Ann Thorac Surg 2003;75:1697-1704
© 2003 The Society of Thoracic Surgeons
Original article: general thoracic
A modified bronchial anastomosis technique for lung transplantation
Carsten Schröder, MDa,
Frank Scholl, MDa,
Emmanuel Daon, MDa,
Andrea Goodwin, RN, MSNa,
William H. Frist, MDa,
John R. Roberts, MDa,
Karla G. Christian, MDa,
Mathew Ninan, MDa,
Aaron P. Milstone, MDb,
James E. Loyd, MDb,
Walter H. Merrill, MDa,
Richard N. Pierson, III, MDa*
a Department of Cardiac and Thoracic Surgery, Vanderbilt University, Nashville, Tennessee, USA
b Department of Medicine, Vanderbilt University, Nashville, Tennessee, USA
Accepted for publication December 22, 2002.
* Address reprint requests to Dr Pierson, Division of Cardiac Surgery, University of Maryland, 22 South Greene St N4W94, Baltimore, MD21201, USA.
e-mail: rpierson{at}smail.umaryland.edu
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Abstract
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BACKGROUND: Low rates of major complications have been reported for the intussuscepting bronchial anastomotic technique but stenosis, malacia, and granulation tissue at the anastomosis may cause clinically important morbidity. We hypothesized that a modification of the telescoping technique that improves bronchial wall apposition might be associated with improved bronchial healing and clinical outcomes.
METHODS: The telescoping horizontal mattress "U-stitch" suture technique was modified to incorporate figure-of-eight sutures placed in the cartilaginous wall between each of three intussuscepting U stitches. Serial videotape records of 152 individual anastomoses (99 modified, 53 telescoped) in 118 consecutive operative survivors were retrospectively reviewed by examiners blinded with respect to technique used. Stenosis, airway instability, mucosa quality, and devascularized luminal tissue were graded at 4 to 14 days (initial), 4 to 12 weeks (early), and 6 to 12 months (late) after transplantation.
RESULTS: The incidence of anastomotic stenosis was significantly lower using the modified technique at the initial (p = 0.025) and late (p = 0.015) observations. In the initial phase airway instability (p = 0.015) and devascularization grades (p = 0.001) were also significant lower in the modified group. There were no significant differences in mucosal condition between techniques. The modified telescoping technique was associated with significant survival advantage (mean 17.7%; p = 0.029) by multivariate analysis. The incidence of major airway complications (dehiscences and stenoses required stents) tended to be lower (3% versus 6%) in the modified group.
CONCLUSIONS: The modified telescoping bronchial anastomosis technique is associated with improved early and late bronchial healing and higher 5-year survival without increased major airway complications.
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Introduction
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Impaired healing of the bronchial anastomosis threatens successful outcome after lung transplantation. Ischemia of the donor bronchus [1, 2] and other factors such as rejection [3], intense immunosuppressive therapy [4], invasive infections [5] or inadequate organ preservation [2] may all contribute to compromised airway healing. Medical and surgical strategies to minimize the risk of dehiscence and stricture allowed safe clinical application of pulmonary parenchymal replacement and they remain the key to success in this field [6].
Bronchial anastomotic techniques have evolved over the last several decades. Multiple interrupted sutures gave way to simpler approaches. Today two suturing techniques are commonly employed. The classic "telescoping" technique [7] uses a running suture of the membranous portion and multiple interrupted U stitches for the cartilaginous portion, intussuscepting one airway (usually the donor) inside the other. This technique leaves a shelf of bronchial tissue protruding into the bronchial lumen, which may necrose or serve as a nidus for retention of secretions or invasive airway infection. In response to these problems, some centers have reported better results using end-to-end technique with a continuous suture [8] although this approach is controversial [6, 9]. Using these surgical strategies the incidence of major bronchial healing complications has fallen below 10% [8, 10]. However it was our clinical impression that problems with bronchial healing such as malacia or subcritical stenosis continue to occur, frequently becoming manifest weeks to month after transplantation.
