the last 2 years.
DePaulis and colleagues [9] recently introduced a Dacron graft with engineered aortic sinuses that appears suitable for the David I reimplantation technique. The senior author (DEC) has used these new grafts since May 2002 with encouraging results. It is also our impression that late prosthetic root dilatation is a greater problem with children than adults, which may simply reflect that patients who require surgical intervention earlier in life have more severe connective tissue disorders.
Growth of the child with respect to the root prosthesis has not been an issue in the vast majority of patients. Even the young patients have dilated aortic annular diameters that approach adult size. Those with small roots were among the most severely affected with connective tissue disease, had a higher rate of reintervention for mitral or distal aortic disease anyway, and had worse survival. No patient outgrew a prosthesis, and there was no evidence for late morbidity related to patient–prosthesis size mismatch.
The importance of late imaging of the residual aorta is illustrated in Table 2 and in Figure 4. Four patients required late surgery for new dissection of the aortic arch or descending thoracic aorta 5-years to 14-years after aortic root surgery. A fifth patient required late aortic arch replacement resulting from a DeBakey Type I dissection (precomposite graft).
Other observations from this study are the following: mitral disease appears to be a "marker" for more severe connective tissue disease and need for earlier operative intervention; children as young as 6 years of age do well with composite grafts, with a minimal risk of late thromboembolism or hemorrhage; and homograft aortic root replacement was effective for young children, but lacked durability.
This study does not address the issue of optimal timing of aortic root replacement in children. Clearly, in children with severe mitral insufficiency, timing of surgical intervention is straightforward. However, there are few data on risk of rupture or dissection as it relates to aneurysm diameter in children. Currently we treat adolescents as adults, and apply the adult criteria: prophylactic intervention when the diameter reaches 5.5 cm, or 5.0 cm if there is a family history of aortic dissection or rupture. In children less than 12 years of age, surgery is recommended when the aneurysm satisfies adult criteria (> 5.5 cm), or if the diameter has increased 1 cm or more in 12 months. Furthermore, the emergence of aortic insufficiency has been an indication for early intervention if a VS procedure is anticipated.
In summary, this study demonstrates that (1) aortic root replacement in children has low surgical risk, satisfying the prerequisite of little or no operative mortality for a prophylactic operation; (2) composite grafts provide excellent long-term results in children with aortic root aneurysm, because they have a low risk of late endocarditis, thromboembolism, or hemorrhagic events; (3) early onset of mitral valve dysfunction may signal a severe loss of connective tissue integrity and predicts a less favorable outcome; and (4) valve-sparing procedures promise excellent quality of life by avoiding anticoagulation, but will need further refinement to match the high standards set by composite grafts.
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Acknowledgments |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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Discussion |
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First, I congratulate Steve Cattaneo on a splendid presentation. He is just a general surgery resident, for those in the audience who don't know. I wonder, Bill, what was his heart rate when he stepped up there to the podium? He did a great job. Second, the early and late results from Hopkins in this very challenging subset of 50 children with the Marfan syndrome (MFS) and ascending aneurysms are spectacularly good. That is a tribute to all of you.
The only real question I have is something I forewarned Steve about yesterday after reading the manuscript. We didn't see on the graphs, which were drawn out to 15 and 20 years, the number of patients remaining at risk and the error bars—or variability of the estimates—for survival and reoperation. The curves extending to 20 years are probably fair for the composite valve graft (CVG) group; but, if we are focusing on the valve-sparing group, we are really only talking about 3- to 5-year results, and for the homografts it is only 5 to 10 years. I would like to see the numbers of patients remaining at risk and the error bars in the graphs so in our minds we know where to truncate those curves. But, if that is the only criticism you are getting from me, most in the audience know you are getting off easy. Good work, Steve.
Now, what have we learned from this 21-year experience in these 50 young patients with the MFS? Number one, since 1997, Duke Cameron and his colleagues have tried to get away from homografts for obvious reasons; the homografts just don't last long enough. Historically we have thought it hazardous to anticoagulate a young child forever; well, this Hopkins experience with CVG (the youngest of which was 6 years old) refutes that presupposition. Surprisingly, not one of those children "outgrew" their composite valve graft and required reoperation; further, none died of a valve-related complication. That is remarkable.
If Ron Elkins were here, I am sure he would disagree with Duke Cameron and me pouring cold water on homografts, but he is not here. I just don't think homografts are going to be durable enough, and that is why Duke switched to valve-sparing root replacement.
