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Ann Thorac Surg 2006;81:1199-1204
© 2006 The Society of Thoracic Surgeons


Original article: General thoracic

Techniques of Reconstruction for Inadequate Donor Left Atrial Cuff in Lung Transplantation

Takahiro Oto, MD a , * , Marc Rabinov, FRACS a , Justin Negri, FRACS a , Silvana Marasco, FRACS a , Michael Rowland, FRACS a , Adrian Pick, FRACS a , Gregory Snell, FRACP b , Franklin Rosenfeldt, FRACS a , Donald Esmore, FRACS a

a Department of Cardiothoracic Surgery, The Alfred Hospital, Monash University, Melbourne, Australia
b Department of Respiratory Medicine, The Alfred Hospital, Monash University, Melbourne, Australia

Accepted for publication November 28, 2005.

* Address correspondence to Dr Oto, Department of Cardiothoracic Surgery, The Alfred Hospital, Commercial Rd, Melbourne, VIC 3004, Australia (Email: takahirooto{at}aol.com).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: An inadequate donor left atrial (LA) cuff due to an anatomical abnormality of the pulmonary vasculature or technical errors at the time of procurement can exclude the lungs from transplant. This study aims to describe the incidence, efficacy, and various techniques of LA cuff reconstruction in lung transplantation.

METHODS: A total of 637 pulmonary venous anastomosis in 405 consecutive lung transplants from January 1995 to July 2005 were reviewed. Comparison between the patients who required LA cuff reconstruction (reconstruction group) or who did not (no-reconstruction group) was made in posttransplant outcomes.

RESULTS: An overall incidence of requirement of LA cuff reconstruction was 2.7% (4% on the right, 1% on the left, p = 0.03). Seventy-one percent of LA inadequacy was corrected using a pericardial patch on the anterior LA cuff wall; the remainder required complicated reconstruction for separated/short pulmonary veins to create a new LA cuff. There was no significant difference between the reconstruction and no-reconstruction groups, respectively, in oxygenation (329 ± 28, 337 ± 10, p = 0.81), duration of intubation and intensive care unit stay (p = 0.54, p = 0.89, respectively), 30-day mortality (12%, 6%, p = 0.30), and 5-year survival (57%, 52%, p = 0.80).

CONCLUSIONS: Inadequate donor LA cuff is an infrequent but potentially serious complication in lung transplantation. Donor LA cuff reconstruction using donor pericardium or pulmonary artery remnant is a useful technique to salvage surgically marginal lungs without affecting early and late posttransplant outcomes. These lungs should not be excluded from transplantation.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
A single anastomosis between the donor left atrial cuff and the recipient left atrium rather than anastomosing individual pulmonary veins is a well-established technique for minimizing procedure time and the risks of stenosis and thrombosis in lung transplantation [1]. Owing to the anatomical abnormalities of the donor pulmonary vasculature or technical errors at the time of procurement, surgeons occasionally face an inadequate donor left atrial cuff at the confluence of the superior and inferior pulmonary veins for anastomosis to the left atrium of the recipient [1–4]. Major inadequacy of the left atrial cuff could potentially exclude the lungs from transplant; however, on many occasions, the surgeon is required to still use lungs with inadequate cuffs, as critically ill recipients have already undergone thoracotomy and the transplant procedure has passed the "point of no return". Despite the various degrees of inadequacy of the donor left atrial cuff, efforts must then be made to repair or to reconstruct the pulmonary venous cuff to overcome this technical challenge.

A few case reports have described techniques for the management of an inadequate left atrial cuff [1–4]; however, no study has shown the incidence, techniques, and efficacy of left atrial reconstructions in lung transplantation. We describe various techniques for left atrial cuff reconstruction to overcome donor inadequacies in lung transplantation by reviewing our own experience and the previous literature.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
From January 1995 to July 2005, in 405 consecutive lung transplant procedures, a total of 637 pulmonary venous anastomosis including 232 bilateral and 173 single lung transplants were performed at the Alfred Hospital, Melbourne, Australia. Institutional Ethics Committee advice was sought, and ethical exemption without the necessity for consent was confirmed.

