2005;79:284-288 Ann Thorac SurgKatharina Schmid and Walter Klepetko

Shahrokh Taghavi, Gabriel M. Marta, Georg Lang, Gernot Seebacher, Gunther Winkler, for Prevention of Postpneumonectomy Bronchopleural Fistula

Bronchial Stump Coverage With a Pedicled Pericardial Flap: An Effective Method

http://ats.ctsnetjournals.org/cgi/content/full/79/1/284located on the World Wide Web at:

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Print ISSN: 0003-4975; eISSN: 1552-6259. Southern Thoracic Surgical Association. Copyright © 2005 by The Society of Thoracic Surgeons.

is the official journal of The Society of Thoracic Surgeons and theThe Annals of Thoracic Surgery

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ronchial Stump Coverage With a Pedicledericardial Flap: An Effective Method forrevention of Postpneumonectomy Bronchopleuralistula

hahrokh Taghavi, MD, Gabriel M. Marta, MD, Georg Lang, MD,ernot Seebacher, MD, Gunther Winkler, MD, Katharina Schmid, MD, andalter Klepetko, MD

epartment of Cardiothoracic Surgery and Clinical Institute of Pathology, Medical University of Vienna, Vienna, Austria

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Background. Bronchopleural fistula is a serious compli-ation after pneumonectomy. The aim of this retrospec-ive study was to investigate the efficacy of bronchialtump reinforcement with a pedicled flap of wholeericardium.Methods. The bronchial stump of 93 consecutive pa-

ients who underwent pneumonectomy between July988 and March 2003 was covered with a pedicled peri-ardial flap. Pneumonectomy was performed for primaryung cancer in 89.2% of patients. The study patientseceived concomitant extensive mediastinal lymphade-ectomy, resection of adjacent structures (aorta, venaava, thoracic wall), and neoadjuvant or planned adju-ant chemotherapy or radiotherapy, or both. Operativend perioperative complications were recorded, and pa-ients were followed up for a mean of 15 � 21.2 months

range, 9 to 126).

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urgery, Medical University of Vienna, Währinger Gürtel 18-20, A-1090ienna, Austria; e-mail: walter.klepetko@medunivie.ac.at.

2005 by The Society of Thoracic Surgeonsublished by Elsevier Inc

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Results. Perioperative mortality was 4.3% (n � 4; pul-onary embolism, sepsis, cardiac arrest, and sudden

eath in 1 patient each). Perioperative complicationsccurred in 2 patients: renal failure and hemiplegia in 1atient and cardiac tamponade in 1 patient. The latteromplication, caused by tight reconstruction of the peri-ardium, was directly related to the applied method andequired reoperation. No evidence of postpneumonec-omy bronchopleural fistula was observed periopera-ively and during the whole follow-up. One-year and-year survival was 65.7% and 44.8%, respectively.Conclusions. Bronchial stump reinforcement with a

ericardial flap is a highly effective method for prevent-ng postpneumonectomy bronchopleural fistula in se-ected patients.

(Ann Thorac Surg 2005;79:284–8)

© 2005 by The Society of Thoracic Surgeons

onectomy [6], and pericardiophrenic pedicles [5] have

mains the most serious complication after pneumo-

ectomy and occurs with an incidence of 0% to 12%Table 1). It leads to a number of life-threatening situa-ions, such as aspiration of infectious fluid from theleural cavity, pneumonia of the remaining lung, and

nfection of the pleural cavity followed by empyema.urgical technique is clearly related to its occurrence,nd different approaches with regard to the optimallosure of the bronchial stump have been described1–4]. Besides the different attempts to optimize theechnique of bronchial stump closure, it has been em-hasized that additional coverage with surrounding tis-ue might decrease the incidence of PBPF [3, 5]. However,t is still unclear whether reinforcement of the bronchialtump should be performed in every patient and, espe-ially, what is the particular value of flaps for preventionf PBPF. Different biological materials such as pleura [6],

ntercostal muscle [7], pericardial fat pad [5, 8], dia-hragm [9], vena azygos in case of a right-sided pneu-

ccepted for publication June 11, 2004.

