- Email: [email protected]
A Stepwise Approach for Postlobectomy Bronchopleural Fistula
ARTICLE IN PRESS Thoracic
A Stepwise Approach for Postlobectomy Bronchopleural Fistula Andrei Y. Gritsiuta, MD Takashi Eguchi, MD, PhD David R. Jones, MD and Gaetano Rocco, MD, FRCSEd Although rare, bronchopleural fistula (BPF) following anatomic lung resection is a serious complication associated with high rates of mortality (25%-71%). Risk factors for BPF include surgical approach, neoadjuvant therapy, diabetes mellitus, and chronic obstructive pulmonary disease. As neoadjuvant treatment is increasingly being administered to patients with locally advanced lung cancer, and as more patients are being diagnosed with lung cancer at an older age—elderly patients present with a higher index of multiple comorbidities—the incidence of BPF among patients undergoing anatomic resection for lung cancer is expected to increase. In this manuscript, we detail risk factors and considerations for BPF and describe a stepwise approach to treat BPF following lobectomy for lung cancer. Operative Techniques in Thoracic and Cardiovasculary Surgery 00:1 20 Ó 2019 Published by Elsevier Inc. KEYWORDS Bronchopleural fistula, Lobectomy, Vacuum-assisted closure (VAC), Lung cancer
Introduction ronchopleural fistula (BPF)—defined as an abnormal communication between the pleural cavity and bronchial tree—after anatomic lung resection is associated with high rates of mortality (25%-71%).1-5 BPF has been reported to occur after 0.1% of segmentectomies, 0.2%-3% of lobectomies, and 0.9%-6.8% of pneumonectomies.4-6 Right-side pneumonectomy, right lower lobectomy, and right middlelower bilobectomy in particular have been associated with increased risk of BPF, owing to anatomic factors inherent to the procedures.7 At present, lobectomy is the most commonly used surgical approach for patients with lung cancer and is associated with the most favorable outcomes.8 Surgical factors associated with postoperative development of BPF include ischemia of the bronchial stump due to extensive dissection,2 inappropriate apposition of the bronchial mucosa, and excessive length of the bronchial stump due to stagnation of bronchial secretions and bacterial contamination.9 Nonsurgical risk factors associated with postoperative BPF include neoadjuvant therapy, diabetes mellitus, and chronic obstructive pulmonary disease.7,10-12 Given the increasing use of neoadjuvant chemotherapy or chemoradiotherapy for patients with locally advanced lung cancer and the increasing number of elderly patients with lung cancer, who have higher rates of multiple comorbidities,13 the
B
Thoracic Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY Address reprint requests to Gaetano Rocco, MD, FRCSEd, Thoracic Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York, NY 10065. E-mail: [email protected] 1522-2942/$ see front matter © 2019 Published by Elsevier Inc. https://doi.org/10.1053/j.optechstcvs.2019.11.005
incidence of BPF among patients undergoing lung resection is expected to increase. The presence of a fistula leads to bacterial and/or fungal contamination of residual pleural space, which leads to lung expansion failure as well as recurrent pneumonia of the healthy contralateral lung due to aspiration of infected pleural fluid. In general, the management of BPF is based on control of the infection and closure of the fistula. The principal components of treatment include (1) initial chest tube drainage, (2) administration of intravenous antibiotics, (3) optimization of nutrition, (4) surgical or endoscopic closure of the fistula, and (5) obliteration of the residual infected space. To decrease further complications, the chest drainage typically serves as the initial procedure after patient admission. However, in the case of chronic empyema or calcified parietal pleura, this step can be very challenging. The final decision about strategy should be made on the basis of the CT scans. In our opinion, OWT should be performed as soon as possible once the diagnosis of pleural empyema with BPF has been made. Endoscopic interventions can speed up spontaneous closure of a BPF, especially after lobectomy.14 Several therapeutic options to close the fistula have been proposed, such as fibrin glues 3 and Amplatzer double-disk occlusion (ASO; AGA Medical Corp., Plymouth, MN) 15,16; however, in cases of large (ie, >5 mm) or chronic (refractory) BPF, no approach has proven to be as effective as a surgical stepwise traetment.17 Surgical closure of BPF is successful in 80%-95% of cases.17 In most cases, treatment is conducted in 2 or 3 steps. Clagget and Geraci first described a 2-stage treatment approach: open drainage of the pleural cavity and subsequent obliteration of the fistula by use of an antibiotics solution.18 Pairolero and colleagues added to 1
2
ARTICLE IN PRESS
this method, covering the occluded bronchus stump by transposition of a muscle flap, and observed a success rate of 86%.19 The use of vacuum-assisted closure (VAC) therapy creates negative pressure in the pleural cavity and leads to the rapid formation of granulation tissue, reduction of bacterial load, removal of excess interstitial fluid, improvement in tissue oxygenation, and decrease in residual pleural space volume. Accumulated experience indicates that vacuum therapy holds promise for the treatment of BPF after lobectomy as it accelerates the phases of the wound-healing process and reduces the length of hospitalization.20-22 Properly applied VAC therapy has been demonstrated to be a highly beneficial and safe procedure. The main disadvantages of pain syndrome and sponge adherence to the cavity have been described. Hemodynamic complications, injury of mediastinal structures, bleeding, and arrhythmia are avoided as low
A.Y. Gritsiuta et al.