Transplant Protocol
Details of donor and recipient assessment and matching are described elsewhere [5–7]. Although lung donor selection criteria are based on standard criteria [8], extended or marginal donors, including a donor history of asthma [6] and smoking more than 20 pack-years [5], an abnormal chest radiograph, purulent secretions on bronchoscopy, age more than 55 years, and an arterial oxygen tension/inspired oxygen consumption (PaO2/FiO2) ratio less than 300 mm Hg [7], are commonly utilized at our institution.

Donor Lung Procurement
Lung procurement and preservation followed standard procedures [9]. In Australia, the home state of the donor has priority to receive the donor referral; however, any organs including heart/lungs not utilized in the donor state are offered to interstate transplant programs in rotation. Normally, the surgeons from the transplant center where the organs are to be implanted perform the donor procurement. Occasionally, lungs not utilized in the donor state are procured and transported to other centers by local surgeon. Heart-lung en-bloc procurement including an intravenous infusion of prostacyclin (Flolan; Wellcome, Sydney, Australia) at 40 to 80 ng · kg–1 · min–1 for approximately 10 minutes before cross clamp followed by single antegrade flush with cold modified Euro-Collins solution is routinely performed. The flush solution is drained through the transected left atrial appendage to ensure adequate decompression of the left atrium. In September 2004, Perfadex (Vitrolife, Göteborg, Sweden) replaced Euro-Collins solution at our institution.

The details of the operative findings of the donor lungs at the time of organ procurement, including any anatomical abnormalities, are reported to the transplant surgeon by the procuring surgeon and the donor coordinator. Division of a heart-lung bloc is usually performed in the recipient operating theater; however, when the heart is to be utilized in another center, the heart-lung bloc is divided in the donor hospital. In the recipient theater, the lungs are again carefully inspected on the back table before completion of recipient pneumonectomy. Bronchial, pulmonary arterial, and left atrial cuffs of the donor lungs are trimmed in preparation for single anastomosis. In the study group, when the left atrial cuff was inadequate for anastomosis, efforts had to be made to repair it not only by further dissection and freeing of the pulmonary veins and the left atrial cuff but also by repair and reconstruction with a donor pericardial patch or donor pulmonary arterial remnant. The recipient superior and inferior pulmonary veins were separately disconnected, and the junction of the veins was opened to maximize left atrial cuff circumference on the recipient.

Repair/Reconstruction of Left Atrial Cuff
Techniques of reconstruction for various degrees of inadequate left atrial cuff are depicted in Figure 1. When an inadequate length of the left atrial cuff was limited in its anterior wall, a partial patch augmentation of the anterior wall with donor pericardium was performed (Fig 1A). When an inadequate length of the left atrial cuff was seen in both its anterior and posterior wall, a donor pericardial patch repair was performed for both the anterior and posterior wall (Fig 1B). When the superior and inferior pulmonary veins were separated, further dissection of the distal pulmonary veins was performed to gain additional length of both superior and inferior pulmonary veins, and then the two separate veins were sutured back together directly with a wide septum to recreate an oval cross sectional cuff (Fig 1C) [4]. When the separated superior and inferior pulmonary veins were too short to be directly sutured back together, the divided edges of the two veins were sutured with pericardium around each of the vein orifices to create a new cuff (Fig 1D) [2, 3]. When the inferior pulmonary vein had been amputated at the level of the two segmental branches, the segmental veins were sutured back together, and a segment of donor pulmonary artery was used to create a new inferior pulmonary vein conduit. This new conduit was then sutured to the superior pulmonary vein to form a new left atrial cuff (Fig 1E and Fig 2). All these reconstructions were performed using a 5-0 polypropylene running suture. Care was taken not to stretch or twist the pulmonary venous anastomosis.


Figure 1
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Fig 1. Reconstruction techniques for an inadequate left atrial cuff. (A) For a short length of the left atrial cuff limited in its anterior wall, a partial patch repair with donor pericardium was performed. (B) For a short length of the left atrial cuff seen both in its anterior and posterior wall, a donor pericardial patch repair for both the anterior and posterior walls was performed. (C) For separated superior and inferior pulmonary veins, the two separated veins were directly sutured back together with a wide septum to create an oval cross-sectional cuff. (D) For separated superior and inferior pulmonary veins that were too short to be directly sutured back together, the divided edges of the two veins were sutured with pericardium around each of the vein orifices, and a new cuff was created. (E) When the inferior pulmonary vein was discontinued at the level of a segmental branch, a cylinder of donor pulmonary artery was used as a conduit between segmental veins that had been sutured back together. This cylinder was sutured to the superior pulmonary vein to create a new atrial cuff.