ddress reprint requests to Dr Klepetko, Department of Cardiothoracic

een used for such a prophylactic coverage. Particularly,he use of the patient’s own pericardium has been thereferred method for bronchial stump coverage in ourepartment for many years.The aim of this retrospective study was therefore to

nalyze the resulting large series of patients and toescribe the efficacy of coverage of the bronchial stumpfter pneumonectomy with a pericardial flap for preven-ion of PBPF.

atients and Methods

total of 697 patients underwent pneumonectomy be-ween July 1988 and March 2003 at our department (381eft-side and 316 right-side pneumonectomies). Of these,atients were included in our study if they had a stan-ard resection procedure of the main bronchus, did notndergo concomitant pleuropericardophrenectomy, andhen the bronchial stump was covered with a pericardialap as described below. Additional resection proceduresesides the pneumonectomy such as resection of the

horacic wall or resection of the greater vessels did not

xclude patients from the study. Ninety-three patients

0003-4975/05/$30.00doi:10.1016/j.athoracsur.2004.06.108

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69 male, 24 female; mean age, 54.5 years) finally enteredhe analysis.

Indications for pneumonectomy were primary lungancer in 89.2% (n � 83), other malignancies in 5.4% (n �), and benign diseases in 5.4% (n � 5). Fifty-sevenatients (61.3%) underwent right side pneumonectomynd 36 patients (38.7%) underwent left side pneumonec-omy. Operative reports and postoperative courses withegard to major events and complications were recorded.nderlying histology, TNM stage for primary lung can-

ers, and preoperative or postoperative chemotherapy oradiation therapy, or both, was documented (Tables 2nd 3).Of the total of 93 patients, 69 (74.2%) received some

orm of additional therapy (irradiation or chemotherapy),ither alone or in various combinations. In 19 patients20.4%), preoperative neoadjuvant therapy was given; theemaining 50 patients (53.8%) had postoperative treat-ent with or without induction therapy. All patients

ischarged from hospital were seen in our outpatientepartment 1 month after surgery and thereafter twiceearly by the referring pulmologist. For this analysis,ffice records, written questionnaires, or direct telephone

able 1. Incidence of Postpneumonectomy Bronchopleuralistula (PBPF) According to Different Authors

uthor (Year) ReferenceNumber of

PatientsIncidence of

PBSF (%)

arsam (1989) 2 332 0samura (1992) 3 464 4.5eissberg (1992) 19 75 2.6

onlan (1995) 20 124 5l-Kattan (1995) 21 471 1.5right (1996) 1 256 3.1ollaus (1997) 22 797 12.0lepetko (1999) 15 129 0.8irbu (2001) 23 490 4.4avadpour (2003) 24 157 1.9

able 2. Indications for Pneumonectomy (n � 93) andnderlying Histology

iagnosis Histology

Patients

n %

ung cancer 83 89.2Squamous cell carcinoma 46 49.5Adenocarcinoma 28 30.1Small cell carcinoma 6 6.4Large cell carcinoma 3 3.2

ther malignancies 5 5.4Metastasis 2 2.2Lymphoma 2 2.2Malignant thymoma 1 1

enign diseases 5 5.4Bronchiectasis 2 2.2

eInfectious diseases 3 3.2

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ontact were employed. Follow-up ranged from 9 to 126onths (mean, 15 � 21.2) and was 97% complete (3

atients were lost to follow-up).

urgical TechniqueLOSURE OF THE BRONCHUS. Bronchial stump closure waserformed with commercial mechanical staplers (Ethiconnd Auto Suture) in all patients. Stapling was performedy approximation of the membranous and the cartilagi-ous portion of the bronchus, as suggested before [10].umor negativity of resection margins was ensured byistologic examination of frozen sections. The bronchialtump was then checked for air leakage with 30 cm H2Oustained airway pressure.YMPH NODE DISSECTION. In all patients with primary lungancer, a complete systematic mediastinal lymphadenec-omy was routinely added to the resection procedure.ypically, the subcarinal and tracheobronchial lymphodes were resected en bloc with the lung. This was

ollowed by complete dissection of the other remainingediastinal lymph node compartments.