negative pressure (up to 125 mm Hg) is applied to the postlobectomy pleural space, with viable lung parenchyma serving as a buffer. The sponge can be easily changed at the bedside every 3-4 days. Herein, to address the pressing need for appropriate management of BPF after lobectomy, we illustrate a step-wise surgical approach to treat BPF, highlighting the technical details with representative figures and pictures. This approach begins with a computed tomography scan with contrast, with the addition of 3-D modeling if available (Fig. 1). Next, an open-window thoracostomy is performed, with rib resection, followed by debridement, antiseptic washing and drying, and marsupialization (Figs. 2-4). Following control of the infection, VAC therapy can be administered (Fig. 5). Finally, thoracomyoplasty is performed by transposition of the latissimus dorsi muscle (Figs. 6-9).
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
3
Figure 1 BPF after right lower lobectomy (RLL). Computed tomography with contrast, with 3-D reconstruction if available, is helpful to determine the exact location of the empyema cavity and fistula and to assess the relationships of the bronchial and vessel stumps.
4
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 2 Skin incision and rib resection sites for open-window thoracostomy. To facilitate effective drainage of the infected pleural cavity, to be able to change the dressing through the window, and to avoid self-closure due to the scarring process, a wide open thoracostomy is recommended. An Hshaped incision of soft tissue is made at the bottom of the empyema cavity, and 1 to 2 ribs are resected for a length of 10-15 cm. The latissimus dorsi and pectoralis major muscles are identified and spared. In contrast to BPF after pneumonectomy, in which the incision should be as posterior and rostral as possible, after lobectomy, preoperative planning with 3-D CT modeling is critical for performance of OWT. The incision should be made in the middle of the postlobectomy residual pleural space. Since BPF after lower lobectomy and bilobectomy is the most common presentation, we demonstrate an operative technique in this situation: in the majority of cases, the incision should be performed in the fourth or fifth intercostal space, centered on the middle axillary line. This incision allows for the performance of effective drainage and dressing of the empyema cavity after lower lobectomy/bilobectomy. However, the exact location can vary depending on the location of the cavity on CT scan. In the case of empyema after upper lobectomy, OWT placement should be moved up to the 2nd or 3rd intercostal space, with muscle sparing. We do not recommend the use of the VATS approach, since CT with contrast provides sufficient data about the location of the residual pleural space and the presence of BPF makes this step unnecessary.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
5
Figure 3 Debridement (A) and marsupialization (B) following open-window thoracostomy and rib resection. Whether to use a previous thoracotomy or not depends on the localization of the empyema cavity on CT scan. (A) Once the chest is entered, the pleural cavity is deeply cleaned and debrided, with visualization of the BPF. The suction and ring clamps are used to drain the cavity and remove fibrinous and purulent material, blood clots, etc. Parietal pleura in this area is removed by the curette, and the empyema cortex is carefully excised on the lung side, with special attention to vessel stumps. Additionally, the pleural cavity is washed with antiseptics and dried. The most common complication of this step is prolonged air leak from the lung parenchyma, which can be easily managed with open dressings. . The ends of the resected ribs are covered with a periosteum with sutures. (B) The skin-musculofascial edges of the operative wound are invaginated, and the edges of the skin are fixed around the perimeter, with interrupted sutures, to the periosteum and the parietal pleura. It is necessary to achieve careful adaptation of the edges of the skin and subperiosteal-pleural flaps.
6
ARTICLE IN PRESS
Figure 3 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 4 Open-window thoracostomy 1 month after the procedure.
