Multiple tracheal resections and anastomoses in a blue and gold macaw (Ara ararauna).
Article Type: Report
Subject: Macaws (Health aspects)
Macaws (Research)
Macaws (Care and treatment)
Anastomosis (Methods)
Anastomosis (Health aspects)
Anastomosis (Research)
Surgical anastomosis (Methods)
Surgical anastomosis (Health aspects)
Surgical anastomosis (Research)
Trachea (Stenosis)
Trachea (Causes of)
Trachea (Research)
Trachea (Diagnosis)
Trachea (Care and treatment)
Authors: Jankowski, Gwen
Nevarez, Javier G.
Beaufrere, Hugues
Baumgartner, Wes
Reed, Scott
Tully, Thomas N.
Hedlund, Cheryl
Hennig, Geoff
Huck, Jennifer
Pub Date: 12/01/2010
Publication: Name: Journal of Avian Medicine and Surgery Publisher: Association of Avian Veterinarians Audience: Academic Format: Magazine/Journal Subject: Health Copyright: COPYRIGHT 2010 Association of Avian Veterinarians ISSN: 1082-6742
Issue: Date: Dec, 2010 Source Volume: 24 Source Issue: 4
Topic: Event Code: 310 Science & research
Geographic: Geographic Scope: United States Geographic Code: 1USA United States
Accession Number: 252005075
Full Text: Abstract: A 1.5-year-old, male blue and gold macaw (Ara ararauna) was anesthetized for a health examination and blood collection. The following day it was returned for episodes of coughing. The bird was presented again 13 days after the initial presentation with severe dyspnea. A tracheal stenosis was diagnosed by endoscopy and treated by surgical resection of 5 tracheal rings and tracheal anastomosis. The bird was discharged but returned 2 days later with a recurrent stenosis. Bougienage and balloon dilation of the stenotic area were performed separately; each resulted in less than 48 hours' improvement in clinical signs after treatment. A second tracheal resection and anastomosis was performed, during which an additional 10 tracheal rings were removed. This second anastomosis was significantly more difficult to complete given the marked variation in diameter of the proximal and distal tracheal segments. The macaw recovered without complication and has had no recurrence of respiratory abnormalities 2 years after the second surgery. This report describes the longest total tracheal segment to be resected, followed by tracheal anastomosis, in a psittacine bird. The positive outcome in this case suggests that, when surgical therapy is elected, an aggressive approach is necessary to prevent recurrence of tracheal stenosis. In addition, macaws can recover well even after significant lengths of the trachea are resected.

Key words: trachea, stenosis, intubation, anesthesia, resection, anastomosis, avian, blue and gold macaw, Ara ararauna

Clinical Report

A 1.5-year-old male blue and gold macaw (Ara ararauna) that weighed 878 g was presented for a routine health assessment. The macaw was anesthetized with isoflurane and intubated with a 4.0-mm uncuffed, Murphy-eye endotracheal tube for a total anesthetic period of 30 minutes. Results of a physical examination, complete blood cell count (CBC), and plasma biochemical analysis were within normal limits. After recovery, the bird regurgitated once in the clinic, and the owners reported a small amount of regurgitation during transportation home. The bird was presented the following day for coughing, and aspiration or tracheal irritation was suspected. Doxycycline (40 mg/kg IM q7d; Vibramycin, Boehringer Ingelheim, Ingelheim, Germany) and meloxicam (0.2 mg/kg IM q24h; Metacam, Pfizer, Exton, PA, USA) were administered. The macaw was presented to a referring veterinarian 12 days later with a history of acute respiratory distress. Upon presentation after referral, the bird demonstrated inspiratory dyspnea, tachypnea, and tail bobbing but appeared alert, and improved with oxygen administration. Pieces of white caseous material, which measured an average of 3 mm X 5 mm, were expelled from the trachea, which was visible by virtue of marked glottal dilatation. Smears from the tracheal material were stained with a modified Wright's stain, and results of a cytologic examination revealed heterophilic inflammation, with no evidence of infectious organisms. The differential diagnosis included bacterial or fungal tracheitis and/or trauma with secondary fibrosis of the tracheal mucosa, but involvement of the lower respiratory tract could not be ruled out. Because of the bird's debilitated condition, empirical therapy for bacterial and fungal infection that involved the respiratory tract was initiated (day 0): ciprofloxacin (20 mg/kg PO q12h), meloxicam (0.2 mg/kg PO q24h), metronidazole (25 mg/kg PO q12h), itraconazole (10 mg/kg PO q24h; Sporanox, Ortho-McNeil-Janssen Pharmaceuticals, Raritan, NJ, USA), and amphotericin B (1 mg/ml solution nebulized q12h).