DDITIONAL RESECTION PROCEDURES. In 14 patients (15%),dditional resection procedures were performed (aorta, n

5; superior vena cava, n � 3; thoracic wall, n � 6).esection of the aorta was performed with cardiopulmo-ary bypass, and details about these complex proceduresave been published elsewhere [11]. Reconstruction of

he thoracic wall was performed with polytetrafluoroeth-lene (Gore-Tex, W. L. Gore and Associates, Inc, Flag-taff, AZ).OVERAGE OF THE BRONCHUS. A generous flap of the antero-ateral pericardium, pedicled at its cranial part with orithout inclusion of the phrenic vessels and measuring

pproximately 4 � 12 cm, was prepared. This techniqueas applied regardless of whether the pericardium hadeen opened during the resection procedure. The flapas attached caplike over the bronchial stump withumerous single mattress stitches of 4-0 polydioxanon

PDS) (Johnson and Johnson Intl, Woluwe, Belgium) (Fig). In all patients, the resulting defect in the pericardiumas reconstructed with Vicryl mesh (Johnson and John-

on Intl, Brussels, Belgium).

esults

erioperative Periodedian hospital stay was 6 days (range, 3 to 65). Periop-

able 3. Tumor Stage Distribution in Patients With Primaryung Cancer (n � 83)

Tumor Stage

Patients (n � 83)

n %

8 9.6I 29 34.9IIa 27 32.6IIb 19 22.9

rative mortality was 4.3%; 4 patients died within 30 days

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286 TAGHAVI ET AL Ann Thorac SurgBRONCHIAL STUMP COVERAGE WITH PERICARDIAL FLAP 2005;79:284–8

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f surgery. The causes of death were pulmonary embo-ism, multiorgan failure due to sepsis, cardiac arrest, andudden death in 1 patient each.

Significant perioperative complications occurred in 2

ig 1. (A) A pedicled pericardial flap is attached, caplike, to a leftronchial stump with single mattress stitches of 4-0 polydioxanon.PP � pericardiophrenic patch; BS � bronchial stump; Es � esoph-gus.) (B) Schematic illustration of left mediastinum with pericar-iophrenic patch to cover left bronchial stump.

atients (2.2%). One patient had renal failure and hemi- f

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legia after additional resection of the aorta; the otheratient had cardiac tamponade due to tight reconstruc-

ion of the pericardium. That was the only patient with aomplication directly related to the method who requiredeoperation, and the problem of cardiac compression wasvercome by insertion of a larger Vicryl mesh. Postoper-tive recovery of this patient was uneventful.Supraventricular tachyarrhythmia occurred in 16 pa-

ients (17%), and was successfully managed pharmaco-ogically in all of them.

ong-Term Follow-Upixteen patients (17.2%) died within 6 months postoper-tively. In these patients, causes of death were infection43%), tumor progression (35%), and other causes (car-iovascular, renal, 22%). For the studied patients, sur-ival was 65.7% at 1 year, 44.8% at 2 years, and 23% at 3ears (Fig 2). In the long-term follow-up, the overwhelm-ng cause of death was tumor recurrence. No case ofBPF occurred during the entire outpatient follow-uperiod. Late empyema developed in 1 patient 2 monthsfter operation. No evidence of bronchopleural fistulaas detected at broncoscopy, and the patient was treatedith open window thoracostomy. In 2 patients, tumor

ecurrence was detected at the bronchial stump, which,owever, did not result in stump insufficiency. Neither of

hese 2 patients underwent reoperation, as other sys-emic metastases were present at the same time in both.