Based on the presumption that functional bronchial anastomotic narrowing might contribute to significant morbidity we developed a modified intussuscepting technique to address perceived technical deficiencies with previously described intussuscepting interrupted U suture anastomotic technique. In this study we critically assess results using this modification based on retrospective review of a nonrandomized single-center experience. We show improvement of bronchial healing, improved survival, and a trend toward reduced major airway complications.
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Patients and methods
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Study population
One hundred forty-five adult patients underwent single or bilateral sequential lung transplantation at Vanderbilt University Medical Center between November 1990 and February 2001 (Fig 1)
for a variety of end-stage lung diseases. Five-year survival according to airway anastomosis technique was evaluated in all 145 patients and in a subset of 126 patients surviving at least 30 days.
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Fig 1. Distribution of cases (with completed follow-up) by year and anastomotic technique for Vanderbilt lung transplant program over the study period between November 1990 and February 2001. Checkered bars = classic telescoping technique; solid bars = modified telescoping technique.
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For 118 patients at least one bronchoscopic examination was recorded on videotape and was available for retrospective review. Comprehensive clinical records and all available follow-up bronchoscopic examinations were analyzed retrospectively for this group of patients. In this group 34 bilateral sequential single (double) lung transplants and 84 single lung transplants (29 left and 55 right) were performed. A total of 152 anastomoses were retrospectively analyzed by videotape archive of serial fiberoptic bronchoscopy. The mean number of airway observations per patient was 2.1. Fifty-seven patients (22 classic, 35 modified) and 76 anastomoses (25 classic, 51 modified) had airway observations at all three timepoints. Survival and cohort analysis were separately analyzed for the 118 patients included in videotape airway analysis. Of this cohort 8 died within 30 days and 3 additional patients died within 90 days, leaving 110 and 107 patients available for analysis at these times, respectively.
Overall 30-day mortality was 19 of 145 (13.1%). Mean follow-up time for all patients was 3.6 ± 2.5 years (range, 0.1 to 11.4). Attrition in the study population was accounted for by patient death (total n = 85 of 145; classic n = 50 of 70, modified n = 35 of 75). This study was approved by the Vanderbilt Committee for Protection of Human Subjects.
Operative technique
One of two surgical techniques was used for constructing each bronchial anastomosis. Both the classic [7] telescoping technique and the modification employ a running suture in the membranous airway. In addition we invaginate one bronchus into the other (usually the donor into the recipient). The classic technique uses multiple U stitches (Fig 2)
placed in the cartilaginous wall. This technique often leaves a rim of bronchial tissue protruding into the lumen (Fig 2b, arrow). The modification uses three U stitches, in the middle and at either end of the cartilaginous wall. Two or three figure-of-eight sutures (Fig 3a) are placed in between each pair of U stitches to coapt the bronchial walls (Fig 3b, c). Monofilament absorbable polydioxanone (PDS [Ethicon, Somerville, NJ]) replaced absorbable braided polyglactin (Vicryl; Ethicon) in 1992 and was used in every instance thereafter.
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Fig 2. The classic telescoping technique (a) leaves a devascularized shelf of bronchial tissue protruding into the lumen (b, arrow) using just U stitches. A running suture is used for the membranous posterior wall.
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Fig 3. The modified telescoping technique (c) uses just three U stitches (a) at 0, 90 and 180 degrees and two or three figure-of-eight sutures in between (b) to coapt the walls properly. A running suture is used for the membranous posterior wall.
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The modified technique was developed in 1994 by one of the authors (RNP), after 32 single and 2 double lung transplants. Thereafter both techniques were used continuously in varying proportions over the course of the remaining 7 years of study interval for the 84 single and 34 double lung transplants. Choice of anastomotic technique was dictated principally by attending surgeon preference, with the majority performed by supervised surgical trainees. Although the majority of modified technique anastamoses were done or supervised by one surgeon, other surgeons also contributed some cases using this technique. No end-to-end (nonintussuscepting) anastomoses, bronchial revascularization, or pedicle wrap procedures were performed.