The following day (day 1) results of a plasma biochemical analysis were within reference ranges. The CBC results showed a heterophilic leukocytosis (white blood cell count, 22 900 cells/[micro]L [reference range, 6000-12 000 cells/[micro]L]; and heterophils, 21 400 cells/[micro]L [reference range, 4500-8860 cells/[micro]L]). (1) On the morning of day 4, the bird had an obstructive breathing pattern, which was nonresponsive to oxygen therapy. Anesthesia was induced, with isoflurane delivered via a face mask. A left lateral incision was made caudal to the last rib and cranial to the pubic bone, and an air sac cannula (made from a 4-mm, noncuffed, endotracheal tube cut to a length of 4 cm, with fenestrations in the tip) was placed in the left caudal thoracic air sac. (2) A noticeable improvement in breathing was observed after placement of the cannula. A tracheoscopy was performed by using a 2.7-mm, 30-degree, rigid endoscope (Karl Storz Veterinary Endoscopy, Goleta, CA, USA), without the protective sheath. Approximately 5 7 cm caudal to the glottis, a focal tracheal stenosis, lined by mildly roughened and hyperemic mucosa, effectively reduced the tracheal lumen diameter by 80% (Fig 1). The membrane spanning the tracheal lumen was 1-2-mm thick, but the mucosa on the periphery exhibited gradual thickening. Multiple globules of white mucocaseous material were adherent to the mucosa in this area. An 8-Fr red rubber catheter was passed alongside the endoscope to aspirate material from the tracheal lumen. The catheter could not pass through the stenotic area, nor could the tissue be dislodged. The aspirated caseous material was submitted for aerobic bacterial culture and sensitivity, which yielded no bacterial growth.

Immediately after the tracheoscopy, wholebody radiographs were obtained, which revealed a soft-tissue tracheal opacity along a 1.7-cm segment of the dorsal and ventral tracheal walls (Fig 2) and a gas-filled proventriculus and small intestine. Because of the severity of the lesion, a tracheal resection and anastomosis procedure was elected.

Nine days after presentation, the bird was premedicated with butorphanol (2.5 mg/kg IM;

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Torbugesic, Fort Dodge Animal Health, Overland Park, KS, USA) and atropine (0.04 mg/kg IM). Anesthesia was then induced and maintained by using isoflurane (3% at 2 L/min) in oxygen delivered via the air sac cannula. Feathers were removed from the neck, and the area was sterilely prepped for surgery. A 5-cm skin incision was made by using the ventral midline cervical approach. An 8-Fr red rubber catheter was passed through the trachea to a point of resistance, which was determined to be the stenotic area, at which point 2 tracheal rings were resected. Because mucosal thickening was still observed at the resection site, 3 additional rings were resected from the proximal tracheal segment. By using 4-0 polypropylene (Prolene, Ethicon Inc, Scottsdale, AZ, USA), the tracheal ends (approximately 6 mm in diameter) were apposed by placing 10 evenly spaced, simple interrupted sutures, and 4 tension-relieving sutures were placed, which encircled the tracheal rings proximal and distal to the anastomosis site. After lavaging the area with saline solution, the musculature and underlying tissues were closed by using 5-0) poliglecaprone 25 suture (Monocryl; Ethicon) in a simple interrupted pattern, and the skin was closed by using 5-0 nylon suture (Ethilon; Ethicon) in a cruciate pattern. The resected tracheal rings were submitted for histopathologic analysis. A transparent adhesive bandage (OpSite, Smith and Nephew, London, England) was placed over the skin incision. A neck brace, which consisted of a padded 8-cm-long section of hollowed cylindrical foam was applied to avoid unnecessary movement at the surgical site. Nebulization was discontinued to avoid irritating the tracheal tissue after surgery, but all other treatments were continued.

