Materials and Methods

Case selection—Medical records from the Matthew J. Ryan Veterinary Hospital of the University of Pennsylvania from July 2008 through April 2013 were reviewed. All cases were client-owned animals that underwent TAPS partial or complete lung lobectomy. Dogs and cats of any age, sex, and weight were included in the study if a TAPS lung lobectomy had been performed, a complete medical record was available for review, and short-term follow-up (6 months after surgery) was available.

Historical, laboratory, and imaging data—Data regarding history, patient signalment, clinical signs, and physical examination findings were recorded. All animals had a CBC, serum biochemical analysis, and blood typing performed prior to anesthesia. Preoperative thoracic imaging (thoracic radiography, CT, or both) was performed in all cases.

TAPS lung lobectomy technique—On the day of the procedure, patients were premedicated, anesthetized, and mechanically ventilated. Protocols for induction and maintenance of general anesthesia were determined at the discretion of the attending anesthesiologist, and varied among cases. One-lung ventilation was not implemented in any of the patients. At the time of surgery, all patients were administered perioperative antimicrobial prophylaxis (cefazolin sodium, 22 mg/kg [10 mg/lb, IV], given at anesthetic induction and then q 90 min intraoperatively). All surgical procedures were performed by the same board-certified surgeon (JJR). One of the authors (SS), a physician with a subspecialty in minimally invasive thoracic surgery and proficient in video-assisted thoracoscopic surgery in human patients, assisted in the first 2 cases. Patients were placed in lateral recumbency with the affected hemithorax uppermost. A 5- to 10-mm incision was made in the dorsal third of the thorax for initial entry into the thorax and thoracoscopic exploration with a 5-mm 30° rigid telescope.^a This initial telescope incision was typically made 5 to 7 intercostal spaces away from the center of the lesion to be removed. In general, the telescope port was placed in the caudal aspect of the hemithorax (9th to 12th intercostal spaces) for cranial lung lesions and in the cranial aspect of the hemithorax (4 to 6 intercostal spaces) for caudal lung lesions to facilitate visualization of the affected lung and exploration of the hemithorax. Following localization of the pulmonary lesion, a 2- to 7-cm minithoracotomy incision was made under direct thoracoscopic visualization (Figure 1). For cranial lung lobe lesions, the minithoracotomy was positioned 1 to 2 intercostal spaces (approx 3 to 5 cm) caudodorsal to the lesion. For caudal lung lobe lesions, the incision was positioned 1 to 2 intercostal spaces (3 to 5 cm) craniodorsal to the lesion. This positioning facilitated exteriorization of the affected lung lobe as well as easier access to the pulmonary hilus when necessary. In 10 of 11 patients, a 360° wound retraction device^b was placed in the minithoracotomy incision prior to exteriorization of the affected lung lobe to protect the incision and facilitate visualization (Figure 2). In 1 patient, a domestic shorthair cat, the wound retractor was too large and compressed the lungs in its immediate vicinity; therefore, it was removed prior to exteriorization of the lung. Partial (n = 5) or complete (6) lung lobectomy was performed with either a laparoscopic stapling device^c (6 cases) or a conventional open stapling device (30 to 3.5 mm; 5 cases).^d The intrathoracic lymph nodes were evaluated thoracoscopically in all patients, although nodal resection was not attempted in any case. The thorax was closed routinely with an interrupted appositional suture pattern and absorbable monofilament suture material. An indwelling thoracostomy tube was placed and secured by means of a Chinese finger trap suture.

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Intraoperative photograph of a 360° wound retraction device placed through a right minithoracotomy incision in a 7-year-old spayed female Bernese Mountain Dog with a right caudal lung lobe mass detected incidentally on thoracic radiography. Preoperative CT confirmed the presence of a 3-cm right caudal lung lobe mass. Pulmonary adenocarcinoma was diagnosed on subsequent histologic examination of tissue samples.

Citation: Journal of the American Veterinary Medical Association 245, 9; 10.2460/javma.245.9.1036

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Intraoperative photograph of the same patient as in Figure 1, with a 3 × 2-cm mass involving the peripheral aspect of the right caudal lung lobe. The mass is being exteriorized via the 360° wound retraction device. The pulmonary ligament has been transected with a bipolar vessel-sealing device.

