Video-assisted extirpation of cranial mediastinal masses in dogs: 18 cases (2009–2014)

Melissa A. MacIver Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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J. Brad Case Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Eric L. Monnet Department of Clinical Sciences, College of Veterinary Medicine, Colorado State University, Fort Collins, CO 80523.

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Geraldine B. Hunt Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Philipp D. Mayhew Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Michelle L. Oblak Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada.

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Jeffrey J. Runge Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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Ameet Singh Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 2W1, Canada.

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Daniel D. Smeak Department of Clinical Sciences, College of Veterinary Medicine, Colorado State University, Fort Collins, CO 80523.

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Michele A. Steffey Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Sarah E. Boston Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Abstract

OBJECTIVE To characterize clinical findings, surgical procedures, complications, and outcomes in dogs undergoing extirpation of masses from the cranial mediastinum via video-assisted thoracic surgery (VATS) and establish preliminary guidelines for case selection when considering VATS for thymectomy in dogs.

DESIGN Retrospective case series.

ANIMALS 18 client-owned dogs that underwent extirpation of a cranial mediastinal mass by means of VATS at 5 academic referral hospitals from 2009 through 2014.

PROCEDURES Medical records were reviewed and data extracted regarding signalment, clinical signs, physical examination findings, diagnostic imaging results, surgical approach and duration, cytologic and histologic examination results, complications, outcome, and cause of death, when applicable.

RESULTS 16 dogs had a thymoma, 1 had thymic anaplastic carcinoma, and 1 had hemangiosarcoma. Seven had both megaesophagus and myasthenia gravis. Median approximate tumor volume was 113.1 cm3 (interquartile range, 33.5 to 313.3 cm3). Median duration of VATS was 117.5 minutes (interquartile range, 91.5 to 136.3 minutes). Conversion to an open thoracic surgical procedure was required for 2 dogs, 1 of which died during surgery. Median survival time following VATS for dogs with thymoma and concurrent myasthenia gravis and megaesophagus was 20 days. Dogs with thymoma without paraneoplastic syndrome survived for ≥ 60 days, and none of these dogs died of disease-related causes.

CONCLUSIONS AND CLINICAL RELEVANCE VATS appeared to be an acceptable approach for extirpation of masses from the cranial mediastinum in dogs under certain conditions. Dogs with myasthenia gravis and megaesophagus had a poor postoperative outcome.

Abstract

OBJECTIVE To characterize clinical findings, surgical procedures, complications, and outcomes in dogs undergoing extirpation of masses from the cranial mediastinum via video-assisted thoracic surgery (VATS) and establish preliminary guidelines for case selection when considering VATS for thymectomy in dogs.

DESIGN Retrospective case series.

ANIMALS 18 client-owned dogs that underwent extirpation of a cranial mediastinal mass by means of VATS at 5 academic referral hospitals from 2009 through 2014.

PROCEDURES Medical records were reviewed and data extracted regarding signalment, clinical signs, physical examination findings, diagnostic imaging results, surgical approach and duration, cytologic and histologic examination results, complications, outcome, and cause of death, when applicable.

RESULTS 16 dogs had a thymoma, 1 had thymic anaplastic carcinoma, and 1 had hemangiosarcoma. Seven had both megaesophagus and myasthenia gravis. Median approximate tumor volume was 113.1 cm3 (interquartile range, 33.5 to 313.3 cm3). Median duration of VATS was 117.5 minutes (interquartile range, 91.5 to 136.3 minutes). Conversion to an open thoracic surgical procedure was required for 2 dogs, 1 of which died during surgery. Median survival time following VATS for dogs with thymoma and concurrent myasthenia gravis and megaesophagus was 20 days. Dogs with thymoma without paraneoplastic syndrome survived for ≥ 60 days, and none of these dogs died of disease-related causes.

CONCLUSIONS AND CLINICAL RELEVANCE VATS appeared to be an acceptable approach for extirpation of masses from the cranial mediastinum in dogs under certain conditions. Dogs with myasthenia gravis and megaesophagus had a poor postoperative outcome.

Neoplasia of the cranial mediastinum is rare in dogs, but when observed, thymoma is the most common diagnosis.1,2 The recommended treatment for neoplasia in this particular region is mass extirpation via intercostal thoracotomy or median sternotomy.1,3,4 A video-assisted technique for CMM excision in dogs (n = 2) has been reported.5 In human medicine, VATS is an established technique for the removal or biopsy of mediastinal masses in adults and pediatric patients.6,7 However, some surgeons are hesitant to use a VATS approach unless masses are of a certain size because of concerns of complete resectability.8

Humans undergoing VATS thymectomy have less thoracic drainage, less pain, and shorter hospital stays than those undergoing thoracotomy.6 In dogs, VATS pericardectomy has been associated with similar reductions in pain and rapid return to function.9 Consequently, several reports9–15 have been published describing techniques and outcomes in dogs undergoing VATS for various conditions. The objective of the study reported here was to characterize clinical and surgical findings, complications, and outcome in dogs undergoing CMM extirpation by means of VATS. A secondary objective was to develop preliminary guidelines for case selection when considering a VATS approach to CMM extirpation in dogs.

Materials and Methods

Case selection criteria

All dogs that had undergone CMM extirpation from 2009 through 2014 at 5 veterinary academic referral hospitals were eligible for inclusion in the study. Dogs for which intercostal thoracotomy or median sternotomy had been performed were included only if a VATS procedure was initially attempted for CMM removal and conversion to an open thoracic surgical procedure was required.

Medical records review

Information was collected from the medical records regarding dog signalment; clinical history; clinical signs at hospital admission; physical examination findings; whether myasthenia gravis was present before or after CMM extirpation; CBC, serum biochemical, and urinalysis results; anti-ACHR antibody titer; response to IV edrophonium chloridea administration; diagnostic imaging findings (radiography, ultrasonography, CT, or MRI); surgery date; anesthesia protocol; intubation method (endotracheal or endobronchial); whether 1-lung ventilation was performed; surgical findings; ports and patient positioning; concurrent procedures; tumor size; duration of surgery; intraoperative complications; duration of indwelling thoracic drainage; postoperative complications; cytologic and histologic examination results; tumor margins; tumor stage; adjuvant treatment; date of hospital discharge; date of last followup; and date and cause of death (if applicable).