7
8
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 5 Open-window thoracotomy before (A) and after (B) VAC placement. After formation of healthy granulation tissue following control of infection, VAC therapy can be applied. (A) A VAC sponge is inserted through the open-window thoracostomy to fill the entire empyema cavity. Vacuum drainage should be constant and gentle: 75 mm Hg at initiation, with a gradual increase in pressure as indicated. We do not recommend the placement of any material under the sponge, since low negative pressure is safe for lobar hilum vessel and it can influence the efficacy of the procedure. In contrast to postpneumonectomy BPF, after lobectomy, the smaller bronchial fistula allows for the achievement of a sufficient suction rate, and chances for spontaneous closure are high. Dressing changes are performed every 3-4 days, with microbiological evaluation. VAC therapy may be discontinued when a wound swab shows no further bacterial colonization and obliteration of the pleural cavity can be performed.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 5 Continued
9
10
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 6 Thoracomyoplasty by transposition of the latissimus dorsi muscle. (A) The vascular anatomy, with the standard incision indicated, and (B) the topographic anatomy of the thoracodorsal artery and serratus branch are shown. (A) The incision is marked, extending from the axilla or the posterior axillary fold and then inferiorly and medially over the latissimus muscle. The thoracodorsal artery should be identified and preserved. (B) Care should also be taken to avoid injury to the serratus branch of the thoracodorsal artery to the serratus muscle, in case the branch is needed for a vascular pedicle. This large vessel is the first visible branch of the thoracodorsal artery. The serratus branch is traced in the proximal direction to the place of branching from the thoracodorsal artery—the vascular pedicle. In addition, the thoracodorsal artery can be detected quite easily by palpation under the proximal edge of the muscle. The second branch of the thoracodorsal artery, going to the corner of the scapula, is found opposite the serratus branch. Depending on the required length of the vascular pedicle, it is isolated up to the circumflex scapular artery. Proximal dissection of the vascular pedicle is facilitated if the skin incision is extended to the armpit.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 6 Continued
11
12
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 7 Mobilization of the latissimus dorsi muscle by dissecting the muscle posteriorly and inferiorly and dividing the muscle origin. Following medial and inferior release, dissection proceeds underneath the muscle toward the axilla. (A, B) The muscle harvest is complete, and the pedicle remains attached. Quite often, it is mistaken for the thoracodorsal artery; take its branch to the serratus muscle. Do not cut it until the thoracodorsal artery is clearly defined. In some cases, the serratus branch can be used as a vascular pedicle at the intersection of the thoracodorsal artery before branching. If additional muscle bulk is needed to reach the thoracic cavity, the muscle flap is separated from all points of bone fixation. In the region of the humeral bone, the flap is mobilized to the insertion tendon of the muscle and divided. However, in the case of the postlobectomy pleural space, this maneuver is usually unnecessary due to its small size.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 7 Continued
13
14
ARTICLE IN PRESS
Figure 7 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
15
Figure 8 (A) Liquidation of the fistula with (C) obliteration of residual pleural space. The muscle flap moves to the chest through the excised portion (4 cm) of the third or fourth rib. The mobilized flap of the latissimus dorsi muscle is able to fill the postlobectomy cavity. (B) The distal portion of the muscle flap is attached to the bronchial stump area. It is anchored to all 4 aspects of the bronchial stump using 4 horizontal mattress absorbable sutures. If the latissimus dorsi muscle was damaged previously, alternative tissue flaps are used: serratus anterior muscle, pectoralis major muscle, or greater omentum.
16
ARTICLE IN PRESS
Figure 8 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
17
Figure 9 (A) The serratus anterior muscle has blood supply from the thoracodorsal vessels, which makes it possible to widely mobilize the entire flap. Secondary blood supply occurs through the lateral thoracic artery, which supplies only a limited portion. Full muscle mobilization leads to the formation of a flap, which is comparable in volume to the latissimus dorsi muscle, which can be moved to the axial residual pleural space. Due to common blood supply, the latissimus dorsi and serratus anterior muscles can be rotated as a single unit onto the thoracodorsal artery as a vascular pedicle. (B) The pectoralis major muscle flap has good mobility using the thoracoacromial artery and mainly serves to obliterate the apical pleural space. When using perforating vessels of the internal thoracic and anterior intercostal arteries, the mobility of the flap decreases sharply. (C) The greater omentum is mobilized with preservation of the right gastroepiploic artery, which ensures the viability of the flap and moves into the chest through the foramina of Morgagni. The distal portion of the omental flap is formed in the region of its maximum width in order to ensure maximum contact area with the BPS region. The flap is fixed directly to the bronchus stump by U-shaped sutures and is additionally strengthened along the periphery with separate interrupted sutures.
18
ARTICLE IN PRESS
Figure 9 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 9 Continued
19
20
ARTICLE IN PRESS
Conclusion The use of a stepwise approach to surgically treat BPF after lobectomy for lung cancer has been shown to be safe and is associated with good outcomes. The addition of VAC to the previously described approaches holds promise for achieving even better results, with decreased morbidity and shorter hospital stay. The steps described above should be planned appropriately to ensure optimal treatment outcomes in patients experiencing BPF after undergoing lobectomy for lung cancer.
Declaration of Competing Interest David R. Jones serves as a senior medical advisor for Diffusion Pharmaceuticals and a consultant for Merck and AstraZeneca. Gaetano Rocco has financial relationships with Baxter, Scanlan, and Medtronic. The other authors have nothing to disclose.
8.
9.
10.
11.
12.
13.
14.