Cardiopulmonary bypass was used for all 34 double lung transplants and for 16 of 84 (19%) of single lung transplants.
Therapeutic regimen
Standard immune system suppression consisted of prednisone, cyclosporine, azathioprine, and antibody induction therapy; the regimen remained consistent throughout the study interval. Prednisone 10 mg twice per day was given immediately after transplant and usually tapered to 0.1 mg/kg per day within 3 months. All patients but 1 received antilymphocyte antibody induction therapy intraoperatively and in the early postoperative period. Episodes of rejection were treated with intravenous methylprednisolone at a dose of 1 g/d for 3 days followed by steroid taper. Perioperative antibiotics consisting of vancomycin and a third-generation cephalosporin were administered to all patients. Prophylaxis against Pneumocystis carinii (Bactrim or pentamidine) and herpes (acyclovir) was standard, whereas cytomegalovirus (CMV) prophylaxis was determined by preoperative serologic status of both donor and recipient and postoperative monitoring, as previously described [11].
After 1996 mycophenolate mofetil was occasionally substituted for azathioprine on a case-by-case basis, rarely before 3 months, in the context of recurrent acute rejection, azathioprine intolerance, or for clinical or histologic evidence of obliterative bronchiolitis.
Clinical and bronchoscopic follow-up
Patients underwent initial routine bronchoscopic surveillance before hospital discharge. Routine surveillance bronchoscopic examinations (ie, in the absence of symptoms or abnormalities on chest roentgenogram) were planned for 4 to 8 weeks postoperatively and then every 3 months during the first postoperative year. Results of personal hand-held spirometry or formal pulmonary function testing, radiographic findings, and clinical symptoms were used to determine the need for additional bronchoscopic evaluations.
Lower respiratory tract infection was diagnosed according to standard definitions by deep sputum culture or bronchoscopic lavage.
To evaluate each anastomosis, the initial (4 to 14 days), early (4 to 12 weeks), and late (6 to 12 month) phases of bronchial healing were retrospectively analyzed. Anastomoses were retrospectively scored by one or two independent observers "blinded" with respect to technique used. Four variables were analyzed using semiquantitative grading scales: stenosis (percent luminal narrowing relative to proximal native airway; scoring: < 10% = mild), 10% to 30% = moderate, 30% to 50% = moderately severe, more than 50% = severe); dynamic airway stability (airway patency with spontaneous ventilation or cough; scoring: absent; mild, moderate, severe); donor mucosa quality (viability, vascularity; scoring: 0 = normal pink mucosa, no edema; 1 = pale donor mucosa; 2 = pale and edematous mucosa, paucity of submucosal vessels; 3 = ulceration, erythema; 4 = necrosis, sloughing mucosa); and percent of airway circumference (1% to 100%) exhibiting devascularization in areas of mucosa grading 1 to 4. Major airway complication was defined as anastomotic dehiscence (visible disruption of the suture line) or stent placement for either stenosis or dehiscence.
Statistical analysis
Unless otherwise mentioned all data are presented as means and standard deviation for all variables. Continuous variables were checked for normality by plotting histograms. Variables that were not normally distributed were analyzed using the Kruskal-Wallis test and the Mann-Whitney U test. Those that were normally distributed were assessed with a one-way analysis of variance and the Student t test. The 
2 test for trend was used for scoring variables and their changes over time. Survival statistics were calculated by the Kaplan-Meier method using the log-rank test for significance analysis and two-stage Cox proportional hazard models by adjusting for independent variables (sex, age, preoperative steroids, CMV mismatch, single versus double lung transplantation, cardiopulmonary bypass use, and infection). Correlation between anastomotic technique and other variables was studied using the Pearson or Spearman correlation test. All p values less than 0.05 were considered statistically significant. All tests were two-tailed. All statistical analyses were performed on a personal computer with the statistical package SPSS for Windows (Version 10.0, SPSS, Chicago, IL).