Citation: Journal of the American Veterinary Medical Association 245, 9; 10.2460/javma.245.9.1036

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Results

Signalment—Eleven patients met the criteria for inclusion in the study. Three were domestic shorthair cats, and 8 were dogs (2 Labrador Retrievers, 1 Portuguese Water Dog, 1 Miniature Schnauzer, 1 Australian Shepherd, 1 Boxer, 1 English Setter, and 1 German Shepherd Dog). Of the 3 cats included in the study, 2 were neutered males and 1 was a spayed female. Of the 8 dogs, 4 were spayed females, 3 were castrated males, and 1 was a sexually intact male.

Preoperative data—Median age at the time of surgery was 11 years (range, 9 to 14 years). Median dog weight was 30.4 kg (66.9 lb; range, 9.9 to 48.3 kg [21.8 to 106.3 lb]), and median cat weight was 6.79 kg (14.9 lb; range, 6.1 to 8.2 kg [13.4 to 18.0 lb]). Most patients (8/11) were subclinically affected, and pulmonary disease was found incidentally on thoracic radiographs. In those patients (n = 3; 1 cat and 2 dogs) with clinical pulmonary disease, the most common clinical signs included coughing (2), increased respiratory noise (1), and restlessness (1), with 2 patients having more than 1 clinical sign (1 cat and 1 dog). None of the patients had clinically important abnormalities on preoperative clinicopathologic analyses.

All patients underwent preoperative thoracic radiography, and 10 of 11 patients underwent a preoperative CT scan for surgical planning. In all 11 patients, thoracic imaging revealed solitary pulmonary masses in the following locations: right cranial lobe (n = 1), right middle lobe (1), right caudal lobe (4), left cranial lobe (2), and left caudal lobe (3). Median size (largest dimension measured on CT [n = 10] or radiographs [1]) of the pulmonary masses was 4.7 cm (range, 2.9 to 11.4 cm). Nine of the 11 masses were classified as peripheral on the basis of their radiographic or CT appearance. No masses were localized to the pulmonary hilus. Of the 10 patients that had a thoracic CT scan, 5 had evidence of mild intrathoracic lymph node enlargement (sternal lymph nodes [n = 2], mediastinal lymph nodes [3], tracheobronchial lymph nodes [3]).

Operative data—Partial (n = 5) or complete (6) TAPS lung lobectomy was performed successfully in all patients. Telescope portals were placed in the following locations to allow for exploration of the affected hemithorax: fourth (n = 6), sixth (2), eighth (2), and ninth (1) intercostal spaces. Minithoracotomy incisions were positioned in the fourth (n = 2), fifth (1), sixth (5), seventh (1), eighth (1), and eleventh (1) intercostal spaces for exteriorization of the affected lung lobe. Median surgery time was 92.7 minutes (range, 77 to 150 minutes). Intraoperative hemorrhage was subjectively estimated to be minimal in all cases, and no intraoperative surgical complications necessitating conversion to open thoracotomy were encountered.