Supplementary materials Supplementary material associated with this article can be found in the online version at doi:10.1053/j.optechstcvs.2019.11.005.
15.
16.
References 1. Shekar K, Foot C, Fraser J, et al: Bronchopleural fistula: an update for intensivists. J Crit Care 25:47–55, 2010 2. Benhamed L, Bellier J, Fournier C, et al: Postoperative ischemic bronchitis after lymph node dissection and primary lung cancer resection. Ann Thorac Surg 91:355–359, 2011 3. Nagahiro I, Aoe M, Sano Y, et al: Bronchopleural fistula after lobectomy for lung cancer. Asian Cardiovasc Thorac Ann 15:45–48, 2007 4. Sirbu H, Busch T, Aleksic I, et al: Bronchopleural fistula in the surgery of non-small cell lung cancer: incidence, risk factors, and management. Ann Thorac Cardiovasc Surg 7:330–336, 2001 5. Sonobe M, Nakagawa M, Ichinose M, et al: Analysis of risk factors in bronchopleural fistula after pulmonary resection for primary lung cancer. Eur J Cardio-Thorac Surg 18:519–523, 2000 6. Vallieres E: Management of empyema after lung resections (pneumonectomy/lobectomy). Chest Surg Clin N Am 12:571–585, 2002 7. Li S, Fan J, Zhou J, et al: Residual disease at the bronchial stump is positively associated with the risk of bronchoplerual fistula in patients
17.
18. 19.
20.
21.
22.
A.Y. Gritsiuta et al.
undergoing lung cancer surgery: a meta-analysis. Interact Cardiovasc Thorac Surg 22:327–335, 2016 Dai C, Shen J, Ren Y, et al: Choice of surgical procedure for patients with non-small-cell lung cancer 1 to 2 cm among lobectomy, segmentectomy, and wedge resection: a population-based study. J Clin Oncol 34:3175–3182, 2016 Okuda M, Go T, Yokomise H: Risk factor of bronchopleural fistula after general thoracic surgery: review article. Gen Thorac Cardiovasc Surg 65:679–685, 2017 Li S, Fan J, Liu J, et al: Neoadjuvant therapy and risk of bronchopleural fistula after lung cancer surgery: a systematic meta-analysis of 14 912 patients. Jpn J Clin Oncol 46:534–546, 2016 Li SJ, Fan J, Zhou J, et al: Diabetes mellitus and risk of bronchopleural fistula after pulmonary resections: a meta-analysis. Ann Thorac Surg 102:328–339, 2016 Li SJ, Zhou XD, Huang J, et al: A systematic review and meta-analysisdoes chronic obstructive pulmonary disease predispose to bronchopleural fistula formation in patients undergoing lung cancer surgery? JThorac Dis 8:1625–1638, 2016 Eguchi T, Bains S, Lee MC, et al: Impact of increasing age on causespecific mortality and morbidity in patients with stage I non-small-cell lung cancer: a competing risks analysis. J Clin Oncol 35:281–290, 2017 Naranjo Gomez JM, Carbajo Carbajo M, Valdivia Concha D, Campo-Canaveral de la Cruz JL: Conservative treatment of post-lobectomy bronchopleural fistula. Interact Cardiovasc Thorac Surg 15:152–154, 2012 Takanami I: Closure of a bronchopleural fistula using a fibrin-glue coated collagen patch. Interact Cardiovasc Thorac Surg 2:387–388, 2003 Klotz LV, Gesierich W, Schott-Hildebrand S, et al: Endobronchial closure of bronchopleural fistula using Amplatzer device. J Thorac Dis 7:1478–1482, 2015 Massera F, Robustellini M, Della Pona C, et al: Open window thoracostomy for pleural empyema complicating partial lung resection. Ann Thorac Surg 87:869–873, 2009 Clagett OT, Geraci JE: A procedure for the management of postpneumonectomy empyema. J Thorac Cardiovasc Surg 45:141–145, 1963 Pairolero PC, Arnold PG, Trastek VF, et al: Postpneumonectomy empyema. The role of intrathoracic muscle transposition. J Thorac Cardiovasc Surg 99:958–966, 1990. discussion 966-958 Passera E, Guanella G, Meroni A, et al: Amplatzer device and vacuumassisted closure therapy to treat a thoracic empyema with bronchopleural fistula. Ann Thorac Surg 92:e23–e25, 2011 Rocco G, Cecere C, La Rocca A, et al: Caveats in using vacuum-assisted closure for post-pneumonectomy empyema. Eur J Cardio-Thorac Surg 41:1069–1071, 2012 Saadi A, Perentes JY, Gonzalez M, et al: Vacuum-assisted closure device: a useful tool in the management of severe intrathoracic infections. Ann Thorac Surg 91:1582–1589, 2011
A Stepwise Approach for Postlobectomy Bronchopleural Fistula Andrei Y. Gritsiuta, MD Takashi Eguchi, MD, PhD David R. Jones, MD and Gaetano Rocco, MD, FRCSEd Although rare, bronchopleural fistula (BPF) following anatomic lung resection is a serious complication associated with high rates of mortality (25%-71%). Risk factors for BPF include surgical approach, neoadjuvant therapy, diabetes mellitus, and chronic obstructive pulmonary disease. As neoadjuvant treatment is increasingly being administered to patients with locally advanced lung cancer, and as more patients are being diagnosed with lung cancer at an older age—elderly patients present with a higher index of multiple comorbidities—the incidence of BPF among patients undergoing anatomic resection for lung cancer is expected to increase. In this manuscript, we detail risk factors and considerations for BPF and describe a stepwise approach to treat BPF following lobectomy for lung cancer. Operative Techniques in Thoracic and Cardiovasculary Surgery 00:1 20 Ó 2019 Published by Elsevier Inc. KEYWORDS Bronchopleural fistula, Lobectomy, Vacuum-assisted closure (VAC), Lung cancer