omment

ostpneumonectomy bronchial fistula remains one of theost serious complications after pneumonectomy, and

here is proven evidence that a number of patient-related

ig 2. Kaplan-Meier survival analysis of 93 patients who underwentneumonectomy and had bronchial stump coverage with a pericar-ial flap, between July 1988 and March 2003. Numbers in paren-heses represent patients at risk.

actors as well as factors related to the operative tech-

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287Ann Thorac Surg TAGHAVI ET AL2005;79:284–8 BRONCHIAL STUMP COVERAGE WITH PERICARDIAL FLAP

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ique are important for its development. In particular,atients undergoing pneumonectomy, who in additioneceive adjuvant or neoadjuvant therapies, do have alearly elevated risk [12]. The extent of the surgicalesection and the need for additional therapies are de-ermined by oncologic principles, however, and directnfluence on the prevention of PBPF can therefore be

ade only by the applied technique for closure andoverage of the bronchial stump.

A large number of publications have dealt with thisroblem in the past, and especially the need for bronchialtump coverage has been emphasized repeatedly [13, 14],lthough no prospective randomized trial on this ques-ion has ever been published.

Several years ago, we reviewed our personal experi-nce with routine coverage of the postpneumonectomytump with various tissues [15]. The flaps used includedleura, azygos vein, intercostal muscle, pericardial fatad, and pericardial flaps; and the overall reported

ncidence of PBPF was as low as 0.8%. Since then, ourreferred technique for bronchial stump coverage haseen the use of a pedicled pericardial flap, and theurpose of this paper is now to review the resultschieved with this particular technique in a much largerroup of patients.The use of a flap of pericardium in thoracic surgery was

rst described as an alternative method to the pericardialat graft by Brewer and associates [8] as early as 1953.nderson and Miller [5, 6] later on have used this

echnique in different clinical situations, such as repair ofracheoesophageal fistulas, sleeve lobectomies, trachealnastomosis, and extended pneumonectomies. Theresent paper represents the largest published series ofatients in whom pericardial flaps were used for cover-ge of postpneumonectomy stumps.Two different techniques have been applied in these

atients. In some of them, the bronchial stump wasovered with pedicled pericardium; in the remainingatients, a pericardial flap including the pericardio-hrenic vessels was used. At the beginning of our expe-ience, we used pericardiophrenic flaps only in thoseatients whose phrenic nerve had to be sacrificed forncologic reasons. Theoretically, phrenic nerve dysfunc-ion after pneumonectomy might have an impact on theunctional behavior of the contralateral diaphragm asell. However, no studies have investigated the func-

ional difference of a pneumonectomy with or withouthrenic nerve injury until now. If any difference could bexpected at all, this would be of importance only in thearly postoperative period, because later on the dia-hragm becomes completely fixed on the pneumonec-

omy side. In our initial series, no particular functionalisadvantage of the loss of the phrenic nerve after pneu-onectomy was observed, and therefore the phrenic

erve was sacrificed on purpose later on in a number ofatients to allow harvesting of a pedicled pericardio-hrenic flap, which owns the potential advantage of aetter blood supply.Attachment of the flaps to the bronchial stump was

erformed caplike with single stitches of 4-0 PDS, in a

ay that covered the stump completely, without neces- t

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arily decreasing its blood supply. Right-sided flaps usu-lly were brought into the thoracic cavity behind theuperior vena cava to avoid functional narrowing of theessel.In all patients, the resulting defect in the pericardiumas reconstructed with a Vicryl mesh [16], which was

ewn in to prevent herniation of the heart through theesulting defect. The potential side effects that can bexpected from such a procedure are arrhythmias in theostoperative period, infection of the foreign material,nd cardiac tamponade in case of tight reconstruction. Inhis series, these specific complications occurred at a lowate. The incidence of postoperative supraventricularachyarrhythmia was 17% (n � 16), which was within theange described in literature [17]. Intrathoracic infectionesulting in empyema was observed in 1 patient only,nd it must remain speculative whether this was relatedo the use of foreign material. The patient was treated byhoracic wall fenestration and the bronchial stump re-