Duration of surgery was defined as the interval from first skin incision to placement of the last suture. Tumor stage was determined as described elsewhere.16 Presence and extent of paraneoplastic syndromes were classified as no evidence of paraneoplastic syndrome, myasthenia gravis, or nonthymic malignant tumor. Presence or absence of myasthenia gravis was recorded on the basis of clinical signs and either the anti-ACHR antibody titer or response to edrophonium chloridea administration.

For tumor size values, approximate tumor volume was calculated on the basis of the volume of a sphere (4/3πr3) because use of 3-D imaging varied among dogs and was not performed for some dogs. Computed tomographic measurements were preferred over radiographic measurements when available. Tumor radius was calculated as half of the largest diameter measured on imaging.

With regard to outcomes, major intraoperative complications were defined as any complication resulting in death or emergent conversion to an open thoracic surgical procedure. Major postoperative complications included aspiration pneumonia and any complication resulting in patient death or the need for another surgery. Minor postoperative complications were defined as any adverse event that was self-limiting or resolved with medical treatment. Final diagnosis was determined by histologic examination of the mass by a board-certified pathologist. Follow-up information was obtained via recheck appointment or telephone interview with the referring veterinarian or dog owner. Survival time was defined as the interval between the date of surgery and date of last follow-up or death. Dogs that died or were euthanized within 1 month (30 days) after surgery were defined as having died of disease-related causes in situations in which a specific cause of death could not be determined.

Statistical analysis

Statistical softwareb was used for all calculations. Continuous data are reported as median (IQR). A product limit (Kaplan-Meier) curve was generated to determine short-term survival rate in dogs in which the CMM was determined to be a thymoma. The log-rank method was used to compare survival time between dogs with myasthenia gravis and megaesophagus and dogs without these diseases. Values of P < 0.05 were considered significant.

Results

Animals

Eighteen dogs (9 castrated males, 8 spayed females, and 1 sexually intact female) met the inclusion criteria for the study. Median age was 10.9 years (IQR, 10.2 to 12.0 years). Median body weight was 29.6 kg (65.1 lb; IQR, 21.3 to 32.6 kg [46.9 to 71.7 lb]). Breeds included Golden Retriever (n = 3), Beagle (3), mixed (3), Labrador Retriever (2), Border Collie (2), pit bull type (2), Australian Cattle Dog (1), Alaskan Malamute (1), and Chesapeake Bay Retriever (1).

Clinical signs and physical examination

At hospital admission, 3 dogs had signs of lethargy, 2 had collapse, 4 had weakness, and 2 had exercise intolerance. Four dogs had dyspnea, 3 had persistent panting, and 5 had coughing. Other clinical signs included ptyalism (n = 5), hyporexia or anorexia (4), regurgitation (4), vomiting (3), and gagging (1).

For 8 dogs, results of physical examination were unremarkable. Findings for the remaining dogs included tachypnea (n = 2), several subcutaneous masses (2), pelvic limb muscle atrophy (2), systolic heart murmur (2), signs of tenseness during abdominal palpation (2), absent lung sounds (1), increased respiratory sounds (1), harsh lung sounds in the right hemithorax (1), tachycardia (1), pelvic limb proprioceptive deficits (1), pelvic limb weakness (1), signs of pain on palpation of the right pelvic limb at the site of a previous fracture (1), palpably smaller left popliteal lymph node versus right popliteal lymph node (1), nonambulatory tetraplegia with decreased postural reactions (pelvic reaction greater than the thoracic reaction) secondary to weakness (1), general paresis (1), decreased segmental reflexes in all limbs (1), absent gag reflex (1), bilateral ptosis (1), mydriasis of the left eye and miosis of the right eye (1), generalized neck and muscle weakness (1), hypersalivation (1), 2-cm soft subcutaneous mass on left ventral aspect of the thorax with raised pink masses on the dorsal and right lateral aspects of the muzzle (1), high body condition score (7/9; 1), and superficial mass in the right ear (1).

Laboratory tests

Serum biochemical abnormalities included high alanine aminotransferase activity (n = 7), high alkaline phosphatase activity (6), mildly high creatine kinase activity (3), high aspartate aminotransferase activity (2), and hypercalcemia (2). Complete blood count abnormalities included leukocytosis (n = 3), neutrophilia (3), and thrombocytosis (2). Eleven dogs received a urinalysis, and mild proteinuria was identified in 3 of these dogs. In all 7 dogs in which megaesophagus was diagnosed via CT, a diagnosis of myasthenia gravis was made through results of anti-ACHR antibody testing (n = 6) or a positive response to edrophonium chloridea administration (1).

Diagnostic imaging

Three-view thoracic radiography was performed for all dogs, revealing a mass in the cranioventral portion of the mediastinum in each dog. In 7 dogs, megaesophagus was diagnosed before surgery. Aspiration pneumonia affecting the right middle lung lobe was diagnosed in 1 dog with myasthenia gravis and megaesophagus. Another dog had a mild, diffuse pulmonary interstitial pattern on radiographs. A third dog had a rounded soft tissue nodule in the right cranial lung lobe, whereas a fourth dog had multiple pulmonary nodules in the right cranial lung lobe.

Two-view abdominal radiography was performed for 3 dogs. In 1 dog, a cranial abdominal mass, splenomegaly, gastrointestinal foreign material, and subcutaneous masses were identified. Hepatomegaly and a gastrointestinal foreign body were detected in another dog. No abnormalities were identified in the third dog.

