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Ann Thorac Surg 2009;87:503-513. doi:10.1016/j.athoracsur.2008.11.033
© 2009 The Society of Thoracic Surgeons
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Original Articles: Adult Cardiac

Aortic Root Replacement With Stentless Porcine Xenografts: Early and Late Outcomes in 132 Patients

Scott A. LeMaire, MD*, Susan Y. Green, MPH, Kapil Sharma, MD, Catherine K. Cheung, Hon BSc, Aryan Sameri, Peter I. Tsai, MD, Gerald Adams, EdD, Joseph S. Coselli, MD

The Texas Heart Institute at St. Luke's Episcopal Hospital, and the Division of Cardiothoracic Surgery, Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston, Texas

Accepted for publication November 12, 2008.

* Address correspondence to Dr LeMaire, One Baylor Plaza, BCM 390, Houston, TX 77030 (Email: slemaire{at}bcm.edu).

Presented at the Fifty-fourth Annual Meeting of the Southern Thoracic Surgical Association, Bonita Springs, FL, Nov 7–10, 2007.


Dr Coselli discloses that he has a financial relationship with Medtronic Inc and St. Jude Medical.

 

   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Background: Traditionally, aortic root replacement has most commonly involved mechanical composite valve grafts, which have excellent durability but necessitate lifelong anticoagulation. Stentless porcine xenografts (bioroots) are a recently developed alternative that enable root replacement without the necessity of long-term anticoagulation. This study examined the early and late outcomes of aortic root replacement with porcine bioroots.

Methods: Porcine bioroots were used for root replacement in 132 patients. Of these, 129 (97.7%) required graft extensions for ascending aortic replacement, and 55 (41.7%) underwent aortic arch replacement. Twenty-three operations (17.4%) were reoperations. Twenty-four patients (18.2%) had aortic dissection. Early and late outcomes were ascertained by reviewing medical records. Changes in New York Heart Association (NYHA) class were used to assess improvements in functional status. Follow-up echocardiography results were reviewed to assess bioprosthetic valve function and changes in left ventricular ejection fraction.

Results: There were 10 operative deaths (7.6%), 9 of which were directly related to intraoperative ventricular failure. Nine patients (6.8%) had late valve-related complications, including 5 patients with prosthetic endocarditis (3 died), 1 annular pseudoaneurysm, and 3 sudden, unexplained deaths. Survivors' NYHA status and left ventricular ejection fraction improved significantly. No structural valve dysfunction was evident during follow-up. Actuarial survival was 85.6% ± 3.1% at 1 year and 77.8% ± 4.8% at 5 years.

Conclusions: Aortic root replacement with porcine xenografts can be performed with respectable early and late outcomes, even when combined with aortic arch replacement. Further follow-up is necessary to evaluate long-term bioroot durability.

Despite the increasing popularity of valve-sparing root reconstructions, root replacement remains a standard approach to treating aortic root disease [1, 2]. Although mechanical composite valve grafts (CVGs) are extremely durable, recipients receive lifelong anticoagulation to prevent thromboembolic complications. In patients who might benefit from a bioprosthetic valve, alternatives for aortic root replacement include valved conduits consisting of an aortic valve bioprosthesis attached to a synthetic aortic graft, cryopreserved aortic root homografts, and pulmonary autografts. A recently developed option is the stentless porcine aortic root—or bioroot—prosthesis.

Bioroots are xenografts composed of a thin, stentless, synthetic sewing cuff attached to a glutaraldehyde-preserved porcine aortic root. They were initially developed as customizable prostheses that could be sculpted as needed into various configurations to enable different degrees of aortic valve replacement, ranging from subcoronary valve replacement to full root replacement. Their use for aortic valve replacement has gained in popularity since their introduction in the 1990s, and they have been used in an increasingly wide spectrum of aortic valve operations [3–15]. Unlike most other commercially available root prostheses, bioroots have a combination of highly desirable features: they are ready to implant and available off the shelf in a variety of sizes, and lifelong anticoagulation is not required. This retrospective study examined the early and late outcomes of aortic root replacement with bioroots.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 Acknowledgments
 References
 
Patients and Data Collection
Institutional Review Board approval was obtained for the collection and analysis of clinical data and waiver of individual consent. Our prospectively maintained clinical database was used to identify 132 consecutive patients (Table 1) who had undergone aortic root replacement with porcine bioroots. In all patients the indication for operation was aneurysm or dissection involving the aortic root; no patient in this series underwent root replacement to treat isolated aortic valve disease [10]. We collected perioperative data after study-specific variables were selected and defined according to relevant reports and reporting guidelines [3–9, 11–21]. Follow-up data were obtained from medical records detailing office visits, hospitalizations, and telephone contacts.