Introduction ronchopleural fistula (BPF)—defined as an abnormal communication between the pleural cavity and bronchial tree—after anatomic lung resection is associated with high rates of mortality (25%-71%).1-5 BPF has been reported to occur after 0.1% of segmentectomies, 0.2%-3% of lobectomies, and 0.9%-6.8% of pneumonectomies.4-6 Right-side pneumonectomy, right lower lobectomy, and right middlelower bilobectomy in particular have been associated with increased risk of BPF, owing to anatomic factors inherent to the procedures.7 At present, lobectomy is the most commonly used surgical approach for patients with lung cancer and is associated with the most favorable outcomes.8 Surgical factors associated with postoperative development of BPF include ischemia of the bronchial stump due to extensive dissection,2 inappropriate apposition of the bronchial mucosa, and excessive length of the bronchial stump due to stagnation of bronchial secretions and bacterial contamination.9 Nonsurgical risk factors associated with postoperative BPF include neoadjuvant therapy, diabetes mellitus, and chronic obstructive pulmonary disease.7,10-12 Given the increasing use of neoadjuvant chemotherapy or chemoradiotherapy for patients with locally advanced lung cancer and the increasing number of elderly patients with lung cancer, who have higher rates of multiple comorbidities,13 the
B
Thoracic Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, New York, NY Address reprint requests to Gaetano Rocco, MD, FRCSEd, Thoracic Service, Department of Surgery, Memorial Sloan Kettering Cancer Center, 1275 York Avenue, New York, NY 10065. E-mail: [email protected] 1522-2942/$ see front matter © 2019 Published by Elsevier Inc. https://doi.org/10.1053/j.optechstcvs.2019.11.005
incidence of BPF among patients undergoing lung resection is expected to increase. The presence of a fistula leads to bacterial and/or fungal contamination of residual pleural space, which leads to lung expansion failure as well as recurrent pneumonia of the healthy contralateral lung due to aspiration of infected pleural fluid. In general, the management of BPF is based on control of the infection and closure of the fistula. The principal components of treatment include (1) initial chest tube drainage, (2) administration of intravenous antibiotics, (3) optimization of nutrition, (4) surgical or endoscopic closure of the fistula, and (5) obliteration of the residual infected space. To decrease further complications, the chest drainage typically serves as the initial procedure after patient admission. However, in the case of chronic empyema or calcified parietal pleura, this step can be very challenging. The final decision about strategy should be made on the basis of the CT scans. In our opinion, OWT should be performed as soon as possible once the diagnosis of pleural empyema with BPF has been made. Endoscopic interventions can speed up spontaneous closure of a BPF, especially after lobectomy.14 Several therapeutic options to close the fistula have been proposed, such as fibrin glues 3 and Amplatzer double-disk occlusion (ASO; AGA Medical Corp., Plymouth, MN) 15,16; however, in cases of large (ie, >5 mm) or chronic (refractory) BPF, no approach has proven to be as effective as a surgical stepwise traetment.17 Surgical closure of BPF is successful in 80%-95% of cases.17 In most cases, treatment is conducted in 2 or 3 steps. Clagget and Geraci first described a 2-stage treatment approach: open drainage of the pleural cavity and subsequent obliteration of the fistula by use of an antibiotics solution.18 Pairolero and colleagues added to 1
2
ARTICLE IN PRESS
this method, covering the occluded bronchus stump by transposition of a muscle flap, and observed a success rate of 86%.19 The use of vacuum-assisted closure (VAC) therapy creates negative pressure in the pleural cavity and leads to the rapid formation of granulation tissue, reduction of bacterial load, removal of excess interstitial fluid, improvement in tissue oxygenation, and decrease in residual pleural space volume. Accumulated experience indicates that vacuum therapy holds promise for the treatment of BPF after lobectomy as it accelerates the phases of the wound-healing process and reduces the length of hospitalization.20-22 Properly applied VAC therapy has been demonstrated to be a highly beneficial and safe procedure. The main disadvantages of pain syndrome and sponge adherence to the cavity have been described. Hemodynamic complications, injury of mediastinal structures, bleeding, and arrhythmia are avoided as low
A.Y. Gritsiuta et al.