Thoracic ultrasonography was performed for 8 dogs. A CMM was identified in all but 1 dog, in which interference by the aerated lung occurred. Abdominal ultrasonography was performed for 12 dogs. Pertinent findings included a splenic mass (n = 2), hepatic mass with nodules (2), bilateral renal corticomedullary indistinction (2), gallbladder sludge (2), mildly enlarged pancreas (1), mild diffuse nonspecific hepatopathy (1), stereovacuolar hepatopathy (1), splenic nodules (1), generalized splenomegaly (1), hyperechoic splenic nodules (1), multiple gastric foreign bodies (1), gastric nodules (1), lymphadenopathy (1), cystic regions in the medial iliac lymph node (1), punctate mineralization of the left adrenal gland (1), left adrenal nodule (1), mild right adrenomegaly and absent left adrenal gland (1), bilateral renal cortical cysts (1), cystic nodules within the gallbladder lumen with a cholelith (1), cavitated echogenic mass in the right caudal aspect of the abdomen (1), and prostatomegaly (1).

Noncontrast- and contrast-enhanced CT were performed prior to surgery for 16 dogs. Median approximate tumor diameter was 6.0 cm (IQR, 4.0 to 8.4 cm), and median estimated tumor volume was 113.1 cm3 (IQR, 33.5 to 313.3 cm3). In none of the CMMs was invasion of surrounding structures apparent. Additional thoracic findings included megaesophagus (n = 7), interstitial pulmonary pattern (4), alveolar pulmonary pattern (4), thoracic fat-density masses (3), sternal lymphadenopathy (3), a soft tissue nodule in the right cranial lung lobe (1), axillary and superficial cervical lymphadenopathy (1), soft tissue–attenuating nodule in the left caudal lung lobe (1), focal ground glass opacities in the lungs (1), focal osteolysis of the 13th thoracic vertebral body (1), mineralization of the aortic root (1), and pleural effusion (1). Additional abdominal findings included gallbladder sedimentation (2); hepatic mass (1); splenic nodule (1); multiple splenic masses (1); generalized splenomegaly (1); mesenteric nodule (1); bilateral renal dystrophic mineralization, nephrolithiasis, and cortical infarct (1); renal recess mineralization in the right kidney (1); abdominal subcutaneous fat mass (1); cholelithiasis (1); mineralization of the right kidney (1); and mild hepatic lymphadenopathy (1).

Cytologic and histologic examination

Preoperative cytologic examination of fine-needle aspirate samples obtained from the CMM was performed for 12 dogs, resulting in the diagnosis or suspicion of thymoma in 8 dogs. Hemorrhagic effusion with reactive mesothelial hyperplasia was diagnosed in 1 dog. For the remaining 3 dogs, results of cytologic examination were nondiagnostic. Needle-core biopsy was performed for 1 dog, and results of histologic examination of biopsy specimens were consistent with thymoma.

Clinical staging

Nine dogs with thymoma were classified as having stage I disease, 3 dogs as stage II disease, and 3 dogs as stage III disease according to a reported staging scheme.16 Seven dogs were further classified as having no evidence of paraneoplastic syndrome, 7 dogs as having myasthenia gravis, and 3 dogs as having a nonthymic malignant tumor. For 3 dogs, staging was not applicable because either thymoma was not diagnosed (n = 2) or results of histologic examination for determination of tumor margins were unavailable owing to the dog's death during surgery (1).

Perioperative medical treatment

Four of the 7 dogs with myasthenia gravis and megaesophagus were treated with pyridostigminec prior to surgery. The preoperative dose was reduced for 1 of these 4 dogs because of concerns about cholinergic toxic effects. Two dogs received prednisone prior to surgery (one dog at 0.07 mg/kg [0.03 mg/lb], PO, q 24 h, and the other at 1.2 mg/kg [0.55 mg/lb], PO, q 24 h); neither of these dogs had myasthenia gravis.

Anesthetic management

Anesthesia was provided according to the discretion of the attending anesthesiologist. In general, most dogs received an opioid for premedication, and anesthesia was induced with propofol and maintained with isoflurane in oxygen. Two dogs were endobronchially intubated, and the remainder were endotracheally intubated. Four endotracheally intubated dogs underwent subsequent endobronchial blockade. One-lung ventilation was performed for 6 dogs during dissection of the CMM.

Surgical procedures

Dogs were positioned in dorsal recumbency with portsd–f placed as described elswhere,5 except for 1 dog that was positioned in lateral recumbency. Vessel-sealing devicesg,h and angled 5-mm telescopesi were used in all situations. In all dogs but 1, masses were extirpated by use of specimen retrieval bagsj (Supplemental Video S1, available at avmajournals.avma.org/doi/suppl/10.2460/javma.250.11.1283). The largest CMM resected successfully via VATS measured 12 × 6 cm with an estimated volume of 1,317 cm3. Median duration of the VATS procedure was 117.5 minutes (IQR, 91.5 to 136.3 minutes). A chest tube was placed in 17 dogs, with a median duration of indwelling placement of 17 hours (IQR, 12 to 20 hours).

Additional procedures included VATS lung lobectomy (n = 2) in the dog with the mass in the right cranial lung lobe and the dog with multiple pulmonary nodules in the same lobe. Splenectomy via a laparotomy was performed in 1 dog. In 1 dog with lymphadenopathy, the mediastinal lymph node was submitted for histologic examination.

Complications

Major intraoperative complications occurred in 1 dog in which iatrogenic laceration of the vena cava resulted in severe hemorrhage during dissection dorsal to the mass. Emergency intercostal thoracotomy was performed to provide open-chest CPR, but resuscitation was unsuccessful. No other major intraoperative complications were noted. Nonemergent conversion to median sternotomy was necessary in 1 dog because of the large size of the mass and adhesions detected during surgery.

Major postoperative complications occurred in 6 dogs with myasthenia gravis and megaesophagus. One dog developed respiratory arrest while the chest tube was being aspirated. Cardiopulmonary resuscitation was attempted but was unsuccessful. No postmortem examination of the dog was performed. Five dogs developed aspiration pneumonia, and 4 of these dogs subsequently died or were euthanized. The fifth dog survived and was alive at last follow-up 351 days after the surgery.