Two days after surgery (day 11), the air sac cannula was occluded and later removed. The tip of the cannula was swabbed and submitted for aerobic bacterial culture and sensitivity testing. The site was closed by using 4-0 polydioxanone (PDS; Ethicon) in a single cruciate suture. The bacterial culture produced no growth. The bird was discharged on day 12 on continued prophylactic treatment with antimicrobial and antifungal medications.

Histopathologic analysis of the excised tracheal rings revealed moderate inflammation, chronicactive fibroplasia, and mucosal denudation. The entire mucosal epithelium was lost in the sections examined, and the submucosa was expanded primarily by fibrovascular tissue (granulation tissue) with scattered heterophils, occasional macrophages, and multinucleated giant cells. Inflammatory infiltrates were concentrated near the luminal surface, and no etiologic agents were detected within the tissues examined. Lesions were consistent with intraluminal tracheal trauma and tracheitis (Fig 3).

[FIGURE 3 OMITTED]

The bird was presented again on day 15 because of periodic wheezing, particularly after receiving oral medications. The bird was hospitalized and switched from oral to intramuscular administration of meloxicam. Itraconazole and metronidazole were discontinued, but the bird continued to receive doxycycline intramuscularly and ciprofloxacin orally. Physical examination revealed an inspiratory stridor, pectoral muscle tremors upon inspiration, and lethargy. Depression and anorexia were also observed during hospitalization. Blood was submitted for a CBC, results of which remained within reference ranges.

The macaw became more dyspneic and lethargic over the subsequent 4 days. On day 19, the bird developed an obstructive breathing pattern with bilateral serous nasal discharge and was anesthetized by using isoflurane delivered via a face mask for endoscopic placement of an air sac cannula and tracheoscopy. During placement of the second air sac cannula in the left caudal thoracic air sac, a 1-cm-wide, white plaque, presumed to be a fungal colony, was observed on the craniomedial aspect of the air sac. This lesion was considered secondary to environmental exposure from the previous air sac cannula. Treatment with itraconazole (10 mg/kg PO q24h), terbinafine (10 mg/kg PO q12h; Lamisil, Novartis, East Hanover, NJ, USA), and nebulization with amphotericin B (1 mg/mL for 15-30 min q12h) was instituted. Tracheoscopy revealed a rim of fibrous scar tissue immediately cranial to the sutures of the previous anastomosis site. Bougienage was performed by advancing the endoscope through the scar tissue to dilate the tracheal lumen, after which the respiratory character improved.

By day 21, the bird began wheezing, partially because the air sac cannula intermittently became occluded with mucoid and hemorrhagic discharge. The bird began regurgitating the morning of day 24. Because it continued to have difficulty breathing, the air sac cannula was removed on day 25 and another was placed in the right caudal thoracic air sac. Celioscopy revealed that the fungal colony in the left air sac was now yellow, plaque-like, and friable, which suggested the antifungal therapy was effective. Two large areas of pulmonary hemorrhage and air sac fibrosis that involved approximately 20% of the left cranial air sac were observed, likely because of trauma from the air sac cannula. Tracheoscopy revealed stenosis of the tracheal lumen, which was dilated by passing a 6-Fr Foley catheter past the level of the stenosis, dilating the balloon, and gently retracting the inflated catheter through the stenotic region.

The macaw was able to breathe easily after dilation of the tracheal stenosis and replacement of the air sac cannula. Its appetite improved dramatically, although its weight had decreased to 806 g by this time. After 48 hours, the air sac cannula was occluded to evaluate the bird's ability to breathe through the trachea. The bird did not develop dyspnea and exhibited minimal respiratory noise, and the air sac cannula was removed 72 hours after the last endoscopic procedure.

Approximately 12 hours after removing the air sac cannula (day 29), the macaw developed an obstructive breathing pattern and another air sac cannula was placed in the right caudal air sac. Tracheoscopy revealed severe tracheal fibrous stenosis, with narrowing of the tracheal lumen, and radiographs revealed intratracheal opacity over a distance of 1.3 cm, as well as a circular soft-tissue opacity approximately 0.5 cm in diameter, which protruded ventrally from the trachea at the level of the previous surgical site (Fig 4). Resection with anastomosis was recommended.