negative pressure (up to 125 mm Hg) is applied to the postlobectomy pleural space, with viable lung parenchyma serving as a buffer. The sponge can be easily changed at the bedside every 3-4 days. Herein, to address the pressing need for appropriate management of BPF after lobectomy, we illustrate a step-wise surgical approach to treat BPF, highlighting the technical details with representative figures and pictures. This approach begins with a computed tomography scan with contrast, with the addition of 3-D modeling if available (Fig. 1). Next, an open-window thoracostomy is performed, with rib resection, followed by debridement, antiseptic washing and drying, and marsupialization (Figs. 2-4). Following control of the infection, VAC therapy can be administered (Fig. 5). Finally, thoracomyoplasty is performed by transposition of the latissimus dorsi muscle (Figs. 6-9).
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
3
Figure 1 BPF after right lower lobectomy (RLL). Computed tomography with contrast, with 3-D reconstruction if available, is helpful to determine the exact location of the empyema cavity and fistula and to assess the relationships of the bronchial and vessel stumps.
4
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 2 Skin incision and rib resection sites for open-window thoracostomy. To facilitate effective drainage of the infected pleural cavity, to be able to change the dressing through the window, and to avoid self-closure due to the scarring process, a wide open thoracostomy is recommended. An Hshaped incision of soft tissue is made at the bottom of the empyema cavity, and 1 to 2 ribs are resected for a length of 10-15 cm. The latissimus dorsi and pectoralis major muscles are identified and spared. In contrast to BPF after pneumonectomy, in which the incision should be as posterior and rostral as possible, after lobectomy, preoperative planning with 3-D CT modeling is critical for performance of OWT. The incision should be made in the middle of the postlobectomy residual pleural space. Since BPF after lower lobectomy and bilobectomy is the most common presentation, we demonstrate an operative technique in this situation: in the majority of cases, the incision should be performed in the fourth or fifth intercostal space, centered on the middle axillary line. This incision allows for the performance of effective drainage and dressing of the empyema cavity after lower lobectomy/bilobectomy. However, the exact location can vary depending on the location of the cavity on CT scan. In the case of empyema after upper lobectomy, OWT placement should be moved up to the 2nd or 3rd intercostal space, with muscle sparing. We do not recommend the use of the VATS approach, since CT with contrast provides sufficient data about the location of the residual pleural space and the presence of BPF makes this step unnecessary.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
5
Figure 3 Debridement (A) and marsupialization (B) following open-window thoracostomy and rib resection. Whether to use a previous thoracotomy or not depends on the localization of the empyema cavity on CT scan. (A) Once the chest is entered, the pleural cavity is deeply cleaned and debrided, with visualization of the BPF. The suction and ring clamps are used to drain the cavity and remove fibrinous and purulent material, blood clots, etc. Parietal pleura in this area is removed by the curette, and the empyema cortex is carefully excised on the lung side, with special attention to vessel stumps. Additionally, the pleural cavity is washed with antiseptics and dried. The most common complication of this step is prolonged air leak from the lung parenchyma, which can be easily managed with open dressings. . The ends of the resected ribs are covered with a periosteum with sutures. (B) The skin-musculofascial edges of the operative wound are invaginated, and the edges of the skin are fixed around the perimeter, with interrupted sutures, to the periosteum and the parietal pleura. It is necessary to achieve careful adaptation of the edges of the skin and subperiosteal-pleural flaps.
6
ARTICLE IN PRESS
Figure 3 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 4 Open-window thoracostomy 1 month after the procedure.