For 24 to 48 hours after surgery, all patients were maintained on IV analgesics including methadone (0.1 to 0.3 mg/kg [0.045 to 0.14 mg/lb], IV, q 4 h to q 6 h; 5 cases), hydromorphone (0.1 mg/kg, IV, q 4 h to q 6 h; 1 case), buprenorphine (0.01 to 0.02 mg/kg [0.005 to 0.009 mg/lb], IV, q 6 h to q 8 h, 2 cases), fentanyl (1 to 4 μg/kg/min [0.45 to 1.8 μg/lb/min]; 2 cases), and butorphanol (0.1 to 0.5 mg/kg/h [0.045 to 0.23 mg/lb/h]; 1 case). In 4 of 11 cases, postoperative analgesia was augmented by means of local infusion of bupivacaine (1.5 mg/kg [0.68 mg/lb] diluted 1:1 with sterile saline [0.9% NaCl] solution) administered via the thoracostomy tube every 6 to 8 hours for the first 24 hours following surgery. All patients had air and fluid removed through their chest tubes with a syringe every 2 to 4 hours or as indicated on the basis of clinical signs. Thoracostomy tubes were removed a median of 22.3 hours after surgery (range, 18 to 36 hours). Median time to discharge following surgery was 3.1 days (range, 1 to 6 days). Patients were discharged on a 5-day course of analgesic medication including tramadol (2 to 4 mg/kg [1.8 to 2.2 mg/lb], PO, q 8 h to q 12 h; 8 cases), carprofen (2.2 mg/kg, PO, q 12 h; 2 cases), and buprenorphine (0.01 to 0.02 mg/kg, PO, q 8 h to q 12 h; 2 cases). A return visit for reexamination 10 to 14 days after surgery was recommended. Further follow-up either at our hospital or with the primary care veterinarian was dependent on histopathologic findings and patient clinical status.

Histologic examination identified 7 primary pulmonary neoplasms, including adenocarcinoma (n = 3), bronchiolar alveolar carcinoma (1), adenosquamous carcinoma (1), and histiocytic sarcoma (2). There were 2 cases of benign pulmonary masses (an eosinophilic granuloma and adenomatous hyperplasia). Solitary metastatic lesions were diagnosed in the remaining 2 patients (metastatic osteosarcoma and metastatic carcinoma). For all cases, examination of the margins of surgical resection showed no evidence of neoplasia as determined by the reviewing pathologist.

Postoperative complications—In all but 1 patient, the postoperative duration of hospitalization was ≤ 4 days. One 11-year-old domestic shorthair cat was hospitalized for 6 days because it developed elevations in renal markers (BUN and creatinine concentrations) 1 day after surgery, which were thought at the time to be secondary to anesthesia-related acute renal injury. This cat required prolonged hospitalization for monitoring and IV fluid diuresis. At the time of discharge, the abnormal renal laboratory values had resolved. Minor postoperative complications (seroma at incision site [n = 1] and subcutaneous emphysema associated with the thoracostomy tube [2]) were seen in 3 patients and resolved with minimal intervention.

Follow-up—All patients were discharged from hospital, and 9 of 11 were alive 6 months after surgery based on client phone interviews or information from referring veterinarians. One patient (a 12-year-old female spayed domestic shorthair cat) died 5 days after surgery; gross necropsy examination revealed a marked amount of pleural effusion suggestive of congestive heart failure, and histologic evaluation confirmed cardiac abnormalities consistent with restrictive cardiomyopathy. At the time of TAPS in this patient, no obvious pericardial abnormalities or pleural effusion had been noted. Another patient (a 9-year-old castrated male Boxer) died acutely following a syncopal episode 2 months after surgery. A necropsy was not performed on this patient to determine the underlying cause of death.

Discussion

In the present study, partial or complete TAPS lung lobectomy was accomplished successfully in all 11 small animal patients over an approximately 5-year period (July 2008 through April 2013). Surgery time (median, 92.7 minutes; range, 77 to 150 minutes), duration of indwelling chest tube (median, 22.3 hours; range, 18 to 36 hours), and postoperative hospitalization time (median, 3.1 days; range, 1 to 6 days) were comparable to those reported for lateral thoracotomy in veterinary patients (cats and dogs) undergoing lung lobectomy.²⁰ This finding suggests that TAPS may be a viable alternative to traditional open lobectomy in select cases, especially when performed by experienced surgeons proficient in both open and thoracoscopic surgical techniques.

Thoracoscopic exploration of the affected hemithorax prior to partial or complete lung lobectomy was performed in all patients in this study, with visualization improved by the use of the 30° angled telescope. This allowed for intraoperative evaluation of the pleural surfaces, lymph nodes, diaphragm, and mediastinum for metastatic lesions or synchronous primary lesions as well as direct visualization for placement of thoracostomy tubes, in contrast to standard lateral thoracotomy, where visualization is typically limited to the affected lung lobe and the immediate area adjacent to the intercostal incision. Thoracoscopy may be a valuable tool for improving intrathoracic exploration and ruling out concurrent intrathoracic disease, particularly in patients that do not undergo preoperative advanced imaging (eg, CT or MRI) or those with lesions not directly visible via a standard open thoracotomy incision.