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  		Table 1 Preoperative Characteristics of 132 Patients Who Underwent Aortic Root Replacement Operations With Porcine Bioroots
 
Review of follow-up data focused on identifying potential valve-related complications. Values abstracted from the preoperative and most recent available follow-up (ie, >30 days after operation) echocardiography reports included the lowest raw left ventricular ejection fraction (LVEF) [22]. Current vital status for patients who were lost to follow-up was obtained from the Social Security Death Index (SSDI) database.

Bioroot Prostheses
Between March 2001 and July 2007 (Fig 1), 54 patients (40.9%) were implanted with the Medtronic Freestyle Aortic Root Bioprosthesis (Medtronic Inc, Minneapolis, MN). Between May 2002 and November 2005, 78 patients (59.1%) were implanted with the St. Jude Medical Toronto Root Bioprosthesis with BiLinx (St. Jude Medical Inc, St. Paul, MN); data from 26 of these patients were included in a 2004 multicenter report that focused on early outcomes [12].


Figure 1
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  		Fig 1. Histogram shows the number of bioroot procedures performed during the study period, stratified by the Toronto (slanted bars) and Freestyle (black bars) bioroots. *Data for 2007 are from January through July.

 
Patients who received the Toronto bioroot were enrolled in the multicenter investigational device exemption (IDE) clinical trial and provided written informed consent before study enrollment and bioroot implantation. The exclusion criteria for the IDE trial included active endocarditis; need for additional concurrent valve replacement; previous mitral, tricuspid, or pulmonary valve replacement; acute preoperative neurologic event; and renal dialysis. The IDE trial was stopped in 2006, and the Toronto bioroot is no longer being manufactured. The decision to halt progress toward United States Food and Drug Administration approval was reportedly due entirely to business issues and not to any problems with valve safety or performance.

Surgical Techniques
Most of the 132 operations (Table 2) were elective, and 23 procedures (17.4%) were reoperations. Hypothermic circulatory arrest (HCA) was necessary in 57 patients (43.2%), including 10 patients with acute dissection in whom HCA was used to facilitate an open distal anastomosis, most often as a beveled hemiarch. The aortic arch was replaced in 55 patients (41.7%). During the period covered in this series, we used both retrograde and antegrade cerebral perfusion as adjuncts to HCA; our currently favored approach to HCA includes routine use of right axillary artery inflow and antegrade cerebral perfusion [23].


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  		Table 2 Details of 132 Aortic Root Replacement Operations With Porcine Bioroots
 
The sizes of the implanted bioroots ranged from 19 to 29 mm; 25-mm bioroots were used in nearly half of the cases. At the time of implantation, the bioroot was rotated so that the noncoronary sinus of the prosthesis was aligned with the right coronary segment of the patient's annulus. The unused left coronary artery stump of the bioroot was often reinforced with a pledgeted polypropylene suture to prevent bleeding. Early in our experience, we used continuous polypropylene sutures to attach the bioroot sewing ring to the aortic valve annulus (Fig 2A). We eventually changed our technique to make it easier to perform the anastomosis, and we currently favor interrupted supraannular polyester mattress sutures with felt pledgets (Fig 2B). The annular anastomosis was often reinforced with a continuous polypropylene suture to prevent bleeding [24].


Figure 2
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  		Fig 2. The technique of aortic root replacement with a porcine bioroot is illustrated. The annular anastomosis can be performed by using (A) continuous polypropylene suture or (B) interrupted polyester mattress sutures. Note that the bioroot has been rotated so that the noncoronary sinus of the xenograft is aligned with the patient's right coronary artery. (C) Completed repair with both coronary arteries reattached by the button technique.