7
8
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 5 Open-window thoracotomy before (A) and after (B) VAC placement. After formation of healthy granulation tissue following control of infection, VAC therapy can be applied. (A) A VAC sponge is inserted through the open-window thoracostomy to fill the entire empyema cavity. Vacuum drainage should be constant and gentle: 75 mm Hg at initiation, with a gradual increase in pressure as indicated. We do not recommend the placement of any material under the sponge, since low negative pressure is safe for lobar hilum vessel and it can influence the efficacy of the procedure. In contrast to postpneumonectomy BPF, after lobectomy, the smaller bronchial fistula allows for the achievement of a sufficient suction rate, and chances for spontaneous closure are high. Dressing changes are performed every 3-4 days, with microbiological evaluation. VAC therapy may be discontinued when a wound swab shows no further bacterial colonization and obliteration of the pleural cavity can be performed.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 5 Continued
9
10
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 6 Thoracomyoplasty by transposition of the latissimus dorsi muscle. (A) The vascular anatomy, with the standard incision indicated, and (B) the topographic anatomy of the thoracodorsal artery and serratus branch are shown. (A) The incision is marked, extending from the axilla or the posterior axillary fold and then inferiorly and medially over the latissimus muscle. The thoracodorsal artery should be identified and preserved. (B) Care should also be taken to avoid injury to the serratus branch of the thoracodorsal artery to the serratus muscle, in case the branch is needed for a vascular pedicle. This large vessel is the first visible branch of the thoracodorsal artery. The serratus branch is traced in the proximal direction to the place of branching from the thoracodorsal artery—the vascular pedicle. In addition, the thoracodorsal artery can be detected quite easily by palpation under the proximal edge of the muscle. The second branch of the thoracodorsal artery, going to the corner of the scapula, is found opposite the serratus branch. Depending on the required length of the vascular pedicle, it is isolated up to the circumflex scapular artery. Proximal dissection of the vascular pedicle is facilitated if the skin incision is extended to the armpit.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 6 Continued
11
12
ARTICLE IN PRESS
A.Y. Gritsiuta et al.
Figure 7 Mobilization of the latissimus dorsi muscle by dissecting the muscle posteriorly and inferiorly and dividing the muscle origin. Following medial and inferior release, dissection proceeds underneath the muscle toward the axilla. (A, B) The muscle harvest is complete, and the pedicle remains attached. Quite often, it is mistaken for the thoracodorsal artery; take its branch to the serratus muscle. Do not cut it until the thoracodorsal artery is clearly defined. In some cases, the serratus branch can be used as a vascular pedicle at the intersection of the thoracodorsal artery before branching. If additional muscle bulk is needed to reach the thoracic cavity, the muscle flap is separated from all points of bone fixation. In the region of the humeral bone, the flap is mobilized to the insertion tendon of the muscle and divided. However, in the case of the postlobectomy pleural space, this maneuver is usually unnecessary due to its small size.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 7 Continued
13
14
ARTICLE IN PRESS
Figure 7 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
15
Figure 8 (A) Liquidation of the fistula with (C) obliteration of residual pleural space. The muscle flap moves to the chest through the excised portion (4 cm) of the third or fourth rib. The mobilized flap of the latissimus dorsi muscle is able to fill the postlobectomy cavity. (B) The distal portion of the muscle flap is attached to the bronchial stump area. It is anchored to all 4 aspects of the bronchial stump using 4 horizontal mattress absorbable sutures. If the latissimus dorsi muscle was damaged previously, alternative tissue flaps are used: serratus anterior muscle, pectoralis major muscle, or greater omentum.
16
ARTICLE IN PRESS
Figure 8 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
17
Figure 9 (A) The serratus anterior muscle has blood supply from the thoracodorsal vessels, which makes it possible to widely mobilize the entire flap. Secondary blood supply occurs through the lateral thoracic artery, which supplies only a limited portion. Full muscle mobilization leads to the formation of a flap, which is comparable in volume to the latissimus dorsi muscle, which can be moved to the axial residual pleural space. Due to common blood supply, the latissimus dorsi and serratus anterior muscles can be rotated as a single unit onto the thoracodorsal artery as a vascular pedicle. (B) The pectoralis major muscle flap has good mobility using the thoracoacromial artery and mainly serves to obliterate the apical pleural space. When using perforating vessels of the internal thoracic and anterior intercostal arteries, the mobility of the flap decreases sharply. (C) The greater omentum is mobilized with preservation of the right gastroepiploic artery, which ensures the viability of the flap and moves into the chest through the foramina of Morgagni. The distal portion of the omental flap is formed in the region of its maximum width in order to ensure maximum contact area with the BPS region. The flap is fixed directly to the bronchus stump by U-shaped sutures and is additionally strengthened along the periphery with separate interrupted sutures.
18
ARTICLE IN PRESS
Figure 9 Continued
A.Y. Gritsiuta et al.
ARTICLE IN PRESS
Approach for Postlobectomy Bronchopleural Fistula
Figure 9 Continued
19
20
ARTICLE IN PRESS
Conclusion The use of a stepwise approach to surgically treat BPF after lobectomy for lung cancer has been shown to be safe and is associated with good outcomes. The addition of VAC to the previously described approaches holds promise for achieving even better results, with decreased morbidity and shorter hospital stay. The steps described above should be planned appropriately to ensure optimal treatment outcomes in patients experiencing BPF after undergoing lobectomy for lung cancer.
Declaration of Competing Interest David R. Jones serves as a senior medical advisor for Diffusion Pharmaceuticals and a consultant for Merck and AstraZeneca. Gaetano Rocco has financial relationships with Baxter, Scanlan, and Medtronic. The other authors have nothing to disclose.
8.
