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Ann Thorac Surg 2006;81:2020-2025
© 2006 The Society of Thoracic Surgeons

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Original article: General thoracic

Outcomes of Delayed Chest Closure After Bilateral Lung Transplantation

^a Division of Cardiothoracic Surgery, Emory University Hospital and Clinic, Atlanta, Georgia
^b Division of Pulmonary Medicine, Emory University Hospital and Clinic, Atlanta, Georgia
^c McKelvey Lung Transplant Center, Emory University Hospital and Clinic, Atlanta, Georgia

Accepted for publication January 10, 2006.

^_* Address correspondence to Dr Force, Section of General Thoracic Surgery, The Emory Clinic, 1365 Clifton Rd NE, Bldg A, Ste 2100, Atlanta, GA 30322 (Email: sethforce{at}emoryhealthcare.org).

Presented at the Fifty-second Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 10–12, 2005.

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
BACKGROUND: Delayed chest closure (DCC) may be used after bilateral lung transplantation when significant bleeding/coagulopathy or severe pulmonary edema exists. Primary chest closure (PCC) in these patients can lead to heart and lung compression causing cardiopulmonary instability. The purpose of this study is to describe factors associated with DCC and evaluate outcomes after DCC.

METHODS: We performed a retrospective review of all patients undergoing bilateral lung transplantation between September 2003 and March 2005. Statistical significance was determined by two-tailed t test or Fisher's exact test.

RESULTS: Twenty-eight bilateral lung transplantations were performed. Indication for transplant was chronic obstructive pulmonary disease (13), pulmonary fibrosis (5), cystic fibrosis (5), sarcoidosis (3), and pulmonary hypertension (1). Seven patients (25%) required DCC. Mean time to DCC was 5.3 days. Six patients (86%) with DCC required tracheostomy versus 4 patients (20%) with PCC (p = 0.003). Mean days to discharge was 44 in the DCC group and 21 in the PCC group (p = 0.03). Thirty-day survival was 100% in the DCC group and 95% in the PCC group (p = 1.0). There were no wound infections in either group, and 1 patient in the PCC group had sternal nonunion. Delayed chest closure was associated with cardiopulmonary bypass use (p = 0.006), cardiopulmonary bypass time longer than mean cardiopulmonary bypass time (mean, 224 minutes; p = 0.04), PaO₂/FiO₂ less than mean + 1 SD (value = 4.63, p = 0.0002), evidence of moderate/severe reperfusion injury on chest radiograph (p = 0.0002), and PaO₂/FiO₂ less than mean plus moderate/severe reperfusion injury on chest radiograph (p = 0.002).

CONCLUSIONS: Cardiopulmonary bypass use, prolonged cardiopulmonary bypass time, and significant reperfusion injury, as determined by chest radiograph and a low PaO₂/FiO₂ ratio were all associated with an increased incidence of DCC in our bilateral lung transplantation patients. These patients had no wound infections or sternal complications, and although they had longer hospital stays than PCC patients, DCC did not affect operative survival. Delayed chest closure can be employed safely, when necessary, after bilateral lung transplantation with outcomes similar to patients with PCC.

	Introduction

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The importance of delayed sternal closure after complicated cardiac surgery procedures has been recognized since the 1970s [1]. Since that time, delayed sternal closure has been used routinely in adult and pediatric patients in whom cardiac failure develops after cardiac surgical procedures [2, 3]. The open chest is thought to prevent heart and lung compression in patients with significant myocardial and pulmonary edema and those at high risk for postoperative bleeding [4].

Certain patients undergoing lung transplantation, those with prolonged cardiopulmonary bypass times, those with significant intraoperative reperfusion injury, and those with significant intraoperative bleeding are at risk for the same myocardial and pulmonary edema that is witnessed in patients after complex cardiac surgical procedures. Delayed chest closure (DCC) may be an option in these lung transplant patients, but DCC only appears as a brief mention in the lung transplant literature [5]. Therefore, we reviewed our patients who underwent DCC after bilateral lung transplantation to evaluate their outcomes and to identify any variables associated with the need for DCC.

	Patients and Methods

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After approval by our Institutional Review Board, and waiver of need for individual consent, we reviewed our lung transplant database for all patients who underwent bilateral lung transplantation from January 2003 to March 2005. The patients were grouped according to the type of chest closure: primary chest closure (PCC) or DCC. The two groups were then compared with respect to demographics, outcomes, and preoperative and postoperative variables associated with DCC. The variables selected included posttransplant mean PaO₂ and PaCO₂, mean preoperative pulmonary artery pressure, preoperative systolic pulmonary artery pressure, the use of cardiopulmonary bypass, mean cardiopulmonary bypass time, mean ischemic time, presence of primary graft dysfunction (PGD), history of thoracic procedures, body mass index less than 20 or greater than 30, number of packed red blood cells transfused intraoperatively, and the donor/recipient height ratio. Primary graft dysfunction (R-score) was scored from 0 to 3 as defined by the International Heart and Lung Transplant Society Primary Graft Dysfunction Working Group. The R-scores of 0, 1, 2, and 3 were defined as PaO₂/FiO₂ ratios of greater than 300, 200 to 299, and less than 200, respectively. Patients with R-scores of 1 to 3 also had chest radiographic findings of pulmonary edema [6]. Cardiopulmonary bypass was utilized only when cardiac or pulmonary instability was present.

Statistical Analysis
Univariate group comparisons of continuous variables were examined with two-sample t tests or Wilcoxon tests if assumptions were unverifiable. Categorical variables were examined with Fisher's exact test. All analyses are evaluated at the alpha = 0.05 statistical level. The analyses were conducted using the SAS 9.0 statistical program (SAS Institute, Cary, North Carolina).

Surgical Technique
All patients received bilateral lung transplants using the surgical technique described by Pasque and colleagues [7]. Exposure was achieved using bilateral anterior thoracotomies with or without sternal division. Postoperatively all patients were maintained on our standard immunosuppression regimen consisting of cyclosporine A, Cellcept (Roche, Nutley, NJ), and prednisone. The decision to leave a chest open was made by the transplant surgeon and was based on cardiac and pulmonary impairment during attempted closure. Cardiac variables were measured by pulmonary artery catheter and transesophageal echocardiography. Chest cavities that were left open were covered with a double layer of latex-free Esmark bandaging (Fulflex Elastomerics Worldwide, Lincoln, Rhode Island), which was sewn, circumferentially, to the skin using running 2-0 nonabsorbable suture. The Esmark bandage was then covered with an Ioban drape (3M, St. Paul, Minnesota). Only 1 patient required the use of a rib spreader for active sternal separation. All of the transplant patients were placed on intravenous clindamycin and ceftazidime as per the transplant protocol, and DCC patients were additionally placed on intravenous vancomycin until the chest was closed. Cultures were taken of the skin and pleural spaces at the time of chest closure, and the antibiotic regimen was adjusted accordingly. All patients with moderate to severe PGD were maintained on inhaled nitric oxide until their FiO₂ was less than 50%.

The timing of chest closure was based on radiographic evidence of resolving pulmonary edema, improving PaO₂/FiO₂, decreasing inotrope requirement, ability to actively diurese the patient and decreasing soft tissue edema and body weight. Chest closure was performed in the same manner for all PCC and DCC patients who underwent bilateral thoracosternotomies. The sternum was reapproximated with three sternal wires. One wire was place in the middle of the sternum in a figure-of-eight fashion, and two simple wires were placed on either side of that one. The ribs were closed with six number 2 Vicryl (Ethicon, Sommerville, New Jersey) sutures placed in a figure-of-eight fashion. The dermis was reapproximated with a 2-0 Vicryl suture, and the skin was closed with a 3-0 Vicryl suture. Dermabond (Ethicon/Johnson and Johnson, Sommerville, New Jersey) was used to cover the incision.

	Results

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Twenty-eight patients underwent bilateral lung transplantation at our institution between January 2003 and March 2005. Seven patients (25%) underwent DCC and the remaining 21 had PCC. The demographics for the two groups are shown in Table 1.

The mean time to chest closure was 5.3 days (range, 3 to 7) in the DCC group. Six patients (86%) with DCC required tracheostomy versus 4 patients (20%) with PCC (p = 0.003). Mean days to discharge was 44 (range, 26 to 76) in the DCC group and 21 days (range, 10 to 68) in the PCC group (p = 0.03). Thirty-day survival was 100% in the DCC group and 95% in the PCC group (p = 1.0). All patients, except the 1 who died in the PCC group, were discharged from the hospital. There were no wound infections in any of the 28 patients; and only 1 patient, who was in the PCC group, had a sternal nonunion. This nonunion was not associated with a sternal infection and was treated with sternal plating.

Variables associated with DCC were evaluated by univariate analysis and are shown in Table 2. Specific characteristics of the DCC group are shown in Tables 3, 4, and 5. Variables found to be associated with DCC were significant intraoperative blood transfusion, elevated systolic pulmonary artery pressure, the use of cardiopulmonary bypass, mean cardiopulmonary bypass time longer than 4 hours, lung ischemic time longer than 5 hours, a PaO₂/FiO₂ of 2.5 or less, and an R-score of 2 or greater. Variables that were not found to be associated with DCC included the history of previous thoracic surgery, mean pulmonary artery pressure, and the first postoperative PaO₂ and PaCO₂ values. The donor height/recipient height was found to be significantly associated with DCC, with a ratio in the DCC group of less than 1. This result is due to the large number of emphysema patients in the PCC group who had "oversized" donors, and therefore represents a statistical anomaly rather than a true association.

	Comment

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The benefit of DCC in patients with significant cardiopulmonary edema is the avoidance of further respiratory and hemodynamic compromise, caused by a confined rigid space. In theory, DCC prevents lung and heart compression leading to decreased airway pressures and better right and left ventricular function and prevents the deleterious cardiac effects caused by increasing levels of positive end-expiratory pressure. The end result is a more hemodynamically stable patient who can be maintained on lower levels of cardiopulmonary support and who can be diuresed safely while waiting for the lungs to heal (Figs 1 and 2). This concept is supported by data from Pilcher and colleagues [[12], who found an increased operative mortality (13%) in patients after lung transplantation, who were found to have elevated central venous pressure, the need for greater inotropic support and lower PaO₂/FiO₂ ratios.

View larger version (141K): [in this window] [in a new window]   Fig 1. Postoperative chest radiograph of a patient with primary graft dysfunction and opened chest after bilateral lung transplant.

View larger version (127K): [in this window] [in a new window]   Fig 2. Same patient as in Figure 1, one month later with chest closed and extubated.

The results after retransplantation for PGD are not much better than those after ECMO. Werkerle and colleagues [16] found a 78% 30-day mortality in patients who underwent early retransplantation for graft dysfunction. Data from the Pulmonary Retransplant Registry showed a 47% 1-year survival in all patients undergoing retransplantation. However, the survival was significantly lower for patients being transplanted for nonbronchiolitis obliterans graft failure, for those who were retransplanted less than 2 years after their original transplant, and for patients who were nonambulatory at the time of retransplant [17].

The high incidence of graft dysfunction in the patient population presented is due to the high-risk nature of the patients transplanted. This group included patients with Eisenmenger's syndrome, sarcoidosis with pulmonary hypertension, complex pleural spaces, and ventilator dependence at the time of transplantation. Although 5 of the DCC patients met criteria for moderate to severe PGD, none of these patients died, and all of these patients were discharged from the hospital. There was increased morbidity in the group, but surprisingly there were no wound or sternal complications. Delayed sternal closure is a safe technique and provides good short-term survival for patients after bilateral lung transplantation. Delayed chest closure may also provide a treatment option, aside from ECMO and retransplantation, for patients in whom PGD develops. Aggressive use of DCC may lead to a decreased operative mortality for this high-risk patient population.

	Discussion

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DR MALCOLM M. DECAMP (Boston, MA): Fabulous presentation. I really enjoyed that. I have one analytic question and one technical question. The analytic question is, primary graft dysfunction, as you defined it, is a mixture of the aA gradient and the chest X-ray. But you are having to make this decision in the operating room, and I don't think you are advocating we get a chest X-ray in the OR. So you are really talking about looking at a significant aA gradient at the conclusion of your operation to guide your decision regarding chest closure. Is that correct?

DR FORCE: It is really difficult to define risk factors, and I strayed away from that in my paper and in my talk in calling these associated variables. You saw in the slide the reasons for delayed chest closure. They are made at the time of surgery. It is very difficult to predict the need for chest closure, and I am not sure that it makes a difference in outcomes trying to predict at the end of the case who might need this. I think what seems to be more important, at least from this study, is that if you do leave a patient's chest open, they seem to do well. I think if we had a larger number of patients, we may be able to make some broader predictions. But I don't think based on this small series that I could say just based on that, on the PaO₂/FiO₂ ratio, that those patients would do better.

DR DECAMP: Would you then advocate in patients, when you get up to the intensive care unit and you are in this situation some hours later, that reopening could help?

DR FORCE: Well, yes, I think that might be a possibility. Currently your options right now, as I mentioned, are retransplantation, ECMO, or opening their chest. I do think that a first step would be to open their chest. It seems to be the less morbid of the options and probably the easiest, definitely the easiest to do out of those three options. So I would recommend opening a patient's chest if you do get in that situation.

DR DECAMP: And then the technical question, when leaving some of these clamshell thoracotomies open, the edges of the sternum tend to rub on or create a divot in the middle of the right ventricle. Do you have any little technical tricks to prevent that problem, short of leaving the retractor in?

DR FORCE: We haven't had a significant problem with that. A couple of patients I have put a lap sponge in the chest to prevent the edge of the sternum from rubbing on the right ventricle. I haven't had any significant right ventricle compression from that part of the sternum, but I know in talking with others that that can happen. Some people, like in the pediatric population where they can suture a little metal strut to the sternum, you can do that to keep it off the ventricle.