 

Figure 2
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Fig 2. Operative photographs (top panels) and corresponding line diagrams (bottom panels) showing the technique for reconstructing a new left atrial cuff using a segment of donor pulmonary artery as a conduit.

 
Transplant Procedure
Details of the techniques of single and bilateral lung transplantation at our institution have been described elsewhere [10–13]. At the time of completion of implantation, retrograde deairing was followed by antegrade deairing through the untied pulmonary vascular suture line. All the vascular anastomoses were then carefully inspected to detect any tension, kinking, narrowing, or bleeding. Transesophageal echocardiography was routinely performed to confirm adequate pulmonary venous flow. When a pulmonary venous anastomotic problem was suspected, direct pressure measurement using a fine needle inserted into the pulmonary vein was performed to detect any pressure gradient across the anastomosis between the pulmonary veins and the left atrium.

Study Groups
For the purpose of analysis recipients and donors were divided into two groups: recipients who required left atrial reconstruction (reconstruction group) and recipients who did not (no-reconstruction group).

Assessment of Outcome
Indicators of outcome were PaO2/FiO2 ratio at 12 hours after transplantation [14], duration of intubation, length of intensive care unit (ICU) stay, 30-day mortality, and 5-year survival.

Statistical Analysis
Analysis was performed using Statview 5.0 software package (SAS Institute, Cary, North Carolina). Continuous data were expressed as mean ± SEM, and categorical data were expressed as counts and proportions. Comparison between groups was performed with the {chi}2 test for categorical variables, with the Student t test for parametric continuous variables and with the Mann-Whitney U test for nonparametric continuous variables. Duration of intubation, length of ICU stay, and 5-year survival rate were estimated by the Kaplan-Meier method, and the curves were analyzed by use of the log-rank test. A p value of 0.05 was considered to be statistically significant.


    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
Incidence and Types of Left Atrial Reconstruction
Of a total of 637 left atrial cuffs, 17 required reconstruction for an overall incidence of 2.7%. The incidence of reconstruction on the right side (13 of 325, 4%) was significantly higher than that on the left side (4 of 312, 1%; p = 0.03). Types of inadequacy and reconstruction of the left atrial cuff were as follows: 12 of 17 (71%) were type A; 2 of 17 (12%) were type B, and 1 each of 17 was type C, D, and E (Fig 1). An anatomic abnormality of the donor pulmonary vein was seen in one case (type E) such that each of the superior pulmonary vein and two segmental inferior pulmonary veins drained separately into the left atrium. No patient in the reconstruction group was given anticoagulant therapy.

Donor and Recipient Demographics
Demographics of the donor and the recipients are shown in Table 1. There was no significant difference between two groups except for location of the organ procurement team. Lungs procured by surgeons from institutions other than the Alfred, had a greater likelihood of requiring left atrial cuff reconstruction (p = 0.02). In the reconstruction group, in the majority of cases heart-lung block was divided and the heart sent for heart transplantation [16 of 17 (94%)]. In the no-reconstruction group, sufficient data regarding the incidence of the separate heart excision for heart transplantation in other institutions were not available. To our knowledge, no donor lung was discarded because of problems with the adequacy of the left atrial cuff.


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Table 1. Demographics of Donor and Recipient
 
Oxygenation
There was no significant difference in PaO2/FiO2 ratio between the reconstruction and the no-reconstruction group (329 ± 28, 337 ± 10; p = 0.81). In the reconstruction group, poor oxygenation (PaO2/FiO2 ratio < 200) with pulmonary infiltrate on chest radiograph was seen in 2 patients with type A reconstruction within 24 hours after operation; however, transesophageal echocardiography confirmed a patent left atrial anastomosis and adequate venous flow.