The second tracheal resection and anastomosis was performed on day 31 in a manner similar to the first procedure. A 1-cm, ovoid, firm nodule was located and removed at the level of the previous anastomosis site, and 8 tracheal rings at the level of the luminal stenosis were removed before attempting closure. Although tensionrelieving sutures were placed, 2 tracheal rings tore away from the distal segment when anastomosis was attempted. The lumen of the proximal trachea was significantly larger than that of the distal tracheal segment (Fig 5), so the diameter of the proximal trachea ring was reduced by resecting a 3-4-mm segment from the ventral aspect of the tracheal cartilage. The transected edges of the ring were apposed with a simple interrupted suture to reduce the lumen diameter. Apposition of tracheal ends was difficult and resulted in an abrupt reduction in lumen diameter and mild flattening of the proximal segment (Fig 5). Closure of the skin was performed as described for the initial surgery. Resected tissues were submitted for histopathology as well as aerobic bacterial and fungal cultures. After surgery, treatments remained the same except that nebulization with amphotericin B was discontinued to prevent tracheal irritation. Butorphanol (2 mg/kg IM) was administered for analgesia during the postoperative period, and the bird recovered well.

Two days after surgery (day 33), the macaw was discharged after having exhibited minimal respiratory noise and no dyspnea. Treatment with itraconazole, meloxicam, ciprofloxacin, and terbinafine was continued. The bird was kept confined in a quiet area with minimal handling. After the second surgery, itraconazole was continued for 3 weeks, and terbinafine, meloxicam, and ciprofloxacin were continued for 7 weeks. Five weeks after surgery, the bird weighed 936 g, and results of a CBC and plasma biochemical analysis were within normal limits.

Results of a tracheal culture taken before the second surgery revealed an Escherichia coli resistant to all tested antibiotics with the exception of azithromycin. This particular bacterial strain had been present in the hospital's intensive care unit at the time of the macaw's stay. The macaw, however, had continued to do well, so treatment was not modified. Histopathologic analysis of the tracheal tissue removed during the second surgery showed denuded epithelium over a segment of 10 tracheal rings. Exuberant fibrovascular (granulation) tissue extended over the entire resected length and occluded 30%-40% of the tracheal lumen. Moderate numbers of inflammatory cells, dominated by heterophils with lesser numbers of macrophages, were present within the tissue. Abundant gramnegative rods lined the tracheal luminal mucosa but were not present within inflammatory cells, which suggested surface contamination. More than 2 years after the second tracheal resection and anastomosis, the bird continues to do well, with no recurrence of clinical signs.

[FIGURE 4 OMITTED]

Discussion

Tracheal stenosis is a rare problem in avian species, but it is becoming more widely recognized and reported. (34) A variety of species, including geese, bald eagles (Haliaeetus leucocephalus), red-tail hawks (Buteo jamainensis), macaws, and a curassow (Crax alberti), have been affected, and many diagnoses of stenosis are thought to be related to intubation. (4-9) The avian trachea differs from most species in that it is composed of closely spaced, complete tracheal rings and lacks the trachealis muscle. (10) This is thought to make avian species more susceptible to trauma; therefore, endotracheal tubes without cuffs or with uninflated cuffs are recommended. (11,12) Survey data from private practitioners collected by the Association of Avian Veterinarians indicates that tracheal stenosis has been diagnosed and treated medically or surgically in blue and gold macaws, cockatoos, African grey parrots (Psittacus erithacus), and several wildlife species. Based on these data, the author of the cited report suggested that most of the reported cases have been the result of internal tracheal trauma, because infectious agents were not isolated. (3)

Traumatic tracheitis in other species is commonly related to intubation. (13-15) Rabbits have been reported to develop tracheal strictures approximately 15-25 days after intubation because of the difficulty and sometimes traumatic nature of the procedure in that species. (16) Mucosal and submucosal trauma from administration of high concentrations of dry gas through endotracheal tubes also has been described in rabbits. (17) Breathing nonhumidified air has also been a suspected cause of tracheal mucosal damage in guinea pigs. (7)

[FIGURE 5 OMITTED]

In avian species, several initiating factors related to intubation have been suggested to cause tracheal stenosis, including pressure necrosis, friction, infectious organisms that remain on endotracheal tubes, tissue reaction to the material from which endotracheal tubes are manufactured, and chemical disinfectants. (3) Ethylene oxide, which is not adequately vented after being used to sterilize endotracheal tubes, has been reported to be a cause of chemical trauma that leads to tracheal necrosis. (15,18) Phenolic compounds and formaldehyde have been shown to cause tracheitis in people. (19,20) At the authors' clinic, endotracheal tubes are disinfected by soaking in a 1:30 dilution of chlorhexidine, rinsed thoroughly, air-dried, and stored in plastic containers.