 
Whenever possible, both coronary arteries were reattached after being mobilized along with generous buttons of surrounding aortic tissue (Fig 2C). Techniques used to prevent bleeding at the coronary anastomoses have been previously reported in detail [24]. When it was not feasible to use the button technique, an alternative approach to reattachment was used for one or both coronary arteries (Table 2). Alternative methods for reattaching the coronary arteries included the Bentall inclusion technique [1]; the Cabrol technique [25]; the hemi-Cabrol technique, in which one coronary artery was reattached with an 8- or 10-mm polyester interposition graft; and the use of a reversed segment of autologous saphenous vein placed as an interposition graft to a coronary ostium or as a bypass graft to a more distal aspect of the coronary artery. Alternative coronary artery reattachment techniques were used in 9 of 23 patients (39%) undergoing reoperations compared with 16 of 109 patients (15%) undergoing first-time operations.

In nearly all cases, we used a gelatin-impregnated woven polyester graft (Gelweave, Vascutek Inc, Ann Arbor, MI) to bridge the distance between the bioroot and the distal extent of aortic replacement. Graft sizes varied from 18 to 28 mm, with 24-mm grafts being used most commonly.

The most commonly performed concomitant procedure was coronary artery bypass grafting (CABG). This procedure was used in 7 patients as an alternative approach to coronary reattachment and was needed in another 32 patients to treat coronary artery disease, intraoperative ventricular dysfunction, or severe bleeding from a coronary reattachment site [13]. Placement of an intraaortic balloon, a ventricular assist device, or both, was required in 7 patients (5.3%) because they had difficulty separating from cardiopulmonary bypass.

Statistical Analysis
We analyzed only data collected specifically for this retrospective study; no data were obtained from the sponsor of the Toronto bioroot IDE trial. Data were analyzed with SAS 9.2 software (SAS Inc, Cary, NC). Quantitative variables are presented as mean ± 1 standard deviation. Overall actuarial survival was estimated by using the Kaplan-Meier survival model.

In a post hoc analysis, we compared the preoperative characteristics, surgical details, and outcomes of patients who received the Freestyle bioroot with those of patients who received the Toronto bioroot. Categoric variables were analyzed with {chi}2 or Fisher exact tests. Continuous variables were first examined for normality of distribution; the t test was used for those with normal distributions, and the nonparametric Mann-Whitney U test was applied for those with skewed distributions. For survival analysis, we used a Kaplan-Meier survival model in which type of replacement was the factor of comparison. In all tests, two-tailed p-values were calculated.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 Acknowledgments
 References
 
Early Outcomes
Early complications (Table 3) included 10 operative deaths (7.6%): 8 (6.1%) occurred within 30 days postoperatively (Table 4). Nearly all of the early deaths were directly related to intraoperative ventricular failure; technical problems with coronary reattachment had occurred in 4 of these patients. Cardiac arrhythmia was the most common early complication, occurring in 55 patients (41.6%); 45 of the 55 arrhythmias (82%) were atrial in origin.


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  		Table 3 Outcomes after 132 Aortic Root Replacement Operations With Porcine Bioroots
 

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  		Table 4 Causes of Early and Late Deaths After 132 Aortic Root Replacement Operations With Porcine Bioroots
 
Late Outcomes
Clinical follow-up data were available for 119 of the 122 early survivors (97.5%), who had a mean clinical follow-up of 3.3 ± 1.5 years (range, 39 days to 6.8 years). Three patients were lost to follow-up, but their current vital status data were obtained from the SSDI database; thus, current survival data were available for all patients. Of the 17 late deaths (Table 4), 9 occurred in the first postoperative year. Actuarial survival was 85.6% ± 3.1% at 1 year and 77.8% ± 4.8% at 5 years (Fig 3).


Figure 3
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  		Fig 3. Kaplan-Meier survival curve shows survival after 132 aortic root replacement operations with porcine bioroots.