Duration of Intubation and Intensive Care Unit Stay
The percentage of patient not extubated more than 24 hours in the reconstruction and no-reconstruction groups were 31% versus 36% (p = 0.54), respectively; and the percentage of patients staying in the intensive care unit more than 7 days in the reconstruction and no-reconstruction groups were 17% versus 21% (p = 0.89), respectively.

Pulmonary Venous Anastomotic Complications
In the reconstruction group, no vascular anastomotic complications, including narrowing, obstruction, bleeding, and thromboembolic events, were seen. Ventilation/perfusion scan 3 months after transplantation showed matched ventilation/perfusion distribution without defect of perfusion on the reconstructed graft. In the no-reconstruction group, 1 patient required pulmonary venous reanastomosis owing to twisting; however, the left atrial cuffs of the donor and the recipient were sufficient, and no left atrial reconstruction was required for reanastomosis.

Thirty-Day Mortality
The 30-day mortality rates in reconstruction and no-reconstruction groups were 2 of 17 (12%) and 22 of 388 (6%), respectively, with no significant difference between the groups (p = 0.30). The cause of both deaths in the reconstruction group was acute rejection. Autopsy revealed that there was no pulmonary venous anastomotic problem in each of the cases.

Five-Year Survival
The 5-year survivals in the reconstruction and no-reconstruction groups were 57% and 52%, respectively, and there was no significant difference between the two groups (p = 0.80).


    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
This retrospective study shows that an "inadequate" donor left atrial cuff is an infrequent technical consideration in lung transplantation; however, overcoming this problem is crucial for salvaging not only surgically marginal lungs but also critically ill patients who have already undergone thoracotomy. Most of the cases in the reconstruction group were corrected by pericardial patch repair (71%) whereas others required more complicated reconstructions. An inadequate left atrial cuff was seen more frequently on the right side than on the left side. This series reemphasizes the importance of careful surgical dissection, evaluation, and preparation of both the pulmonary and cardiac donor grafts. It is clear that the training of all lung and cardiac retrieval surgeons need to encompass this issue. Additionally, when noted, this information must be passed on to the recipient team.

To prevent this complication intraatrial (Sondegaard's) groove should be developed in the donor either at the time of procurement or during division of the heart-lung block. To ensure adequacy of the left atrial cuff, careful dissection of the donor pulmonary veins distally, development of Sondegaard's groove, and freeing of the recipient left atrial cuff from posterior pericardium can make available more tissue for both donor and recipient atrial cuffs.

This is the first report of successful use of remnant donor pulmonary artery as a tissue substitute to reconstruct an inadequate donor left atrial cuff. Schmidt and colleagues [15] reported the successful use of donor iliac vein to bridge an anomalous pulmonary vein to a left atrial cuff. Parekh and Patterson [1] described the use of the donor superior vena cava and pulmonary artery. The remnant posterior aspect of donor left atrium may also be useful for a patch repair. During surgical donor organ preparation and implantation, it is important to retain on the table all tissue, including fragments of donor pericardium, pulmonary artery, and superior vena cava trimmed from donor graft for potential use as a patch or conduit.

Pericardial patch repairs for type A and B inadequacy can be performed during the anastomosis procedure. More complicated reconstructions for type C, D, and E inadequacy should be performed on a back table before implantation to avoid extra warm ischemic time.

During deairing and reperfusion procedures, care must be made to detect any tension, twisting, or kinking of the venous anastomosis and any sign of rapidly increasing hardness, weight, and darkness in the newly implanted lungs that might indicate incipient pulmonary congestion and edema. If pulmonary venous obstruction is suspected, direct pressure gradient measurement between pulmonary veins and left atrium should be made.

In the early postoperative period, the development of increased pulmonary arterial pressure, increased inotrope requirement or decreased oxygenation should prompt further examination and investigation including transesophageal echocardiography. These are required to distinguish pulmonary venous anastomosis obstruction from ischemia-reperfusion injury, cardiac failure, acute rejection, and fluid overload. Although no pulmonary venous anastomotic problem was seen in the reconstruction group, once anastomotic problems are recognized, immediate reanastomosis should be undertaken.

No patient in the reconstruction group was given anticoagulant therapy because of left atrial reconstruction. It is difficult to initiate anticoagulant therapy in the early posttransplant period because of concerns for bleeding, renal insufficiency, and varying drugs and general condition. This study indicated that anticoagulant therapy was unnecessary for left atrial cuff reconstruction with sufficient pulmonary venous flow.