Physical trauma may result from traumatic tube placement, friction, or pressure necrosis. Some avian veterinarians have suggested that the bevel tip on certain endotracheal tubes may cause focal irritation and that any movement of the tube could damage the trachea. (3) Similar to the findings in this report, the authors reporting most cases of tracheal stenosis have not found evidence of erosion or necrotizing tracheitis so much as proliferation of granulation tissue and fibrosis. (3,4,15) In macaws and Amazon parrots, the trachea narrows by approximately 45% past the glottis, and "deep intubation," or intubation with a tube that is too large for the bird's trachea may lead to segmental and circumferential mucosal trauma. (4) In this case, the fit and position of the endotracheal tube distal to the glottis could not be evaluated, because radiographs were not obtained on the macaw's initial visit.

Causes of tracheal stenosis unrelated to intubation include infectious disease, extramural compression, and neoplasia. (21,22) Bacterial tracheitis may result from lower airway disease, which was also a concern before obtaining radiographs, given this bird's history of regurgitation. (21) Tracheal infections with Aspergillus species are commonly documented. (21,22) Viral diseases, including poxvirus and herpesvirus, have been reported to cause pseudomembranous tracheitis. (21,23) No evidence of viral infection was seen histologically in this case, but viral disease as a predisposing factor cannot be ruled out.

This case is notable for the severity of the tracheal stenosis (involving nearly 1.7 cm of the tracheal lumen), the use of multiple treatment modalities, and sequential tracheal ring resections that resulted in the removal of 15 tracheal rings. Dilation of the stenosis was attempted after surgery with a 2.7-mm, 30-degree rigid endoscope and again with a Foley catheter. Each of these treatment modalities was initially successful at increasing the size of the tracheal lumen and alleviating clinical signs but was not successful long term, because intraluminal exuberant tissue formed within 3 days. This suggests that dilation without concurrent medical therapy may be insufficient to resolve tracheal stenosis or that repeated dilation of the stenotic tracheal segments is required.

Conservative management of tracheal stenosis, including balloon dilation and bougienage, has not been thoroughly explored in avian medicine. In children, endoscopic dilation may be used to treat low-grade tracheal stenosis, but multiple treatments are required over a period of months. (24) Concurrent medical therapies, such as the use of hyaluronic acid, collagen polyvinylpyrrolidone, and steroids, have been reported in dogs to aid in healing and prevent excessive fibrosis after tracheal resection and anastomosis. (25) One report describes treatment of tracheal stenosis in a blue and gold macaw by using endoscopically manipulated instruments to excise the fibrous membrane followed by topical steroids. In that case, the stenosis recurred once and was treated by using the same procedure. The bird remained clinically normal for at least 1 year after surgery Steroid therapy in birds is traditionally controversial but may be appropriate in patients with exuberant wound healing or fibrosis. Topical medical management by using anti-inflammatory drugs was not attempted in this case.

Removal of such an extensive segment of trachea has not been previously reported in psittacine birds, and although there was significant tension present when apposing the tracheal segments, the bird recovered well from the second surgical procedure and remained clinically normal 2 years after surgery. In total, 15 tracheal rings were removed during the 2 procedures, which suggests that the psittacine bird trachea has a large reserve capacity and that large segments may be resected. The largest segment previously resected was 12 tracheal rings from a mallard duck (Anas platyrhynchos), (26) but most case studies report removal of fewer than 5 rings. (6) In this case, the diameter of the proximal tracheal segment was significantly larger than that of the distal segment and had to be narrowed by ventral resection and re-apposition, which left the trachea with a more flattened appearance after anastomosis. Despite these complications, the macaw did well after surgery, and clinical signs related to upper airway disease have not recurred. This case shows the importance of treating large tracheal lesions that encompass as many as 10-15 tracheal rings with surgical resection and anastomosis, because remnant fibrotic or inflamed tracheal tissue may result in recurrent tracheal stenosis.

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Gwen Jankowski, DVM, Javier G. Nevarez, DVM, PhD, Hugues Beaufrere, Dr Med Vet, