Evaluation of Video‐Assisted Thoracic Surgery for Treatment of Spontaneous Pneumothorax and Pulmonary Bullae in Dogs J. Brad Case1, DVM, MS, Diplomate ACVS, Philipp D. Mayhew2, BVM&S, Diplomate ACVS, and Ameet Singh3, BSc, DVM, DVSc, Diplomate ACVS 1

Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, Florida ,2 Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California, Davis, California and 3 Ontario Veterinary College, University Guelph, Guelph, Ontario, Canada

Correspondence Author J. Brad Case, DVM, MS, Diplomate ACVS, Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32610. E‐mail: caseb@ufl.edu Submitted October 2013 Accepted July 2014 DOI:10.1111/j.1532-950X.2014.12288.x

Objective: To describe the operative findings and clinical outcome in dogs undergoing video‐assisted thoracic surgery (VATS) for treatment of spontaneous pneumothorax and pulmonary bullae. Study Design: Multi‐institutional retrospective case series. Animals: Dogs (n ¼ 12) with spontaneous pneumothorax and/or pulmonary bullae. Methods: Medical records (2008–2013) were reviewed for signalment, clinical signs, diagnostic imaging, surgical and histopathologic findings, and outcome in 12 dogs that had VATS for treatment of spontaneous pneumothorax and pulmonary bullae. In particular, conversion to median sternotomy and surgical success were evaluated. Results: Twelve dogs had initial VATS for spontaneous pneumothorax and/or pulmonary bullae. Conversion to median sternotomy because of inability to identify a parenchymal lesion/leak was necessary in 7 (58%) dogs. VATS without conversion to median sternotomy was performed in 6 (50%) dogs. Successful surgical outcomes occurred in 5 (83%) dogs that had conversion to median sternotomy, and in 3 (50%) dogs that had VATS without conversion to median sternotomy. Conclusions: Exploratory thoracoscopy was associated with a high rate of conversion to median sternotomy because of inability to identify leaking pulmonary lesions in dogs with spontaneous pneumothorax and pulmonary bullae. Failure to convert to a median sternotomy may be associated with recurrent or persistent pneumothorax.

Spontaneous pneumothorax is a relatively rare disease in dogs but is most commonly caused by ruptured subpleural blebs and emphysematous pulmonary bullae.1–6 From an anatomic diagnostic viewpoint, leaking blebs and bullae can be difficult to identify preoperatively, and even intraoperatively.1–8 Recently, computed tomography (CT) has been demonstrated to be of limited utility for lesion identification in dogs with spontaneous pneumothorax secondary to ruptured blebs and bullae.8 Because of the limitations of preoperative diagnostics, complete thoracic exploration by median sternotomy has been the recommendation of most surgeons.1–6 Because many dogs have multiple and bilateral lesions, access to both lungs is Dogs included in this study were evaluated and treated at the following institutions: The Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL, the Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California, Davis, CA, the Department of Clinical Studies‐Philadelphia, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA, and Ontario Veterinary College, University Guelph, Guelph, ON, Canada.

necessary.1–3 A video‐assisted thoracic surgery (VATS) approach performed in dorsal recumbency allows access to both hemithoraces for exploration and excision of affected lung tissue.9 Thoracoscopy has inherent advantages over conventional surgical techniques in reducing certain morbidities both in dogs and in people (e.g., less tissue injury, less pain, quicker recovery, reduced infection).10–13 However, when performed in dorsal recumbency, thoracoscopic exploration can be difficult, especially along the more dorsal parietal surfaces and hilar region of the lungs; specific lobes may be difficult to access (e.g., accessory lobe within the mediastinum and caudal lobes attached to the diaphragm via the pulmonary diaphragmatic ligament). Further, some affected dogs have narrow and deep chests, making thoracoscopic exploration of the hilar regions even more challenging. VATS is commonly performed for treatment of pulmonary bullae and spontaneous pneumothorax in people, but there is limited information on the efficacy of VATS for this application in dogs. However, preliminary reports in 13 and 39 dogs are supportive. Thus, our purposes were to (1) report the clinical and operative findings, and (2) surgical outcome in 12 dogs that had VATS for treatment of spontaneous pneumothorax and pulmonary bullae.