9.
10.
11.
12.
13.
14.
Supplementary materials Supplementary material associated with this article can be found in the online version at doi:10.1053/j.optechstcvs.2019.11.005.
15.
16.
References 1. Shekar K, Foot C, Fraser J, et al: Bronchopleural fistula: an update for intensivists. J Crit Care 25:47–55, 2010 2. Benhamed L, Bellier J, Fournier C, et al: Postoperative ischemic bronchitis after lymph node dissection and primary lung cancer resection. Ann Thorac Surg 91:355–359, 2011 3. Nagahiro I, Aoe M, Sano Y, et al: Bronchopleural fistula after lobectomy for lung cancer. Asian Cardiovasc Thorac Ann 15:45–48, 2007 4. Sirbu H, Busch T, Aleksic I, et al: Bronchopleural fistula in the surgery of non-small cell lung cancer: incidence, risk factors, and management. Ann Thorac Cardiovasc Surg 7:330–336, 2001 5. Sonobe M, Nakagawa M, Ichinose M, et al: Analysis of risk factors in bronchopleural fistula after pulmonary resection for primary lung cancer. Eur J Cardio-Thorac Surg 18:519–523, 2000 6. Vallieres E: Management of empyema after lung resections (pneumonectomy/lobectomy). Chest Surg Clin N Am 12:571–585, 2002 7. Li S, Fan J, Zhou J, et al: Residual disease at the bronchial stump is positively associated with the risk of bronchoplerual fistula in patients
17.
18. 19.
20.
21.
22.
A.Y. Gritsiuta et al.
undergoing lung cancer surgery: a meta-analysis. Interact Cardiovasc Thorac Surg 22:327–335, 2016 Dai C, Shen J, Ren Y, et al: Choice of surgical procedure for patients with non-small-cell lung cancer 1 to 2 cm among lobectomy, segmentectomy, and wedge resection: a population-based study. J Clin Oncol 34:3175–3182, 2016 Okuda M, Go T, Yokomise H: Risk factor of bronchopleural fistula after general thoracic surgery: review article. Gen Thorac Cardiovasc Surg 65:679–685, 2017 Li S, Fan J, Liu J, et al: Neoadjuvant therapy and risk of bronchopleural fistula after lung cancer surgery: a systematic meta-analysis of 14 912 patients. Jpn J Clin Oncol 46:534–546, 2016 Li SJ, Fan J, Zhou J, et al: Diabetes mellitus and risk of bronchopleural fistula after pulmonary resections: a meta-analysis. Ann Thorac Surg 102:328–339, 2016 Li SJ, Zhou XD, Huang J, et al: A systematic review and meta-analysisdoes chronic obstructive pulmonary disease predispose to bronchopleural fistula formation in patients undergoing lung cancer surgery? JThorac Dis 8:1625–1638, 2016 Eguchi T, Bains S, Lee MC, et al: Impact of increasing age on causespecific mortality and morbidity in patients with stage I non-small-cell lung cancer: a competing risks analysis. J Clin Oncol 35:281–290, 2017 Naranjo Gomez JM, Carbajo Carbajo M, Valdivia Concha D, Campo-Canaveral de la Cruz JL: Conservative treatment of post-lobectomy bronchopleural fistula. Interact Cardiovasc Thorac Surg 15:152–154, 2012 Takanami I: Closure of a bronchopleural fistula using a fibrin-glue coated collagen patch. Interact Cardiovasc Thorac Surg 2:387–388, 2003 Klotz LV, Gesierich W, Schott-Hildebrand S, et al: Endobronchial closure of bronchopleural fistula using Amplatzer device. J Thorac Dis 7:1478–1482, 2015 Massera F, Robustellini M, Della Pona C, et al: Open window thoracostomy for pleural empyema complicating partial lung resection. Ann Thorac Surg 87:869–873, 2009 Clagett OT, Geraci JE: A procedure for the management of postpneumonectomy empyema. J Thorac Cardiovasc Surg 45:141–145, 1963 Pairolero PC, Arnold PG, Trastek VF, et al: Postpneumonectomy empyema. The role of intrathoracic muscle transposition. J Thorac Cardiovasc Surg 99:958–966, 1990. discussion 966-958 Passera E, Guanella G, Meroni A, et al: Amplatzer device and vacuumassisted closure therapy to treat a thoracic empyema with bronchopleural fistula. Ann Thorac Surg 92:e23–e25, 2011 Rocco G, Cecere C, La Rocca A, et al: Caveats in using vacuum-assisted closure for post-pneumonectomy empyema. Eur J Cardio-Thorac Surg 41:1069–1071, 2012 Saadi A, Perentes JY, Gonzalez M, et al: Vacuum-assisted closure device: a useful tool in the management of severe intrathoracic infections. Ann Thorac Surg 91:1582–1589, 2011