In 2 dogs that developed aspiration pneumonia, myasthenic decompensation appeared to precipitate the aspiration pneumonia and death. One of these dogs developed acute, progressive ambulatory weakness 48 hours after surgery and acute laryngeal paralysis the following day. An airway examination was performed, and the dog was intubated. Edrophonium chloridea (0.2 mg/kg [0.09 mg/lb]) was administered IV, and the dog was extubated for a recheck laryngeal examination, which revealed dramatic improvement in laryngeal function. However, the improved response was transient, and the dog was again endotracheally intubated and started on a constant rate infusion of edrophonium chloridea (0.1 mg/kg/h [0.045 mg/lb/h], IV). After 36 hours, another attempt was made to wean the dog off the ventilator. At this point, a large amount of purulent material was detected in the endotracheal tube, and aspiration pneumonia was diagnosed via thoracic radiography. The owner elected euthanasia.

In the other dog, plasmapheresis was performed because of acute, progressive weakness that developed 24 hours after VATS. These signs were also attributed to underlying myasthenia gravis. Leflunamidek (2.5 mg/kg [1.1 mg/lb], PO, q 24 h), a constant rate infusion of pyridostigminec (0.02 mg/kg/h [0.009 mg/lb], IV), and dexamethasone sodium phosphatel (at the 2 mg/kg [0.9 mg/lb] equivalent prednisone dose, IV, q 24 h) were also administered to this dog. However, acute renal injury occurred, signs of progressive weakness were observed, and the dog developed dyspnea and ventilatory failure. Aspiration pneumonia was diagnosed via thoracic radiography, and the dog was euthanized.

Two dogs developed port-site infections, which resolved with antimicrobial treatment. These infections were considered minor complications.

Histologic examination

Histologic analysis revealed that the extirpated CMM in 16 of the 18 dogs was a thymoma. Bronchoalveolar carcinoma of the lung was diagnosed in addition to thymoma in the dog in which a nodule was detected in the right cranial lung lobe via radiography and CT. Of the 2 dogs without a thymoma diagnosis, the extirpated mass in 1 dog was classified as thymic anaplastic carcinoma. The other dog had multiple pulmonary nodules of the right cranial lung lobe detected via thoracic radiography and received a diagnosis of hemangiosarcoma and associated hematoma (CMM) and intravascular metastatic emboli (lung). Additional histopathologic findings in dogs with thymoma included hemangiosarcoma of the spleen, hemangiosarcoma of the liver, granuloma of the liver, and adenoma of the liver (n = 1) and metastatic carcinoma of the cranial mediastinal lymph node (1).

Cancer treatments

Chemotherapy (alternation between carboplatin and doxorubicin) was initiated in 1 dog with thymoma and a concurrent bronchoalveolar carcinoma that was removed via lung lobectomy during the VATS procedure. Before the VATS procedure, another dog underwent course-fractionated radiation of the thymoma involving administration of three 6-Gy doses. The third dose was administered 9 days before surgery, and imaging was not repeated prior to surgery. This dog died of iatrogenic laceration of the vena cava during dissection.

Survival rates

Seventeen of the 18 dogs survived the VATS procedure. Prior to hospital discharge, 4 of these 17 dogs died of complications relating to myasthenia gravis and megaesophagus (n = 3) or cardiopulmonary arrest during chest-tube aspiration (1). Thirteen dogs survived to hospital discharge. Median duration of hospitalization for dogs discharged from the hospital was 2 days (IQR, 2 to 4 days).

Three dogs were excluded from the survival analysis to determine survival rates in dogs following VATS surgery with thymoma. These dogs included one with thymic anaplastic carcinoma, another with hemangiosarcoma, and the dog with thymoma that died during surgery. Two dogs with nonparaneoplastic thymoma died of an unknown cause 80 and 989 days following surgery. Median survival time after VATS for CMM extirpation (ie, thymectomy in this situation) was 20 days for dogs with concurrent myasthenia gravis and megaesophagus, whereas dogs without myasthenia gravis and megaesophagus survived for at least 60 days (P = 0.004; Figure 1) and had no thymoma-related death (follow-up range, 60 to 989 days). One of the 2 dogs without thymoma died of progression of metastatic hemangiosarcoma 2 weeks after surgery, and the other dog died of thymic anaplastic carcinoma 4 months after surgery.

Figure 1—
Figure 1—

Product limit curves of survival rates following VATS thymectomy in dogs with (solid line; n = 7) and without (dashed line; 8) myasthenia gravis and megaesophagus. The survival rate was significantly (P = 0.004) worse for dogs with myasthenia gravis and megaesophagus. Three dogs were excluded from this survival analysis: 1 with thymic anaplastic carcinoma, 1 with hemangiosarcoma, and 1 with thymoma that died during surgery.

Citation: Journal of the American Veterinary Medical Association 250, 11; 10.2460/javma.250.11.1283

Discussion

A VATS approach to CMM extirpation is a minimally invasive alternative to thoracotomy in certain dogs and, in the present study, was successful in the removal of masses with an approximate volume ≤ 1,300 cm3. However, 75% of tumors had a volume < 313 cm3 or a diameter < 8.4 cm; therefore, we consider an approximate tumor volume ≤ 300 cm3 or diameter < 8 cm in dogs weighing > 20 kg (44 lb) to be a reasonable size for CMM extirpation by means of VATS. Although major intraoperative complications are possible, the risk in the present study was fairly low (1/18) with appropriate preoperative diagnostic imaging, case selection, and competence in VATS. Concordant with findings in other studies,3,17 dogs with paraneoplastic myasthenia gravis and megaesophagus had a poor postoperative outcome despite successful surgery. In contrast, dogs with thymoma without myasthenia gravis and megaesophagus appeared to be excellent candidates for CMM extirpation by means of VATS.