Veterinary Surgery 9999 (2014) 1–8 © Copyright 2014 by The American College of Veterinary Surgeons

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MATERIALS AND METHODS Dogs Dogs that had VATS for treatment of spontaneous pneumothorax and pulmonary bullae between 2008 and 2013 at 4 university small animal hospitals were included. Medical records were reviewed for signalment, clinical signs and results of preoperative diagnostics (complete blood count, serum biochemical profile, thoracic radiographs, and CT). The anesthetic and operative reports were retrospectively evaluated to determine patient position, thoracoscopic port type and location, initial and definitive surgical approach used, gross operative findings, surgical staplers used, surgical time, duration of thoracostomy tube placement, and complications encountered. The medical records and telephone communications with owners were used to document histopathologic diagnosis and clinical outcome. Anesthesia Anesthetic protocols were determined by the attending anesthesiologist and were similar for all dogs. Generally, dogs were premedicated with an opioid and induced using propofol and maintained on isoflurane in 100% oxygen. The method of intubation was either endotracheal or double lumen endobronchial according to surgeon preference.

Surgical Procedures and Findings All procedures were performed by Diplomates of the American College of Veterinary Surgeons with advanced training and experience with VATS. All port sites were infused with subcutaneous bupivacaine before port insertion. Dogs were initially positioned in dorsal recumbency with the 5.5 mm telescope port (Ternamian Endotip, Karl Storz Veterinary Endoscopy, Goleta, CA) placed in a subxyphoid, transdiaphragmatic position. Subsequent to placement of the initial instrument port, exploration of the right or left hemithorax was performed using a rigid telescope (5 mm diameter, 30° Hopkins II telescope, Karl Storz). Remaining ports (Thoracoport 5.5 or 11.5 mm, Covidien, Mansfield, MA) were placed at varying intercostal locations ranging from the 3rd–10th intercostal spaces according to surgeon preference and the location of the suspected and/or affected lobe(s). After placement of the 1st intercostal port, the mediastinum was fenestrated completely using a bipolar energy device (5 mm Blunt Tip LigaSureTM, Covidien) to allow for exploration of the contralateral hemithorax and for subsequent observed intercostal port placement. Fenestration of the mediastinum also facilitated instillation of saline in both hemithoraces for evaluation of pulmonary rupture. Observation of pleural surfaces was facilitated by tilting the dogs 15° to the right and left as well as by manipulation using a blunt probe and the angled view of the telescope. If a definitive lesion was not identified or if inability to resect the affected lobe was encountered, the surgical approach was converted to a median sternotomy or a miniature assisted

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intercostal thoracotomy, respectively. The owners of 1 dog would not allow conversion to median sternotomy despite the strong recommendation of the operating surgeon. Complete and partial lung lobectomy was accomplished using an articulated Endoscopic Stapler (Endo GIA 60 mm, Covidien) and/or a Thoracoabdominal Stapler (TA 55, TA 30, Covidien) depending on surgical approach and surgeon preference. Operative time was defined as the time interval between initial skin incision and complete closure of all surgical wounds. Duration of indwelling thoracostomy tube management was documented. Outcome Surgical outcome was defined as successful when dogs survived to discharge with no development, continuation, or recurrence of pneumothorax within 1 month of hospital discharge. If continuation or recurrence of pneumothorax was observed, the surgical outcome was defined as a failure. The probability of success based on definitive surgical approach was plotted using a product‐limit curve. Statistical Analysis Data were stored and analyzed using statistical software (JMP 9.0.2; SAS Institute © 2011, Cary, NC). Continuous data were reported as median and range. A product‐limit estimator was used to predict surgical success based on definitive surgical approach. The log rank test was used for comparison between groups. A P‐value of 2 cm (Fig. 3).19 Human surgeons have reported similar challenges in identifying visible air leakage in some cases of primary spontaneous pneumothorax. Pleural porosity, which results in air leakage from lung surfaces other than locations of gross emphysema, has been suggested as a possible cause.20 Consequently, ancillary procedures, such as apical pleurectomy, have been performed in cases with type I lesions (no obvious leak at time of VATS) with all cases having microscopic evidence of underlying pulmonary disease in 1 report.20 Type I lesions in people with spontaneous pneumothorax may be similar to 3 dogs in our report in which an active leak could not be identified during VATS or exploration via median sternotomy. All 3 dogs had bullous emphysema diagnosed on histopathology. Fluorescein‐enhanced autofluorescence thoracoscopy (FEAT) has been used to help identify pulmonary pathology in human spontaneous pneumothorax cases. After inhalation of fluorescein, patients had VATS and had significantly more