Since 1997, only 4 of 18 young patients received anything other than a valve-sparing root replacement. They underwent a CVG due to severe aortic regurgitation (AR), aortic dissection, or the need for a mechanical mitral prosthesis. The latter I have no argument with, because it probably is silly to put in a mechanical valve in the mitral position and try to save the aortic valve. On the other hand, I think we now know—speaking from a personal experience of over 80 valve-sparing aortic replacement cases since 1993, about one-half of which were in patients with the MFS—that even if there is rather severe AR and even if the AR is eccentric due to prolapse of the noncoronary or the right coronary cusp, these valves can be repaired satisfactorily today. That is, we don't have to shy away from valve-sparing root replacement. Third, as three centers in Germany (Hannover, Homburg/Saar, and Lubek) and Sir Magdi Yacoub in London have shown us, valve-sparing root replacement is a good operation for aortic dissection, even acute type A dissection. Indeed, the T. David reimplantation approach might be the most hemostatic operation you can do for acute type A aortic dissection. Now, I grant you that that this is taking a big operation and making it into a real big operation, but it has been accomplished with reasonable results. So I am not sure we should back away from valve-sparing root replacement if a dissection is present. Fourth, I personally no longer believe there is any maximal annular size that precludes valve-sparing root replacement. Even if it is 29 mm or 31 mm, it can be done. The unknown question here, of course, is what is the long-term durability of the procedure in this subset?
The Hopkins group's choice of valve-sparing aortic replacement procedure for the last 5 years has been the Yacoub remodeling approach, where you are not fixing the aortic annulus; I submit that explains why 3 of 14 patients needed reoperation for AR, and there is a worrisome degree of dilatation in many of the remaining children. It also explains why Duke Cameron switched in 2002 to the David reimplantation technique in an attempt to make valve-sparing aortic root replacement in patients with the MFS a more durable procedure. After Tirone David's paper at the 2002 AATS, we now clearly know that a Yacoub-type remodeling procedure in patients with the MFS imposes a real risk of late annular dilatation and recurrent AR. But the question remains, is a David-type reimplantation procedure going to be more durable than a homograft, especially in the younger children? Only more time will allow a definitive answer to this question. I predict your future results achieved using the David reimplantation method are going to be much superior to what you have reported here today with the Yacoub remodeling approach. Perhaps, Duke, you can even use a David procedure in the very young, where historically we have been afraid that they are going to outgrow a fixed aortic annulus and develop aortic stenosis. I think it is interesting that none of your children receiving composite valve graft outgrew their prostheses. Now, sure, these are larger-size valves implanted in a supraannular position, but maybe this perceived fear that they are going to outgrow their annulus is not based in fact. In this context a little footnote for the audience may be in order. All of Tirone's many papers on this procedure are from the Toronto General Hospital only, and exclude the younger kids he has operated upon at the Sick Kids Hospital in Toronto. There is one such child that did outgrow a David-I procedure after a growth spurt and required reoperation for stenosis. So it might not be totally reoperation risk free.
I have preferred the David technique since 1993. I did get lazy, however, and perform Yacoub remodeling procedures for a year or so in the late 1990s. It was quicker, involved much less extensive aortic root dissection, and two instead of three suture lines. I returned quickly to the David reimplantation approach due to early durability issues, namely annular dilatation and recurrent AR. Since May 2001, Tirone and I have used what I term the "T. David-V" version of reimplantation. Tirone changes his preferences frequently and somebody should keep track of what he's doing, so I took the liberty of labeling his various procedures with numbers. Tirone doesn't really like this much, but has gone along with it. The T. David-V is nothing more than taking a 6- to 8-mm larger graft than the original David and Feindel formula would indicate, and then necking the big graft down at the annulus—you can make it as small or as big as you want, but it is firmly secured and cannot dilate—and then again up at the Dacron (DuPont Pharmaceuticals) sinotubular ridge. What we are doing is custom fabricating something like Steve illustrated on that last slide with the Terumo Vascutek De Paulis sinus graft prosthesis, but we are doing it on a customized basis where the surgeon has unlimited flexibility to make every component of the geometry fit that patient as he or she sees fit. You end up with tremendous Dacron pseudosinuses, whatever that means. I should remind you, the argument is entirely theoretical whether the leaflets will last longer if Dacron pseudosinuses are created.
So, Duke, Vince, and Steve, I congratulate you. In the future I will be interested to see if you can successfully use the David reimplantation technique in the younger children with MFS.
Thank you.
DR N. KOUCHOUKOS (St. Louis, MO): This is an outstanding series with enormous implications for the future management of young patients with Marfan's syndrome. I have several questions. You reported an absence of thrombolic complications. Could you tell us what the international normalized ratio (INR) range was for these patients? A corollary to that would be whether it is reasonable, in view of the absence of any thrombolic complications, to consider the use of no Coumadin (Du Pont Pharmaceuticals).