ained closed during the whole treatment period. Evenore, in 5 additional patients with concomitant aortic

esection and prosthetic reconstruction, no infectiousomplication of the vascular graft occurred, possiblywing to the beneficial use of the pericardial flap [11].The only serious method-related complication that was

bserved in 1 patient was cardiac tamponade early afterhe operation. Tamponade was caused by tight recon-truction of the pericardium, which most likely waserformed during a temporary hypovolemic status. Dur-

ng postoperative normalization of the filling volume,ymptoms of tamponade occurred. The patient was takennto the operating room, and the Vicryl mesh was ex-hanged for a larger one, thereby overcoming allymptoms.

As mentioned before, controversy exists about theeed for and the benefit from coverage of the bronchialtump. Asamura [3] concluded in his review of more than,300 patients after lung resection that further investiga-ion should be performed to answer whether preventionf PBPF by tissue coverage is of benefit. Wright andolleagues [1] attributed the low incidence of 3.1% PBPFo their coverage technique in the discussion of theiresults with 256 patients after pneumonectomy, in whomhe bronchial stump was routinely covered with autolo-ous tissue. They used pleural flaps and pericardial fatad flaps in the vast majority of their patients. However,f the 8 cases of PBPF described by them, 3 had beenovered with pleura, 2 with omentum, 2 with pericardialat pad, and 1 with intercostal muscle. That gives evi-ence that none of the methods applied, not even the

echnique of omentum pull-up, can offer complete pro-ection against development of PBPF. Choice of theutologous tissue for coverage seems, therefore, to be ofrucial importance for optimal results. Pleural flaps,lthough being the most frequently used structure [6],sually have the disadvantage that they are extremely

hin and sometimes lack adequate blood supply. Inter-ostal muscle flaps have been used in some institutions7]. It was not reported that harvesting of this type of flapould result in any disadvantage. However, vasculariza-

ion at the end of operation sometimes can be poor,

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288 TAGHAVI ET AL Ann Thorac SurgBRONCHIAL STUMP COVERAGE WITH PERICARDIAL FLAP 2005;79:284–8

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espite careful dissection before introduction of the ribetractor. Mineo and coworkers [9] have reported excel-ent results with the use of a diaphragmatic flap toeinforce the bronchial stump after pneumonectomy.edicled omental flaps have widely been used for cover-ge of tracheobronchial defects and empyema [18]. Bothechniques have the disadvantage of extending the tho-acic operation into the abdomen.

The favorable results of the use of a pedicled flap ofericardium in our study and the low incidence ofpecific complications observed suggest that bronchialtump reinforcement with this technique is a highlyffective method for prevention of PBPF especially inatients at risk for bronchial healing problems.

ddendum

ince the submission of this manuscript, we have per-ormed a left pneumonectomy in a 61-year-old man, andhe bronchial stump was covered with a pedicled flap ofericardium. The postoperative course of the patient wasomplicated by pneumonia of the remaining lung, and heequired mechanical ventilation for a total of 8 weeks.ive weeks after pneumonectomy, broncoscopy revealedn opening of the bronchial stump, which was effectivelyrevented by the pericardial patch from communicatingith the thoracic cavity (Fig 3). Without further specific

reatment, the patient continued to improve and wasischarged from hospital. This experience underlines thefficacy of pericardial patch coverage to prevent a com-unication between the bronchial system and the tho-

acic cavity.

eferences

ig 3. Bronchoscopic view of a dehiscent bronchial stump, coveredy pericardial patch. The patch remains intact and prevents commu-ication of the bronchial system with the left thoracic cavity.

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2005;79:284-288 Ann Thorac SurgKatharina Schmid and Walter Klepetko

Shahrokh Taghavi, Gabriel M. Marta, Georg Lang, Gernot Seebacher, Gunther Winkler, for Prevention of Postpneumonectomy Bronchopleural Fistula

Bronchial Stump Coverage With a Pedicled Pericardial Flap: An Effective Method

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