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Results
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Preoperative and operative characteristics
No significant differences were observed between the groups receiving classic or modified telescoping technique with respect to age, sex, proportion of right sided anastomoses, incidence or intensity of preoperative steroids, incidence of cultured respiratory tract infection, or profile of organisms cultured. Bilateral sequential lung transplantation, CMV mismatch, longer graft ischemia time, and use of cardiopulmonary bypass were significantly more common in the modified telescoping group.
Incidence and severity (not shown) of rejection were similar between groups: 35% in the classic group and 39% in the modified technique group experienced a single rejection episode within the first 90 days. Multiple rejection episodes (2 to 4 times) were unusual and seen with similar frequency (4% to 8%) in both groups. Mechanical ventilation time was slightly lower in the modified group (6.3 ± 8.9 days) than in the classic group (7.7 ± 14 days), while the reintubation rate in both groups was 22%. No distinction between duration of intensive care unit stay was possible since program practice was to discharge patients from the intensive care unit. Hospital stay tended to be shorter in the modified group (p = 0.059), with a median of 12 days (Inter quartile range [IQR] 10 to 22 days) compared with 16 (IQR 12.5 to 25.5) days in the classic group.
Bronchial anastomotic complications
In both groups one dehiscence and two stent implantations occurred, for an incidence of major airway complications in the classic group of 6% (3 of 53 anastomoses) versus 3% (3 of 99 anastomoses) in the modified group (p = 0.421). Severe ( > 30%) stenosis was significantly less common using the modified technique at the initial (4% versus 11%; p = 0.025) and late (11% versus 25%; p = 0.015) observations, as illustrated graphically in Figure 4.
Moderate to severe dynamic airway collapse was initially significantly less frequent (p < 0.01) in the modified group (5% versus 21%) but this trend did not maintain significance over subsequent follow-up (Fig 5).
Similarly the devascularization score was significantly lower with the modified technique only at the initial observation (p = 0.001, 2 for trend; Fig 6);
later observations showed no differences between groups as expected (not shown). No differences were appreciated between techniques with respect to donor bronchial mucosal condition, with a mean score on initial assessment of 2.3 (IQR 2 to 3), and subsequent improvement (mean score 1.0, IQR 1 to 2, at early follow-up; and 0.6, IQR 0 to 1, at late follow-up). Statistical findings were confirmed when the 76 anastomoses for which a complete observation set was available (initial, early, and late) were separately analyzed. Additionally correlation analysis showed significance for the same variable pairings as when observed in the complete data set (152 anastomoses).
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Fig 4. Severe stenosis rate (> 30% narrowing relative to caliber of proximal native airway) is significantly lower using the modified telescoping technique. Statistical analysis by 2 for a trend using all grades of stenosis. *p less than 0.03. Checkered bars = classic telescoping technique; solid bars = modified telescoping technique.
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Fig 5. Severe and moderate airway instability rate is lower through the whole observation period when the modified telescoping technique is used. Statistical significance is reached only for the initial observation. *p less than 0.01. Checkered bars = classic telescoping technique; solid bars = modified telescoping technique.
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Fig 6. Devascularization in the initial observation (4 to 14 days after lung transplantation) shown as percentage of devascularized anastomotic circumference. The modified telescoping technique is associated with reduced devascularization (p = 0.039, overall). In the severe (80% to 100%, p < 0.043 single tailed) and moderate (50% to 70%) grades the modified technique shows lower rates of devascularization. The incidence of mild (20% to 40%) grades of devascularization is significantly higher (p = 0.006) using the modified technique. *p less than 0.05. Checkered bars = classic telescoping technique; solid bars = modified telescoping technique.
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By univariate analysis the use of cardiopulmonary bypass had no significant influence on anastomotic scoring for any variable. Overall stenosis score was significantly higher for left versus right side anastomoses for both transplant techniques at the late follow-up (p = 0.038), as previously described [12].