In most patients in this study, TAPS lobectomy was performed via small (< 3 cm) incisions without the need for mechanical rib spreading or retraction. Three patients required an incision larger than 3 cm because of the dimensions of the pulmonary mass to be resected. In the opinion of one of the authors (JJR), the small incisions combined with the lack of rib retraction resulted in good postoperative cosmesis and subjectively improved the postoperative comfort level when compared with patients undergoing traditional open thoracotomy for lung lobectomy. These benefits of minimally invasive thoracic surgery have been recognized in human patients.^1,3,6,7 In the patients in the present study, thoracoscopic instruments were introduced into the thoracic cavity without the use of rigid 5- or 11-mm instrument ports. It is our opinion that by avoiding the use of 11-mm rigid thoracoscopic ports,^e trauma to intercostal nerves, vasculature, and rib periosteum may have been reduced. However, additional studies are needed to objectively evaluate this. Additionally, inserting the telescope and instruments into the pleural space directly allowed for more dramatic instrument torque and mobility and reduced rib interference in certain positions. We have found that use of standard 11-mm thoracoscopic instrument ports^e when placed perpendicular to the rib axis may result in reduced ability to manipulate instruments. However, use of a rigid telescope without an associated cannula or port may also increase the likelihood of lens fogging and potential telescope damage. Therefore, caution and consideration must be exercised when this technique is used.

In 10 of 11 patients included in this study, a wound retraction device was used in conjunction with a minithoracotomy incision (Figures 1 and 2). When passed through the minithoracotomy, the wound retraction device radially distracted the incision 360° and provided static soft tissue retraction and protection without the need for bulky metal retractors or cumbersome laparotomy sponges. This wound retraction device enabled an excellent operative view similar to that achieved with the use of conventional rib spreaders but without the rigid forces they apply against the rib periosteum. The retraction device also assisted in exteriorization of the affected lung lobe, provided a smooth, clean working surface, and served as a barrier between the affected (diseased) lung tissue and the incision. Despite its thickness of only 0.08 mm, the sheath of the wound retractor is durable because of its polyurethane composition; in this group of patients, no tears or leaks were observed in the sheath of the retractor during its usage. Wound retractors have been implemented in human patients undergoing TAPS lobectomy. Previous studies^21–23 have shown that the device not only helps to protect intercostal nerves and muscles better than rib spreaders but appears to reduce the severity of intercostal pain after a minithoracotomy. In addition, the device has been found to decrease the incidence of postoperative surgical site infections.^24,25 It has further been proposed that it may help reduce the incidence of neoplastic disease recurrence when used in oncological surgery.^26,27 In 1 feline patient in the present study, the retraction device was not suitable and had to be removed prior to lung exteriorization. This was thought to be related to the size of the retractor relative to the patient or its positioning, which caused compression of the surrounding pulmonary tissue. The use of this wound retraction device was originally a modification of the existing video-assisted thoracoscopic surgery technique for lung lobectomy performed by one of the authors (SS) in human patients. This wound retractor was adapted for the TAPS technique because it was able to accommodate the differences in chest wall thickness between patients while maintaining intercostal retraction and protection during the entire procedure irrespective of the pulmonary mass size.

Lung lobectomy via minimally invasive approaches (total thoracoscopic, thoracoscopic assisted, and video assisted) is a standard-of-care procedure for resection of many primary lung tumors in human oncology patients.^1–8 The surgical technique used in this case series was adapted from techniques used in human patients under the guidance of one of the authors (SS). The TAPS technique incorporated minor modifications to the existing technique for treatment of human patients used by that author. The most notable modification, compared with existing techniques, was the addition of the wound retractor device. With regard to the feasibility and technical difficulty of the TAPS technique, direct guidance and assistance provided by the minimally invasive thoracic surgeon (SS) was available for the first 2 cases. It should be noted, however, that other authors of this study (DEH and JJR) were also proficient in both open and thoracoscopic surgery. It should be stressed that the outcomes reflected in this study may not represent what inexperienced surgeons may encounter in the early stages of their TAPS learning curve.