Long-term outcomes of the left atrial cuff reconstruction including chronic obstruction or stenosis remained unknown. However, no patient in the reconstruction group died of pulmonary venous anastomotic complications, and left atrial reconstruction did not affect 5-year survival.

In conclusion, donor left atrial cuff inadequacy is an infrequent but potentially serious complication in lung transplantation. Donor left atrial cuff reconstruction using donor pericardium or pulmonary artery, or both, is a useful technique to salvage surgically marginal lungs. Utilizing lungs with an inadequate left atrial cuff need not affect early and late outcomes after lung transplantation, and these lungs should not be excluded from transplantation.


    Acknowledgments
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 
We gratefully acknowledge Anne Griffiths and Sharon Daly for assembling and verifying the clinical data, and Robin McEgan for providing the clinical photograph. We also wish to extend our appreciation to members of the Heart and Lung Transplant Service, The Alfred Hospital, for their assistance.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Parekh K, Patterson A. Technical considerations in adult lung transplantation Semin Thorac Cardiovasc Surg 2005;16:322-331.
  2. Hammond GL, Franco KL, Baldwin JC. Method of single-lung transplantation in the absence of a left atrial cuff Ann Thorac Surg 1992;54:379-380.[Abstract]
  3. Casula RP, Stoica SC, Wallwork J, Dunning J. Pulmonary vein augmentation for single lung transplantation Ann Thorac Surg 2001;71:1373-1374.[Abstract/Free Full Text]
  4. Kirby TJ, Birnbaum PL. Technique of single lung transplantationIn: Patterson GA, Cauraud L, editors. Lung transplantation. New York: Elsevier; 1995. pp. 195-202.
  5. Oto T, Griffiths AP, Levvey B, et al. A donor history of smoking affects early but not late outcome from lung transplantation Transplantation 2004;78:599-606.[Medline]
  6. Oto T, Griffiths A, Levvey B, et al. Donor history of asthma is not a contraindication to lung transplantation12-year single center experience. J Heart Lung Transplant 2004;23:309-316.[Medline]
  7. Gabbay E, Williams TJ, Griffiths AP, et al. Maximizing the utilization of donor organs offered for lung transplantation Am J Respir Crit Care Med 1999;160:265-271.[Abstract/Free Full Text]
  8. de Perrot M, Snell GI, Babcock WD, et al. Strategies to optimize the use of currently available lung donors J Heart Lung Transplant 2004;23:1127-1134.[Medline]
  9. de Perrot, Keshavjee S. Lung preservation Semin Thorac Cardiovasc Surg 2005;16:300-308.
  10. Oto T, Rabinov M, Griffiths A, et al. Unexpected donor pulmonary embolism affects early outcomes after lung transplantationa major mechanism of primary graft failure?. J Thorac Cardiovasc Surg 2005;130:1446-1452.[Abstract/Free Full Text]
  11. Oto T, Rabinov M, Rosenfeldt F, Esmore DS. Extended pericardiotomy avoids cardiopulmonary bypass during bilateral sequential lung transplantation J Thorac Cardiovasc Surg 2005;129:466-467.[Free Full Text]
  12. Oto T, Rosenfeldt F, Rowland M, et al. Extracorporeal membrane oxygenation after lung transplantationevolving technique improves outcomes. Ann Thorac Surg 2004;78:1230-1235.[Abstract/Free Full Text]
  13. Esmore DS, Brown R, Buckland M, et al. Techniques and results in bilateral sequential single lung transplantation J Cardiac Surg 1994;9:1-14.[Medline]
  14. Oto T, Levvey B, Pilcher DV, Bailey MJ, Snell GI. Evaluation of the oxygenation ratio in the definition of early graft dysfunction post lung transplantation J Thorac Cardiovasc Surg 2005;130:180-186.[Abstract/Free Full Text]
  15. Schmidt F, McGiffin DC, Zorn G, Young KR, Weill D, Kirklin JK. Management of congenital abnormalities of the donor lung Ann Thorac Surg 2001;72:935-937.[Abstract/Free Full Text]



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