 
Late valve-related complications have developed in 9 patients (6.8%). In one patient, a pseudoaneurysm arose from the annular and left coronary anastomoses. The bioroot was replaced with a CVG, and the patient remains alive. Endocarditis developed in 5 patients. This complication was fatal in 3 patients and was successfully treated nonoperatively in 2. Three patients died suddenly of unexplained causes (Table 4). Because the causes of death could not be documented, they were classified as valve-related deaths in accordance with the guidelines for reporting adverse events after valve procedures [16]. Therefore, 6 of the late deaths were considered valve-related.

Three patients had late complications due to left main coronary stenosis; although not valve-related, these deaths were attributable to the root-replacement procedure [13]. One of the affected patients died of a myocardial infarction 3 months after operation. In the second patient, severe mitral regurgitation and congestive heart failure developed 2 years after root replacement. This patient was treated with coronary angioplasty and stenting but declined mitral valve repair and ultimately died of heart failure. The third patient remains alive after undergoing emergency CABG 6.5 months after the initial operation.

Follow-up New York Heart Association (NYHA) status was available for 84 of 105 survivors (80%). Comparison of preoperative and follow-up NYHA status showed that after a mean follow-up of 3.5 ± 1.3 years (range, 0.8 to 6.8 years), patients had significant improvement in functional status (Table 5). NYHA status improved in 54 of the 59 patients (92%) who had been in NYHA classes II, III, or IV preoperatively.


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  		Table 5 Comparison of Preoperative Versus Follow-up New York Heart Association Status and Left Ventricular Ejection Fraction
 
Follow-up echocardiography data were available for 99 of 105 survivors (94%). Comparison of preoperative and follow-up LVEF showed that, after a mean follow-up of 2.8 ± 1.4 years (range, 64 days to 6.1 years), patients had significant improvement in ventricular function (Table 5). Of the 39 patients who had reduced LVEF before surgery, LVEF improved in 35 (90%). Valve integrity at follow-up was excellent; only 1 patient had even minimal aortic regurgitation. Mild aortic valve stenosis was found on echocardiography in 8 patients (8.0%), and moderate stenosis was found in 2 (2.0%). No patient had evidence of structural valve deterioration.

Comparison of Freestyle and Toronto Bioroot Groups
Our analysis of preoperative characteristics revealed profound differences in the two patient groups (Table 6). Overall, the Toronto bioroot recipients appeared to be at lower risk than the Freestyle bioroot recipients. The more frequent use of HCA in the Freestyle group corresponded to a trend toward longer cardiopulmonary bypass times in this group. Neither early nor late outcomes differed significantly between the two groups.


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  		Table 6 Comparison of Patients Who Received Toronto vs Freestyle Bioroots a
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 Acknowledgments
 References
 
The stentless porcine xenograft root is a valuable addition to the surgical armamentarium for aortic root replacement. Our study found encouraging results in a uniquely complex group of patients. Connective tissue disorders were present in a relatively high proportion of patients (15.2%). These diseases are characterized by extensive aortic involvement and thus put patients at increased risk of aortic repair failure [26]. All procedures in our series involved total root replacement, most required extended graft repair of the ascending aorta, and 42% involved aortic arch repair. In contrast, in many previous series of bioroot implantations, often less than 30% of patients underwent full root replacement, and it was rare for repairs to extend into the aortic arch [4, 6–9, 18, 27]. A few reports focused on full root replacement (Table 7), but these series included relatively few patients with aortic dissection, reoperations, or aortic arch repairs [11–15]. Despite the high-risk patient profile in our series, early and late results were respectable and comparable with those of previous series.


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  		Table 7 Comparison of Published Series Focusing on Aortic Root Replacement With Porcine Bioroots
 
Follow-up results showing improvements in our cohort's functional status and LVEF, as well as bioroot durability, are encouraging: there was no evidence of structural valve failure, and the incidence of late valve-related complications was low (6.8%). Although sudden unexplained deaths meet reporting standards for valve-related mortality [16], given the clinical circumstances in 2 of these patients—1 with an unrepaired thoracoabdominal aortic aneurysm, and 1 with acute back pain after thoracoabdominal aortic repair—it seems unlikely that the bioroots were the cause of death.