A: Thoracoscopic image of a bulla > 2 cm (type IV lesion) and (B) thoracoscopic image of a bleb (type III lesion).

Veterinary Surgery 9999 (2014) 1–8 © Copyright 2014 by The American College of Veterinary Surgeons

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abnormalities in regular white light compared with controls.21 While FEAT may also help improve detection of lesions during VATS in dogs with spontaneous pneumothorax, study in this area is required before it can be considered clinically. Although missed lesions are a likely explanation for the seemingly high failure rate in the dogs treated solely by VATS, it is also possible that staple failure may have occurred. Five dogs had partial or complete VATS stapled lung lobectomy and 2 developed persistent pneumothorax (dogs 11, 12) in the recovery period. Four of the 5 dogs were diagnosed with bullous or subpleural emphysema (dogs 2, 3, 9, 11) and dog 12 had bronchopneumonia. A necropsy was not performed in dog 11, so it is possible that staple failure could have caused the persistent leaking postoperatively; however, this is thought to be less likely given the success of previous reports using the same surgical staplers for lung lobectomy.22,23 Speculation in dog 12 is more difficult as many lobes had consolidation during thoracoscopy, and an obvious 1 cm defect was seen in the left caudal lobe, which was removed. Although this dog was likely septic (hypoglycemic, elevated total bilirubin) at the time of surgery and may have ruptured other necrotic foci within other lung lobes, pneumothorax persisted immediately after surgery, leaving open the potential of a missed leak or possible failure at the staple/tissue interface because of compromised tissue in the ligation. However, at necropsy, positive pressure ventilation of the lung fields did not show evidence of leakage from the staple line or any other lung lobes. We acknowledge several limitations, most notably small sample size, varying underlying disease processes, and patient population as well as surgeon and institution differences. However, we feel that potentially concerning results should be reported early, especially when newer treatments are being performed clinically,3,9 if for no other reason than to offer caution to surgeons considering a VATS approach in dogs with spontaneous pneumothorax. Whereas large‐scale retrospective and prospective controlled studies are a more reliable method to evaluate novel treatments, it may be difficult to justify this until a standardized and effective method of exploring the canine pleura is developed. We concluded that a VATS approach for the treatment of dogs with spontaneous pneumothorax appears to be associated with a high rate of conversion to median sternotomy and potential for surgical failure. If a VATS approach is to be used for spontaneous pneumothorax in dogs, the surgeon should be prepared to (1) convert to median sternotomy if the offending lesion or lesions is/are not identifiable and (2) anticipate the potential for surgical failure. Further study is required to determine whether benefits exist to using a VATS approach before planned median sternotomy in dogs with spontaneous pneumothorax.