Characteristics of dogs with CMMs in the present study were consistent with those in other reports.1,4,17,18 Clinical signs were attributed to the presence of a thoracic mass and paraneoplastic syndromes such as myasthenia gravis, megaesophagus, other immune-mediated diseases, and hypercalcemia, and those signs were similar to those in previous studies.1,3,4

In 7 dogs with clinical signs suggestive of myasthenia gravis, myasthenia gravis was diagnosed by a positive response to edrophonium chloride administration or by a high anti-ACHR antibody titer. This finding was consistent with those for previously reported paraneoplastic syndromes in humans and dogs with thymomas.1,3,4,19 Two dogs with thymoma in the present study appeared to develop postoperative myasthenic decompensation or myasthenic crisis, which precipitated their deaths. Postoperative development of myasthenia gravis has been reported for human and veterinary patients undergoing thymectomy, but postoperative myasthenic crisis has not been reported for veterinary patients undergoing thymectomy.1,3,4,17,20,21

Myasthenic crisis in humans is defined as a “weakness from acquired myasthenia gravis that is severe enough to necessitate intubation or to delay extubation beyond 24 hours after surgery.”22 Preoperative recommendations for humans with myasthenia gravis prior to thymectomy include serial plasma exchange23 and corticosteroid administration. Because corticosteroid drugs are effective at reducing the number of lymphocytes in the thymic germinal center and the associated autoantibody production, their use has been associated with improved clinical outcome in humans with myasthenia gravis.20,24 Corticosteroid administration was also associated with dramatic improvement in a cat that developed myasthenia gravis 7 weeks after thymectomy in 1 report.21 No dogs in the present study with paraneoplastic myasthenia gravis or megaesophagus received corticosteroid drugs in the perioperative period.

Pyridostigmine has the potential to minimize the risk of postoperative myasthenic decompensation and thus reduce the risk of aspiration pneumonia. Four dogs in which thymoma was diagnosed received pyridostigmine before surgery. Two of these dogs died prior to hospital discharge, and 1 dog died of complications attributed to myasthenia gravis and megaesophagus 3 weeks after surgery. The fourth dog was still alive at final follow-up. Given the small number of dogs treated, we were unable to determine whether perioperative pyridostigmine administration was beneficial; however, we believe this should be considered in dogs with myasthenia gravis.

Plasma exchange is a short-term immune-directed treatment recommended as an adjunctive treatment in humans with myasthenia gravis25,26 in which the bulk of circulating anti-ACHR antibody is eliminated, thereby resulting in a decrease in the severity of clinical signs.27 Although no direct evidence exists to support the preoperative use of plasma exchange in dogs with thymoma and myasthenia gravis, clinical remission was reportedly achieved following plasma exchange and corticosteroid treatment in a dog with myasthenia gravis.28 Given the considerable postoperative morbidity rate and significantly shorter survival time of dogs with myasthenia gravis and megaesophagus in the present study, preoperative plasma exchange with or without pyridostigmine or corticosteroid administration should be considered in select cases to improve outcome. Owners of dogs that have antibody titers indicative of myasthenia gravis or megaesophagus should be counseled that there is a risk of myasthenic decompensation and aspiration pneumonia.

Sixteen dogs in the present study received a preoperative thoracic CT examination. In humans29 and dogs,30,31 thoracic CT is recommended for preoperative staging and assessment of the invasiveness and size of mediastinal masses. Accurate case selection prior to CMM extirpation by means of VATS imparts safety to the procedure and limits the incidence of conversion to an open surgical approach. Therefore, preoperative CT is considered an important step in patient selection for a VATS approach to CMM extirpation.

In 1 dog of the present study, dissection dorsal to the mass resulted in iatrogenic laceration of the cranial vena cava and death. Although an initial CT examination was performed, the dog received 3 radiation treatments prior to surgery. Following radiation treatment, the mass appeared via thoracic radiography to have decreased in size. Radiation causes fibrosis,32 and this effect may have induced some fibrous adhesions between the mass and the vena cava. Caution is recommended when a VATS approach is used for CMMs treated with neoadjuvant radiation. Conversely, vena cava laceration has been reported for dogs undergoing CMM extirpation via thoracotomy1,17 and may have been due to technical error in the dog reported here.

Another dog in the present study required elective conversion to median sternotomy to complete the resection. The mass was likely too large for a VATS approach, measuring approximately 2,572 cm3 in volume. Although masses with a volume as large as 1,300 cm3 were successfully removed, most were < 313 cm3 in volume. Consequently, we believe that noninvasive CMMs with a volume much more than 300 cm3 should be considered carefully when planning for VATS resection.

Surgery in the present study was performed as described elsewhere5 in all but 1 dog, in which a lateral approach was used. From a procedural standpoint, the most important aspect of the procedure is in the creation of a safe plane of dissection from the pericardium and along the dorsal aspect of the mass, which is close to the cranial vena cava. Sponge forceps, grasping forceps, and fan retractors had been used to maintain cranial and ventral traction on the mass during dissection. The dissection had been completed with vessel-sealing devicesf,g in all dogs, and clinically important hemorrhage occurred in only 1 dog in which the vena cava was lacerated.

Port-site metastasis was not observed in any of the surviving dogs. Although rarely reported in the veterinary literature,33 the risk for port-site metastasis might be reduced if retrieval bags or wound retractors were used for specimen extraction.33

The use of 1-lung ventilation has been recommended for VATS thymectomy in dogs.34 One-lung ventilation was accomplished in 6 dogs of the present study by endobronchial blockade or by double-lumen endobronchial intubation and selective ventilation. This ventilation technique is valuable for dogs with smaller thoracic volumes because the working space is decreased.35 One-lung ventilation allows for sufficient visibility of intrathoracic structures in these situations and allows avoidance of intermittent ventilation, which can be unrealistic to perform during long anesthetic procedures.34 Many physicians prefer 1-lung ventilation because it provides improved visibility of the mediastinum and prevents lung ventilation from interfering with the surgical procedure.36

In all but 1 dog of the present study, surgery was successfully completed; however, the postoperative morbidity and mortality rates were high because of the high-risk group of dogs included. Nearly 40% of dogs had myasthenia gravis and associated megaesophagus, and nearly 60% of these dogs died after surgery because of associated complications such as aspiration pneumonia. Median survival time in these dogs was only 20 days. This outcome is consistent with that in a previous report3 of open surgical removal of thymomas in 23 dogs, in which 66% of dogs with concurrent megaesophagus died within 1 week after surgery.3 Similarly, a > 5-fold increase in the risk of death following thymectomy has been identified in dogs with thymoma and paraneoplastic syndromes.17 In contrast, dogs with thymoma without paraneoplastic syndromes had an excellent outcome following VATS thymectomy in the present study, except for the dog that received preoperative radiation treatment. In 3 of the dogs with thymoma, nonthymic tumors were also diagnosed. Two of the dogs failed to survive past 1 month after surgery, with the final dog dying of hemangiosarcoma that developed after hospital discharge. These results concur with those in another report1 that suggest a secondary nonthymic tumor can also result in a shorter median survival time.1