Survival
The modified telescoping technique was associate with a significant survival advantage (Fig 7)
when the overall population of 145 patients is considered, with the majority of the effect evident within the first year. The 1-year survival rate for the modified technique was 81% compared with 66% in the classic technique (p = 0.038). The survival advantage persists to 5 years (14.6% to 23%), with a trend toward further advantage at years 4 and 5 relative to a small difference at year 3. Similar results are seen when the analysis is restricted to 30- or 90-day survivors, for whom the trend approaches significance (p = 0.115 or p = 0.112 respectively at 5 years) or to the 118 patient population for which video airway follow-up was available (p = 0.300).
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Fig 7. Kaplan-Meier survival curves for the modified (n = 75) and classic (n = 70) telescoping technique for the first 5 years after transplantation. Survival is significantly improved in the modified telescoping group. (+ = censored.)
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To more directly assess the impact of anastomotic technique on survival a two-stage Cox proportional hazard model was applied to the 145 patient group and to the 118 patient subgroup to adjust for potentially confounding variables. In these models sex, age, preoperative steroids, CMV mismatch, single versus double lung transplant, cardiopulmonary bypass usage, and infection in the first 90 days were taken into account. Here the modified anastomotic technique had a significant influence in longer 5-year survival (p = 0.028). Among other variables examined lung infection (p = 0.01), particularly non-CMV viral infection (p = 0.022), was independently associated with a high mortality rate in both groups (Fig 8).
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Fig 8. Two-stage Cox proportional hazard model to analyze the influence of anastomotic technique and type of postoperative infection. In addition to infection in the first 90 days in 118 patients with completed airway follow-up, the analysis also took into account sex, age, preoperative steroids, cytomegalovirus (CMV) mismatch, single versus double lung transplantation, and cardiopulmonary bypass usage. Modified anastomotic technique was associated with better outcomes for each category of infection. Although infrequent, non-CMV viral infection was associated with poor outcome regardless of anastomotic technique. (Types of infection: heavy dashed line = none; dash-dotted line = Aspergillus; light dashed line = bacterial; solid line = viral.)
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To exclude possible confounding associations, multiple variables were evaluated by the Pearson test to assess statistical correlation with anastomotic technique. These variables include patient sex, age, preop steroid use, prednisone usage more than 10 mg/d, CMV mismatch or CMV infection, usage of cardiopulmonary bypass, rejection episodes in the first 90 days, ischemia time, side of transplant, and incidence of obliterative bronchiolitis. No association was demonstrable for any of these variables with respect to anastomotic technique.
No effect of airway score (stenosis, mucosal, malacia, and devascularization) on survival was found beyond that associated with anastomotic technique.
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Comment
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Historically bronchial healing was the principal obstacle to successful lung transplantation [13, 14]. Bronchial anastomotic techniques developed by Cooper and coworkers [15] using interrupted absorbable sutures and wrapping with a vascularized tissue pedicle reliably prevented dehiscence, a breakthrough crucial to development of the field. Over the last 2 decades surgical techniques and medical advances have evolved. Improved tissue preservation [16, 17] and steroid-sparing immunosuppressive regimens coupled with technical modifications such as trimming the donor bronchial stump close to the upper lobe takeoff were shown to be sufficiently reliable so that pedicle wrapping is no longer widely used [18–21].
Contemporary reports indicate that the technique of bronchial anastomosis is important to favorable patient outcomes and that a single optimal surgical strategy has not yet been defined [5, 8, 22, 23]. Using either intussuscepting or end-to-end techniques the reported incidence of major bronchial healing complications has fallen below 10%. However with each of these techniques problems with bronchial healing such as malacia, granulation tissue, or subcritical stenosis continue to occur. The classic intussuscepting technique leaves a rim of devascularized tissue within the lumen, which may contribute to secretion retention, invasive infection, or late stricture. End-to-end approximation with continuous suture addresses this problem. This surgical approach is simple but is exquisitely dependent on accurate suture placement and at least in principle seems vulnerable to leak, tissue strangulation, or stricture depending on suture tension.