Two different types of porcine bioroots have been used in the United States; mid- and long-term data after root replacements are limited for one type and are nonexistent for the other. Follow-up data extending up to 12 years for the Freestyle xenograft have shown excellent clinical outcomes, prosthesis durability, and hemodynamic performance; however, most of the data on this device focus solely on its use for subcoronary aortic valve replacement [3–9]. Mid- and long-term data are emerging for its use in root replacement but remain limited (Table 7). In a randomized trial, Melina and associates [15] found that Freestyle bioroots were about as durable as homografts after a median follow-up of 45 months; 5-year actuarial survival for the bioroot group was 83% ± 5%. Kon and associates [14] reported a similar 5-year actuarial survival of 82.8% after aortic root replacements with Freestyle bioroots.

For the Toronto bioroot, published reports are limited to short-term results culled from the IDE clinical study [11–13]; mid- and long-term outcome data are lacking. Early analysis of the IDE study data revealed outstanding short-term durability and a trend toward a reduction in the transvalvular gradient over time; aortic regurgitation, structural valvular deterioration, and nonstructural dysfunction were not found in any patient [12]. Because the Toronto bioroot has been implanted in more than 600 patients, a careful examination of outcomes in these patients remains important even though the device is no longer available for use.

Although this study was not designed to compare the safety or effectiveness of the 2 devices, we believed that a descriptive post hoc comparison might nevertheless be instructive. We predominately used the Toronto bioroot during our early experience and gradually shifted toward the Freestyle device (Fig 1). In general, the patients who received the Toronto bioroot were healthier preoperatively and had less complicated operations. The most likely explanations for this observation are the constraints of the related IDE study, which prevented enrollment of many high-risk patients, and our own expanding use of bioroots in increasingly complex cases over time. The change from the Toronto device to the Freestyle root also paralleled several changes in our technique; for example, Freestyle recipients were more likely to have axillary artery cannulation and interrupted annular sutures. The higher complexity of operations in the Freestyle group is reflected in the slightly higher incidences of operative death, bleeding, and morbidity in that group; however, none of the outcome variables were significantly different between groups.

Nine of the 10 early deaths were associated with intraoperative ventricular failure, and technical problems related to coronary reattachment occurred in 4 of these cases. It is critical to ensure proper alignment of the coronary arteries and to carefully select the reattachment sites to prevent kinking of the coronary arteries. Any difficulty weaning the patient from cardiopulmonary bypass raises immediate concern about coronary malperfusion; whenever this is suspected, we expeditiously perform CABG, which can often be done without cross-clamping the aorta. Bleeding from the coronary buttons can also be catastrophic and is notoriously difficult to control. We routinely use adjunctive techniques, such as reinforcement with pericardial rings, to prevent bleeding at these anastomoses [24]. When faced with severe coronary button bleeding, we have a low threshold for reclamping the aorta so that the button can be directly repaired, reattached with an alternative technique (eg, interposition graft), or oversewn after CABG is performed.

This retrospective study has several important limitations. Because of our practice's referral pattern, most of our patients live far away from our center and receive follow-up care from their local physicians. We were fortunate enough to capture basic follow-up information (vital status, need for reoperation, etc) for most patients, but in some cases it was not possible to obtain the other, more detailed information needed to fully assess valve performance. Even when such data were available, the lack of standardization between centers complicated efforts at detailed interpretation of these data. For example, from the echocardiography results, we were able to collect data on LVEF and bioprosthetic valve stenosis and regurgitation, but not on left ventricular hypertrophy, transvalvular gradients, or other important variables. Similar challenges were encountered when we attempted to ascertain the incidence of late thromboembolic complications during follow-up, preventing us from studying this important aspect of prosthetic valve safety.

Although this study showed encouraging early and late outcomes, additional follow-up studies will be necessary to better determine the long-term durability of these devices. The Achilles' heel of bioprosthetic valves remains their poor long-term durability compared with that of mechanical valves. As a consequence, many surgeons remain justifiably reluctant to use bioprosthetic roots in younger patients. Furthermore, the potential difficulty of the inevitable reoperations in young patients is an important consideration. Notably, the ease of valve explantation and replacement during reoperation is one of the cited potential advantages of a new prefabricated valved conduit comprising a stentless porcine aortic valve and a synthetic vascular graft [28]. It is possible that advances in catheter-delivered aortic valve prostheses will affect future decisions about using bioroots in younger patients; the pliable bioroot with structural valve deterioration may be a very suitable landing area for an expandable valve-stent.