DR FREDERICK L. GROVER (Denver, CO): Very nicely presented, Seth, and obviously good results to get out of a tough situation. I have a couple of questions. Early on, 10 or 15 years ago, when I was first doing these, I had some of these kind of issues. We have seen a lot less lately, and I think we currently maybe only have, I would guess, less than 5%, maybe 3% or 4%, not a 25% incidence of doing this, of having to leave their chest open and being in that situation. We hardly ever pump anybody except for primary pulmonary hypertension (PPH), although sometimes we have to, but it is certainly in the minority. So it is in the pump patients that you tend to have most of this problem where they take on a lot of fluid. If we are doing a heart–double-lung or a double-lung for PPH where we know we are going to be on the pump or they have got a ductus or some other mitigating factor that might prolong that pump, we tend to slightly undersize, and I learned a long time ago, actually we do a lot more than just height and weight. So one of my questions is, we take into account chest circumference, vertical and horizontal, which a lot don't, particularly in double-lungs or heart–double-lungs where you may be on the pump and may have edema. We also use ultrafiltration during the pump. I would be interested if you do that to try to keep the fluid down. And then part of this implies potential problems with donor preservation and what your donor preservation technique is. But thanks a lot. Nice paper.

DR FORCE: Thank you. Just to address those questions, we do use ultrafiltration on the cardiopulmonary bypass circuit for these patients. As far as downsizing the donors, currently I just use height, and I know there are a lot of published papers debating what is the best method. We do try to downsize in complicated patients, but we have been fairly aggressive in just trying to get the patients transplanted. As you know, with a very low numbers of lungs being used overall from donors, sometimes you are stuck lungs that may not be a perfect size match.

This series really represents a hyperbole. These were all very high risk patients. For example, 1 patient was a gentleman with sarcoid, pulmonary hypertension, who had had a right thoracotomy and pleurectomy and a left thoracotomy and talc pleurodesis. There were 3 patients with sarcoid and pulmonary hypertension. Some institutions are not transplanting those patients anymore because of high operative mortality. The very high risk nature of these patients accounted for the high incidence of severe reperfusion injury.

When we looked back, our incidence of primary graft dysfunction is 25%, which is the incidence that is quoted in most studies, but that wasn't our incidence of delayed chest closure, and these were not all the patients. These were only the bilateral lung transplant patients. So, again, the reason really for putting this together was to show that if you need to do this, you can and the patients do well.

Regarding the preservation technique, we use a fairly standard preservation technique. It is with Perfadex, included in that is prostacyclin, THAM, nitroglycerin, and calcium, and we use antegrade and retrograde protection. I don't think it was the method of preservation. Characteristics that were associated with primary graft dysfunction included long ischemic time, over 6 hours, and the use of cardiopulmonary bypass. Many papers quote one or both or most of the variables that we found as significant risks for primary graft dysfunction. The International Society of Heart and Lung Transplantation is working on putting those risk factors together to further evaluate primary graft dysfunction.

DR THORALF SUNDT (Rochester, MN): I am a bit of a spectator in the field of lung transplantation, but I am trying to reconcile this kind of a study with the basic science study that we heard this morning discussing the importance of controlled reperfusion and the role of cardiopulmonary bypass in lung transplantation. The patients who went on pump did worse, but can we really separate out the impact of the pump and the importance of preoperative condition? Was the issue really that the people who were put on-pump were the sickest patients and that is why they have the toughest time? We tend to accept clinically that we should avoid bypass to the extent possible, and yet experimental studies demonstrate controlled reperfusion favorably impacts graft function, and that should be easiest to accomplish with bypass. When we do a double-lung without bypass, we put in a lung that has had 5 hours of ischemic time, and then we force all of the cardiac output through it while we are putting in the second lung. It just doesn't make sense in terms of controlled reperfusion. I just wondered if you had a comment about that.

DR FORCE: I think the problems that you have with that are problems that we all have, especially in lung transplantation. There really aren't enough patients transplanted per year to make valid comparisons. So if you look at one institution's data where cardiopulmonary bypass is used frequently, they may have better outcomes in these patients than at a center where cardiopulmonary bypass is used only when absolutely necessary, when the patients have severe pulmonary hypertension, when we have primary graft dysfunction after the first lung is implanted, and we have to go on emergent bypass. Therefore, you will have worse results in these patients. I do believe in a controlled reperfusion, and I think one way of doing that is by slowly releasing the clamp on the lung that you have transplanted if you are not on bypass. The other way is to actually form the circuit and reperfuse that lung in a controlled fashion. Who is at risk for primary graft dysfunction is difficult to tease out because we are dealing with different donors, different recipients, different ways of doing the procedure, single lungs, and bilateral lungs.

	Acknowledgments

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Supported by The McKelvey Foundation Fund of the Tides Foundation.

	References

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 

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