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2. Holtsinger RH, Beale BS, Bellah JR, et al: Spontaneous pneumothorax in the dog: a retrospective analysis of 21 cases. J Am Anim Hosp Assoc 1993;29:195–210 3. Puerto DA, Brockman DJ, Lindquist C, et al: Surgical and nonsurgical management of and selected risk factors for spontaneous pneumothorax in dogs: 64 cases (1986–1999). J Am Vet Med Assoc 2002;220:1670–1674 4. Lipscomb VJ, Hardie RJ, Dubielzig RR: Spontaneous pneumothorax caused by pulmonary blebs and bullae in 12 dogs. J Am Anim Hosp Assoc 2003;39:435–445 5. Monnet E: Lungs, in veterinary surgery: small animal (Vol. 2). St. Louis, MO, Elsevier, 2003, pp 1758–1761 6. Monnet E: Surgical diseases of the lungs, in small animal soft tissue surgery. Ames, IA, Wiley‐Blackwell, 2013, pp 210–221 7. Au JJ, Weisman DL, Stefanacci JD, et al: Use of computed tomography for evaluation of lung lesions associated with spontaneous pneumothorax in dogs: 12 cases (1999–2002). J Am Vet Med Assoc 2006;228:733–737 8. Reetz JA, Caceres AV, Suran JN, et al: Sensitivity, positive predictive value, and interobserver variability of computed tomography in the diagnosis of bullae associated with spontaneous pneumothorax in dogs: 19 cases (2003–2012). J Am Vet Med Assoc 2013;243:244–251 9. Brissot HN, Dupre GP, Bouvy BM, et al: Thoracoscopic treatment of bullous emphysema in 3 dogs. Vet Surg 2003;32:524–529 10. Walsh PJ, Remedios AM, Ferguson JF, et al: Thoracoscopic versus open partial pericardectomy in dogs: comparison of postoperative pain and morbidity. Vet Surg 1999;28:472–479 11. Mayhew PD, Freeman L, Kwan T, et al: Comparison of surgical site infection rates in clean and clean‐contaminated wounds in dogs and cats after minimally invasive versus open surgery: 179 cases (2007–2008). J Am Vet Med Assoc 2012;240:193–198 12. Villamizar NR, Darrabie MD, Burfeind WR, et al: Thoracoscopic lobectomy is associated with lower morbidity compared with thoracotomy. J Thorac Cardiovasc Surg 2009;138:419–425 13. Rueth NM, Andrade RS: Is VATS lobectomy better: perioperatively, biologically and oncologically? Ann Thorac Surg 2010;89:S2107–S2111 14. Case JB, Maxwell M, Aman A, et al: Outcome evaluation of a thoracoscopic pericardial window procedure or subtotal pericardectomy via thoracotomy for the treatment of pericardial effusion in dogs. J Am Vet Med Assoc 2013;242:493–498 15. Gossot D, Galetta D, Stern JB, et al: Results of thoracoscopic pleural abrasion for primary spontaneous pneumothorax. Surg Endosc 2004;18:466–471 16. Henry M, Arnold T, Harvey J: BTS guidelines for the management of spontaneous pneumothorax. Thorax 2003;58:ii39–ii52 17. Jerram RM, Fossum TW, Berridge BR, et al: The efficacy of mechanical abrasion and talc slurry as methods of pleurodesis in normal dogs. Vet Surg 1999;28:322–332 18. Merbl Y, Kelmer E, Shipov A, et al: Resolution of persistent pneumothorax by use of blood pleurodesis in a dog after surgical correction of a diaphragmatic hernia. J Am Vet Med Assoc 2010;237:299–303 19. Vanderschueren RGJRA: The role of thoracoscopy in the evaluation and management of pneumothorax. Lung 1990;168:1122–1125

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20. Ayed AK, Chandrasekaran C, Sukumar M: Video‐assisted thoracoscopic surgery for primary spontaneous pneumothorax: clinicopathological correlation. Eur J Cardiothorac Surg 2006;29:221–225 21. Noppen M, Dekeukeleire T, Hanon S, et al: Fluorescein‐enhanced autofluorescence thoracoscopy in patients with primary spontaneous pneumothorax and normal subjects. Am J Respir Crit Care Med 2006;174:26–30

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22. Mayhew PD, Hunt GB, Steffey MA, et al: Evaluation of short‐ term outcome after lung lobectomy for resection of primary lung tumors via video‐assisted thoracoscopic surgery or open thoracotomy in medium‐ to large‐breed dogs. J Am Vet Med Assoc 2013;243:681–688 23. Lansdowne JL, Monnet E, Twedt DC, et al: Thoracoscopic lung lobectomy for treatment of lung tumors in dogs. Vet Surg 2005;34:530–535

Veterinary Surgery 9999 (2014) 1–8 © Copyright 2014 by The American College of Veterinary Surgeons

Evaluation of Video-Assisted Thoracic Surgery for Treatment of Spontaneous Pneumothorax and Pulmonary Bullae in Dogs.

To describe the operative findings and clinical outcome in dogs undergoing video-assisted thoracic surgery (VATS) for treatment of spontaneous pneumot...
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