In light of these concerns, when valve-sparing root reconstruction is not feasible, we continue to advocate using mechanical CVGs in patients aged younger than 70 years. Most exceptions to this approach are made for patients with contraindications to warfarin therapy, but a growing number are driven by patient demand. The mean age of 54 years in our patient cohort reflects the trend of younger patients requesting bioprosthetic aortic valves in our practice. Patients are increasingly choosing the risk of reoperation over the risks associated with long-term anticoagulation.

In conclusion, although stentless porcine xenografts are not the ideal choice for young patients who need root replacement, they are an important alternative to mechanical CVGs, particularly for patients who either cannot or choose not to tolerate lifelong anticoagulation. As a consequence, it will be important to continue to collect and report durability data to facilitate valve selection decisions by physicians and patients.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
Acknowledgments
 References
 
DR JOHN W. HAMMON JR (Winston-Salem, NC): My colleague, Dr Neal Kon, was invited to discuss this paper and he had to cancel his trip at the last minute, so I am going to present paraphrased remarks from Dr Kon that were altered to fit the time considerations for the discussion.

We congratulate Dr Coselli and his colleagues on an excellent paper and presentation. We also consider the stentless bioroot a superb option for total root replacement. We began implanting stentless bioroots in 1992 and were part of the original Freestyle study group. The vast majority of surgeons in the Freestyle study group choose to use this valve as a subcoronary implant, but we have always felt it is better utilized if implanted using a full root technique.

I believe our indications and therefore patient population are somewhat different than yours. Our indications for using a stentless bioroot include patients with significant aortic root disease who prefer a tissue valve, the elderly patient with poor tissues, patients with a small aortic root and/or bad ventricles, replacing degenerated stented prostheses, and endocarditis. We can perform AVR [aortic valve replacement] in all patients and not be concerned with patient-prosthesis mismatch. Bioroots offer patients with endocarditis the same advantages as the aortic allograft, the ability to reconstruct the aortic root after extensive débridement of infected tissues. In our series, bioroots have demonstrated very good durability, a 94% freedom from structural valve disease at 14 years, making it an excellent tissue valve replacement option.

We have utilized the simple interrupted suture technique so as to optimize alignment. Why have you chosen to use interrupted mattress sutures or a running technique when each of these techniques might lead to distorting either the bioroot inflow or the left ventricular outflow tract? Have you used the stentless bioroot solely for hemodynamic considerations or do you use it only in patients with significant root disease? Can you elaborate for us, Dr Coselli, what you feel the optimal situations are for implanting a stentless bioroot? Thank you.

DR COSELLI: Thank you, Dr Hammon, for your kind comments. With regards to the suture technique, we have not found that the use of the mattress sutures is a problem with regards to distortion of the root, and quite frankly, we just find it easier to use as a teaching technique with the wide variety of individuals in that role that are encountered.

I agree with all of your indications for the use of bioroots. We have used it for all the indications that you have listed. However, I agree that there is a wide variety of patients in whom this approach can be employed, including those with endocarditis, younger individuals wanting to avoid anticoagulation, and patients with small roots in whom the hemodynamic advantages of the stentless valve make it preferable over the mechanical or the stented bioprosthetic valve.

DR JOHN S. IKONOMIDIS (Charleston, SC): Can you compare and contrast for us the utility of this device vs use of a composite prosthesis consisting of a stented bioprosthesis sewn to a Dacron [DuPont, Wilmington, DE] graft?

DR COSELLI: Quite simply, the superior hemodynamics for any given size is better with the stentless valve than for the same size and virtually any stented valve or mechanical valve. So I think therein lies the primary advantage.


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
References
 
This project was supported by a St. Luke's Episcopal Hospital Roderick Duncan MacDonald Research Fund Award to Dr. Coselli. We thank Scott A. Weldon, MA, CMI, for creating the illustrations; Stephen N. Palmer, PhD, ELS, for providing editorial support; Janet Shaw, LPN, and Jennifer Parenti, RN, for assisting with data collection and follow-up; and Xing Li Wang, MD, PhD, for assistance with statistical analysis.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

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