Importantly, our TAPS technique has several differences compared with other minimally invasive thoracic surgical approaches documented in the current veterinary literature.^15–19 In this series, all lung lobectomies were performed by means of extracorporeal stapling, rather than intracorporeal stapling as described in previous reports.^15,16,19 We believe that this is one of the major benefits of the TAPS procedure because it is comparatively less technically challenging and thus may be more feasible for most appropriately trained surgeons. Additionally, all lung lobectomies in this study were performed without implementation of 1-lung ventilation. We feel that this is another major advantage of the TAPS procedure, whereas 1-lung ventilation has been a necessity for other described minimally invasive lung lobectomy techniques and can be both technically challenging and time-consuming.^16,19

All patients in the present study had small lung lesions (median largest dimension measured on diagnostic imaging, 4.7 cm; range, 2.9 to 11.4 cm) and peripheral in nature, which made exteriorization and resection straightforward. We suggest that appropriate case selection is critical for surgical planning when determining whether patients are candidates for total thoracoscopic surgery, the TAPS approach, or open thoracotomy. For example, the TAPS technique may not be as applicable for patients with large pulmonary tumors (eg, largest dimension > 12 cm), where the thoracic incision required to remove the mass would be approximately the same length as required for an open thoracotomy. Thoracoscopic-assisted pulmonary surgery may also be more technically challenging for treatment of patients with tumors located near the pulmonary hilus given the increased difficulty with tumor exteriorization. It should be noted, however, that one of the authors (JJR) has recently used the described technique to successfully manage patients requiring resection of hilar masses. This does require that the minithoracotomy incision be placed in a slightly different location (ie, incision more dorsal) than it would be for more peripheral tumors (ie, incision centered over the hilus). The TAPS procedure can be more technically challenging in cats and toy to small-breed dogs (patients < 10 kg [22 lb]) because of the inherent working constraints of a small thorax. Thus, when selecting suitable cases early in the learning process, starting with medium- and large-breed dogs may be beneficial.

Nodal metastasis has been shown to be prognostically important in veterinary patients with pulmonary neoplasia.²⁸ Nodal resection was not attempted in any of the cases reported in this series owing to the low index of suspicion for nodal metastasis at the time of surgery. However, since the completion of the present study, when treating subsequent patients, we have successfully removed intrathoracic lymph nodes under thoracoscopic visualization during TAPS, and this is now standard practice at our hospital.

Limitations of the present study include its retrospective nature and the fact that the population evaluated was small and select. Thus, only speculations can be made regarding the overall usefulness of the procedure in the general companion animal patient population. In addition, all procedures were performed by a board-certified surgeon (JJR) experienced with minimally invasive surgical techniques. Thus, the procedure times and complication rates reported here should be interpreted cautiously. Future studies are needed to compare results from TAPS lobectomy with those for veterinary patients undergoing traditional open thoracotomy and other minimally invasive techniques. Ideally, these should be prospective studies and include evaluation of intra- and postoperative complication rates, duration of hospitalization, and postoperative pain scores. In addition, studies on long-term survival rate and disease recurrence in patients undergoing TAPS procedures are needed before conclusions regarding the success of this procedure for treatment of patients with specific diseases (eg, tumors) can be made. Studies focusing on more stringent case selection criteria for TAPS lobectomy in small animals would be useful.

This study demonstrated that the TAPS technique for partial and complete lung lobectomy was safe and feasible in select small animal patients when performed by surgeons proficient with both open and thoracoscopic surgery. When compared with total thoracoscopic surgery techniques, TAPS may offer a more technically feasible approach from both a surgical and anesthetic standpoint, because it provides the benefits of thoracic minimally invasive surgery without the necessity of 1-lung ventilation during anesthesia. Continual refinements in instrumentation and operative technique are needed before this will become a widely accepted approach to the treatment of thoracic disease.