In a reported comparison of VATS thymectomy with open thymectomy (by median sternotomy or intercostal thoracotomy) in humans, no significant difference in mean duration of surgery was identified.6 However, the VATS approach resulted in a significant decrease in amounts of thoracic drainage and postoperative epidural analgesia required and duration of hospitalization. The veterinary literature9 indicates that thoracoscopic surgery is advantageous for pericardectomy because of less postoperative signs of pain, fewer wound complications, and a faster return to function than with thoracotomy. Multiple additional studies11–13 have shown the potential benefits of VATS. In the present study, median duration of surgery was 117.5 minutes. In comparison, another study37 revealed a median duration of surgery of 109 minutes for median sternotomy.

In terms of hospital stay, duration of hospitalization ranged from 3 to 5 days in a study4 involving tumor removal via median sternotomy or intercostal thoracotomy in 9 cats and 11 dogs, with 1 cat hospitalized for 7 days and 1 dog hospitalized for 12 days. In the present study, duration of hospitalization ranged from 2 to 4 days in most surviving dogs. Thoracoscopic thymectomy could also be expected to require a briefer hospitalization period than thoracotomy, but additional research is necessary to support this expectation.

Limitations of the present study included factors inherent to retrospective studies and a small sample size. Additionally, the study was multi-institutional in scope, and therefore, variation existed in anesthetic protocols, perioperative management, follow-up procedures, and surgeon experience. The cause of death for some dogs was also unknown.

Regardless of these limitations, findings of the study reported here suggested that CMM extirpation by means of a VATS approach may be an acceptable minimally invasive alternative to thoracotomy in certain dogs and may be beneficial owing to the advantages of minimally invasive versus more invasive approaches. Major intraoperative complications were uncommon (1/18 dogs). Preoperative CT is recommended for selection of suitable patients and preoperative planning. Dogs weighing > 20 kg and with a noninvasive CMM < 300 cm3 in volume and 8 cm in diameter appeared to be good candidates for a VATS approach, although larger masses might be resectable in some situations. Dogs with paraneoplastic myasthenia gravis and megaesophagus had a poor short-term prognosis, and efforts should be made to improve these dogs' suitability for anesthesia and surgery in the perioperative period.

Acknowledgments

The authors declare that there were no conflicts of interest. Presented in abstract form at the 12th Annual Meeting of the Veterinary Endoscopy Society in Santa Barbara, Calif, April 2015.

ABBREVIATIONS

ACHR

Acetylcholine receptor

CMM

Cranial mediastinal mass

IQR

Interquartile range

VATS

Video-assisted thoracic surgery

Footnotes

a.

Edrophonium chloride, Enlon Mylan Institutional, Rockford, Ill.

b.

JMP, version 9.0.2, SAS Institute Inc, Cary, NC.

c.

Mestinon, Valeant Pharmaceuticals International, Viejo, Calif.

d.

Thoracoport, 5.5 mm, Covidien, Mansfield, Mass.

e.

Thoracoport, 11.5 mm, Covidien, Mansfield, Mass.

f.

Endotip, 5.5 mm, Karl Storz Endoscopy, El Segundo, Calif.

g.

Blunt- or dolphin-tip LigaSure, 5 mm, Covidien, Mansfield, Mass.

h.

Harmonic scalpel, Ethicon, Sommerville, NJ.

i.

Hopkins II 30° telescope, Karl Storz Endoscopy, El Segundo, Calif.

j.

Endobag, Covidien, Mansfield, Mass.

k.

Leflunamide, Heritage Pharmaceuticals Inc, Edison, NJ.

l.

Dexaject SP, Henry Schein Animal Health, Dublin, Ohio.

References

  • 1. Robat CS, Cesario L, Gaeta R, et al. Clinical features, treatment options, and outcome in dogs with thymoma: 116 cases (1999–2010). J Am Vet Med Assoc 2013; 243: 14481454.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Klebanow ER. Thymoma and acquired myasthenia gravis in the dog: a case report and review of 13 additional cases. J Am Anim Hosp Assoc 1992; 28: 6369.

    • Search Google Scholar
    • Export Citation
  • 3. Atwater SW, Powers BE, Park RD, et al. Thymoma in dogs: 23 cases (1980–1991). J Am Vet Med Assoc 1994; 205: 10071013.

  • 4. Zitz JC, Birchard SJ, Couto GC, et al. Results of excision of thymoma in cats and dogs: 20 cases (1984–2005). J Am Vet Med Assoc 2008; 232: 11861192.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Mayhew PD, Friedberg JS. Video-assisted thoracoscopic resection of noninvasive thymomas using one-lung ventilation in two dogs. Vet Surg 2008; 37: 756762.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Chetty GK, Khan OA, Onyeaka CVP, et al. Experience with video-assisted surgery for suspected mediastinal tumours. Eur J Surg Oncol 2004; 30: 776780.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Engum SA. Minimal access thoracic surgery in the pediatric population. Semin Pediatr Surg 2007; 16: 1426.

  • 8. Chung JW, Kim HR, Kim DK, et al. Long-term results of thoracoscopic thymectomy for thymoma without myasthenia gravis. J Int Med Res 2012; 40: 19731981.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. 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: 472479.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Dupre GP, Corlouer J, Bouvy B. Thoracoscopic pericardectomy performed without pulmonary exclusion in 9 dogs. Vet Surg 2001; 30: 2127.