Our modification of the classic interrupted intussuscepting technique derives from these considerations. Improved coaptation of the bronchial walls reduces the shelf of bronchial tissue that protrudes into the lumen of the airway and the associated "cul-de-sac." Accurate open placement of each suture and even distribution of tension along the wound represent advantages over a continuous suture. While the incidence of parenchymal infection did not differ between the classic and modified intussuscepted techniques used in this series, the improvement in survival with our modification suggests that infections were better tolerated, perhaps due to improved pulmonary toilet that might be expected in association with reduced stenosis and dynamic airway collapse. We speculate that the reduced incidence of structural airway weakness we observed may simply reflect improved mechanical buttressing of the recipient bronchus by closely apposed donor cartilage. Alternatively the mechanism may be improved wound vascularity and healing from close tissue apposition or reduced local infection and inflammation when no shelf is left.
More tedious approaches to achieve better bronchial healing have been proposed such as primary bronchial artery revascularization [22, 24]. This strategy is based on the hypothesis that bronchial wall ischemia contributes to poor early wound healing and perhaps even to later development of obliterative bronchiolitis [24, 25]. However there are no recent reports showing a consistent influence on rates of early airway complications or on the incidence of progression to obliterative bronchiolitis [10, 26]. Our approach adds no time or complexity to an interrupted open technique and was tested here in the context of a teaching program. The cost associated with routine use of eight to ten 4-0 monofilament absorbable sutures seems a reasonable trade-off for improved patient outcomes and a trend toward shorter hospital stay. Focal bronchial ischemia may occur within the figure-of-eight sutures. In theory this could contribute to the residual incidence of airway instability and stenosis associated we observed with the modified technique. Use of a interrupted simple sutures might avoid this, at the cost of increased anastomosis time and suture cost.
Several important limitations must be considered in evaluating the importance of our findings. Factors other than anastomotic technique may account for reduced complication rates and improved survival. Because bronchial anastomotic technique was directly associated with attending surgeon, differences in perioperative patient management or other surgeon-specific surgical factors may introduce sources of bias occult to our retrospective analysis. While medical strategies remained broadly constant over the decade of this study the lung transplant team composition and details of the therapeutic regimen evolved over time. If such differences exist they have eluded our efforts to identify them. Our analysis suggests that the population of recipients for whom the modified technique was used tended to be older, higher risk (IPF [idiopathic pulmonary fibrosis], PPH [primary pulmonary hypertension], CF [cystic fibrosis]), higher complexity (bilateral, cardiopulmonary bypass), and thus at higher risk of bronchial wound problems. Any bias introduced by our analytic approach would appear to favor the classic technique and diminish our ability to appreciate improved outcomes with the modified technique.
We conclude that the modified intussuscepting technique for bronchial anastomosis described here is associated with improvement in various indices of bronchial wound healing and with better survival after lung transplantation. We recommend this approach for consideration by other programs.
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Acknowledgments
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This study was supported by Vanderbilt University Transplant Center and the Department of Cardiothoracic Surgery. During the time of this study substantial salary and other administrative support was provided to various authors through grant mechanisms including the National Institutes of Health, the American Lung Association, the Deutsche Forschungsgemeinschaft (CS), Veterans Administration (Merit Review and PECASE), and the Vanderbilt General Clinical Research Center. We thank Daniel Byrne for his statistical analysis expertise. We thank the lung transplant personnel (Jan Muirhead, Lynn Lawrence, Jan Ebolum, Haley Hoy, and Marie Phelan) for their valuable assistance with data acquisition and recovery, and with expert patient care. Thanks also to the pulmonary medical attendings, fellows, and bronchoscopy staff who performed, recorded, and archived the bronchoscopic procedures.
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Abstract
Introduction