Secondly, although the David II or Yacoub procedure appeared to have some degree of aortic regurgitation, if I interpreted the slide correctly, the majority of these patients had no progression of aortic regurgitation over the long term. Why do you believe the David I operation is a better procedure? When using the David I procedure, is there any diameter of the aortic annulus below which you would not insert one of these new prostheses or a standard polyester graft for fear of creating outflow tract obstruction, either early or late?
I enjoyed this paper very much. It is a superb contribution. Thank you.
DR C. KNOTT-CRAIG (Oklahoma City, OK): I too want to congratulate the group from Baltimore on their excellent results and wish we could all emulate these results in the future. I have two questions: what are your current recommendations for those young children with significant or severe aortic regurgitation associated with their root aneurysm? And secondly, do you think the decellularized homografts (eg, SynerGrafts) would favorably influence the longevity of homografts in this pediatric group of patients, since one can usually place an adult size homograft at the time of surgery?
DR CATTANEO: Doctor Miller, thank you for all of your praise and constructive criticism for our paper. In order to answer the first question, I looked up some of our data. Dr Miller is correct that the standard error for actuarial survival and actuarial freedom from reoperation begin to splay past about 10 years because all of our valve-sparing procedures and the majority of our homograft repairs have been performed more recently. There are 30 patients that remain at risk at 5 years, and 19 patients at 10 years. So there is still a significant proportion of patients at 10 years, but then our 15- and 20-year follow-up data is certainly more splayed out.
Our experience with the composites, as I had said during the talk, has involved children as young as 6 years of age. The major reason that we have been able to put in composite grafts without significant outflow obstruction as these children have grown through adolescence into young adulthood is that the annulus is typically dilated significantly enough that an adult size prosthesis can be placed at the time of surgery.
As Dr Miller suggested, Dr David performed one of his first reimplantation procedures on a 14-year-old Marfan patient who, within 2 years of having the valve-sparing reimplantation, developed significant stenosis and went on to having aortic replacement. We have not yet had that experience, but certainly it is a possibility.
Regarding why do we not perform valve-sparing operations in patients with significant aortic insufficiency, our experience has been, as I had illustrated from the slide that demonstrated the preoperative aortic insufficiency, that these children who are presenting for aneurysm repair typically do not have a significant degree of aortic insufficiency, if they have any at all. So we have yet to encounter a situation where we have had to decide if a valve with severe aortic insufficiency would be amenable to a valve-sparing approach as compared to a composite or a homograft replacement.
Doctor Cameron's experience with the DePaulis graft has been since May 2002. He has operated on approximately a dozen patients, six of whom were children. Although we have no short-term or long-term follow-up, we anticipate that this will be a much better procedure as far as correcting the problem associated with Marfan aneurysms, while also hopefully preventing the deterioration we see with the homografts and the potential for outlet obstruction.
Doctor Kouchoukos, the patients who had the composite repair all remain on Coumadin. I do not know the range of the INRs. We strive to keep them in a range of 2 to 2.5 and have been extremely fortunate to not have had any thromboembolic complications in follow-up with these patients. I can't explain why this has been so, but in our series we have managed to avoid any complications. I don't think, though, that aspirin is going to be enough.
Typically, as I have said, the size of the aortic annulus is significantly enlarged in these children, even if they are very young. In 11 of these patients we have not really seen any progression of the aortic insufficiency, however, the follow-up I would caution has only been 2 to 5 years in many of these patients. We are very disheartened that 3 of 14 patients in the series who had the David II have manifested a progression of their aortic insufficiency, with two of them requiring replacement, and the third one, as I had said, with 3+ aortic insufficiency (AI) likely to require replacement in the near future. Therefore, because of this, even though we do not have significant long-term results, Dr Cameron has abandoned the approach and has gone to the reimplantation procedure I just described.
I have partially addressed Dr Knott-Craig's first comment as far as recommendations for significant aortic insufficiency. We haven't really encountered that in the pediatric population. The AI, as I said, has been fairly minor. Our indications for surgery have been aneurysm size and mitral insufficiency, primarily, and therefore we have elected to prophylactically repair these aneurysms prior the development of severe aortic insufficiency, especially in light of the fact if we are going to be attempting valve-sparing procedures we don't want the free margins of the cusps to be thinned out too much as the aortic root continues to dilate.
Thank you very much.
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= composite; 
= homograft; 
= valve-sparing operation.)
and