  • 11. 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: 493498.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Landsdowne JL, Monnet E, Twedt DC, et al. Thoracoscopic lung lobectomy for treatment of lung tumors in dogs. Vet Surg 2005; 34: 530535.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. 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: 681688.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Brissot HN, Dupre GP, Bouvy BM, et al. Thoracoscopic treatment of bullous emphysema in 3 dogs. Vet Surg 2003; 32: 524529.

  • 15. Case JB, Mayhew PD, Singh A, et al. Evaluation of video-assisted thoracic surgery for treatment of spontaneous pneumothorax and pulmonary bullae in dogs. Vet Surg 2015; 44(suppl 1):3138.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Aronsohn M. Canine thymoma. Vet Clin North Am Small Anim Pract 1985; 15: 755767.

  • 17. Garneau MS, Price LL, Withrow SJ, et al. Perioperative mortality and long-term survival in 80 dogs and 32 cats undergoing excision of thymic epithelial tumors. Vet Surg 2015; 44: 557564.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Day MJ. Review of thymic pathology in 30 cats and 36 dogs. J Small Anim Pract 1997; 38: 393403.

  • 19. Thongprayoon C, Tantrachoti P, Phatharacharukul P, et al. Associated immunological disorders and cellular immune dysfunction in thymoma: a study of 87 cases from Thailand. Arch Immunol Ther Exp (Warsz) 2013; 61: 8593.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Drachman DB. Myasthenia gravis. N Engl J Med 1994; 330: 17971810.

  • 21. Singh A, Boston SE, Poma R. Thymoma-associated exfoliative dermatitis with post-thymectomy myasthenia gravis in a cat. Can Vet J 2010; 51: 757760.

    • Search Google Scholar
    • Export Citation
  • 22. Bedlack RS, Sanders DB. On the concept of myasthenic crisis. J Clin Neuromuscul Dis 2002; 4: 4042.

  • 23. Jiann-Hong Y, Hou-Chang C. Optimal volume of processed plasma and total number of selective plasmapheresis sessions in the treatment of patients with severe generalized myasthenia gravis. J Clin Apher 1999; 14: 177180.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Berrih-Aknin S, Le Panse R. Myasthenia gravis: a comprehensive review of immune dysregulation and etiologic mechanisms. J Autoimmun 2014; 52: 90100.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Perlo VP, Shahani BT, Huggins CE, et al. Effect of plasmapheresis in myasthenia gravis. Ann N Y Acad Sci 1981; 377: 709724.

  • 26. Liu J, Wang W, Xue J, et al. Comparing the autoantibody levels and clinical efficacy of double filtration plasmapheresis, immunoadsorption, and intravenous immunoglobulin for the treatment of late-onset myasthenia gravis. Ther Apher Dial 2009; 14: 153160.

    • Search Google Scholar
    • Export Citation
  • 27. Richman DP, Agius MA. Treatment of autoimmune myasthenia gravis. Neurology 2003; 61: 16521661.

  • 28. Bartges JW, Klausner JS, Bostwick EF, et al. Clinical remission following plasmapheresis and corticosteroid treatment in a dog with acquired myasthenia gravis. J Am Vet Med Assoc 1990; 196: 12761278.

    • Search Google Scholar
    • Export Citation
  • 29. Maher MM, Shepard J. Imaging of thymoma. Semin Thorac Cardiovasc Surg 2005; 17: 1219.

  • 30. Yoon J, Feeney DA, Cronk DE. Computed tomographic evaluation of canine and feline mediastinal masses in 14 patients. Vet Radiol Ultrasound 2004; 45: 542546.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Rosado-de-Christenson ML, Strollo DC, Marom EM. Imaging of thymic epithelial neoplasms. Hematol Oncol Clin North Am 2006; 22: 409431.

    • Search Google Scholar
    • Export Citation
  • 32. Denham JW, Hauer-Jensen M. The radiotherapeutic injury— a complex “wound.” Radiother Oncol 2002; 63: 129145.

  • 33. Brisson BA, Reggeti F, Bienzle D. Portal site metastasis of invasive mesothelioma after diagnostic thoracoscopy in a dog. J Am Vet Med Assoc 2006; 229: 980983.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Mayhew PD, Culp WTN, Pascoe PJ, et al. Evaluation of blind thoracoscopic-assisted placement of three double-lumen endobronchial tube designs for one-lung ventilation in dogs. Vet Surg 2012; 41: 664670.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Mayhew KN, Mayhew PD, Sorrell-Raschi L, et al. Thoracoscopic subphrenic pericardectomy using double-lumen endobronchial intubation for alternating one-lung ventilation. Vet Surg 2009; 38: 961966.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Toolabi K, Aminian A, Javid JM, et al. Minimal access mediastinal surgery: one or two lung ventilation? J Minim Access Surg 2009; 5: 103107.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Burton CA, White RN. Review of the technique and complications of median sternotomy in the dog and cat. J Small Anim Pract 1996; 37: 516522.

    • Crossref
    • Search Google Scholar
    • Export Citation

Supplementary Materials

Contributor Notes

Address correspondence to Dr. Case (caseb@ufl.edu).
  • Figure 1—

    Product limit curves of survival rates following VATS thymectomy in dogs with (solid line; n = 7) and without (dashed line; 8) myasthenia gravis and megaesophagus. The survival rate was significantly (P = 0.004) worse for dogs with myasthenia gravis and megaesophagus. Three dogs were excluded from this survival analysis: 1 with thymic anaplastic carcinoma, 1 with hemangiosarcoma, and 1 with thymoma that died during surgery.

  • 1. Robat CS, Cesario L, Gaeta R, et al. Clinical features, treatment options, and outcome in dogs with thymoma: 116 cases (1999–2010). J Am Vet Med Assoc 2013; 243: 14481454.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Klebanow ER. Thymoma and acquired myasthenia gravis in the dog: a case report and review of 13 additional cases. J Am Anim Hosp Assoc 1992; 28: 6369.

    • Search Google Scholar
    • Export Citation
  • 3. Atwater SW, Powers BE, Park RD, et al. Thymoma in dogs: 23 cases (1980–1991). J Am Vet Med Assoc 1994; 205: 10071013.

  • 4. Zitz JC, Birchard SJ, Couto GC, et al. Results of excision of thymoma in cats and dogs: 20 cases (1984–2005). J Am Vet Med Assoc 2008; 232: 11861192.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5. Mayhew PD, Friedberg JS. Video-assisted thoracoscopic resection of noninvasive thymomas using one-lung ventilation in two dogs. Vet Surg 2008; 37: 756762.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6. Chetty GK, Khan OA, Onyeaka CVP, et al. Experience with video-assisted surgery for suspected mediastinal tumours. Eur J Surg Oncol 2004; 30: 776780.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Engum SA. Minimal access thoracic surgery in the pediatric population. Semin Pediatr Surg 2007; 16: 1426.

  • 8. Chung JW, Kim HR, Kim DK, et al. Long-term results of thoracoscopic thymectomy for thymoma without myasthenia gravis. J Int Med Res 2012; 40: 19731981.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. 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: 472479.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Dupre GP, Corlouer J, Bouvy B. Thoracoscopic pericardectomy performed without pulmonary exclusion in 9 dogs. Vet Surg 2001; 30: 2127.

  • 11. 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: 493498.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Landsdowne JL, Monnet E, Twedt DC, et al. Thoracoscopic lung lobectomy for treatment of lung tumors in dogs. Vet Surg 2005; 34: 530535.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. 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: 681688.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Brissot HN, Dupre GP, Bouvy BM, et al. Thoracoscopic treatment of bullous emphysema in 3 dogs. Vet Surg 2003; 32: 524529.

  • 15. Case JB, Mayhew PD, Singh A, et al. Evaluation of video-assisted thoracic surgery for treatment of spontaneous pneumothorax and pulmonary bullae in dogs. Vet Surg 2015; 44(suppl 1):3138.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Aronsohn M. Canine thymoma. Vet Clin North Am Small Anim Pract 1985; 15: 755767.

  • 17. Garneau MS, Price LL, Withrow SJ, et al. Perioperative mortality and long-term survival in 80 dogs and 32 cats undergoing excision of thymic epithelial tumors. Vet Surg 2015; 44: 557564.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Day MJ. Review of thymic pathology in 30 cats and 36 dogs. J Small Anim Pract 1997; 38: 393403.

  • 19. Thongprayoon C, Tantrachoti P, Phatharacharukul P, et al. Associated immunological disorders and cellular immune dysfunction in thymoma: a study of 87 cases from Thailand. Arch Immunol Ther Exp (Warsz) 2013; 61: 8593.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Drachman DB. Myasthenia gravis. N Engl J Med 1994; 330: 17971810.

  • 21. Singh A, Boston SE, Poma R. Thymoma-associated exfoliative dermatitis with post-thymectomy myasthenia gravis in a cat. Can Vet J 2010; 51: 757760.

    • Search Google Scholar
    • Export Citation
  • 22. Bedlack RS, Sanders DB. On the concept of myasthenic crisis. J Clin Neuromuscul Dis 2002; 4: 4042.

  • 23. Jiann-Hong Y, Hou-Chang C. Optimal volume of processed plasma and total number of selective plasmapheresis sessions in the treatment of patients with severe generalized myasthenia gravis. J Clin Apher 1999; 14: 177180.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Berrih-Aknin S, Le Panse R. Myasthenia gravis: a comprehensive review of immune dysregulation and etiologic mechanisms. J Autoimmun 2014; 52: 90100.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25. Perlo VP, Shahani BT, Huggins CE, et al. Effect of plasmapheresis in myasthenia gravis. Ann N Y Acad Sci 1981; 377: 709724.

  • 26. Liu J, Wang W, Xue J, et al. Comparing the autoantibody levels and clinical efficacy of double filtration plasmapheresis, immunoadsorption, and intravenous immunoglobulin for the treatment of late-onset myasthenia gravis. Ther Apher Dial 2009; 14: 153160.

    • Search Google Scholar
    • Export Citation
  • 27. Richman DP, Agius MA. Treatment of autoimmune myasthenia gravis. Neurology 2003; 61: 16521661.

  • 28. Bartges JW, Klausner JS, Bostwick EF, et al. Clinical remission following plasmapheresis and corticosteroid treatment in a dog with acquired myasthenia gravis. J Am Vet Med Assoc 1990; 196: 12761278.

    • Search Google Scholar
    • Export Citation
  • 29. Maher MM, Shepard J. Imaging of thymoma. Semin Thorac Cardiovasc Surg 2005; 17: 1219.

  • 30. Yoon J, Feeney DA, Cronk DE. Computed tomographic evaluation of canine and feline mediastinal masses in 14 patients. Vet Radiol Ultrasound 2004; 45: 542546.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Rosado-de-Christenson ML, Strollo DC, Marom EM. Imaging of thymic epithelial neoplasms. Hematol Oncol Clin North Am 2006; 22: 409431.

    • Search Google Scholar
    • Export Citation
  • 32. Denham JW, Hauer-Jensen M. The radiotherapeutic injury— a complex “wound.” Radiother Oncol 2002; 63: 129145.

  • 33. Brisson BA, Reggeti F, Bienzle D. Portal site metastasis of invasive mesothelioma after diagnostic thoracoscopy in a dog. J Am Vet Med Assoc 2006; 229: 980983.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Mayhew PD, Culp WTN, Pascoe PJ, et al. Evaluation of blind thoracoscopic-assisted placement of three double-lumen endobronchial tube designs for one-lung ventilation in dogs. Vet Surg 2012; 41: 664670.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Mayhew KN, Mayhew PD, Sorrell-Raschi L, et al. Thoracoscopic subphrenic pericardectomy using double-lumen endobronchial intubation for alternating one-lung ventilation. Vet Surg 2009; 38: 961966.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Toolabi K, Aminian A, Javid JM, et al. Minimal access mediastinal surgery: one or two lung ventilation? J Minim Access Surg 2009; 5: 103107.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Burton CA, White RN. Review of the technique and complications of median sternotomy in the dog and cat. J Small Anim Pract 1996; 37: 516522.

    • Crossref
    • Search Google Scholar
    • Export Citation

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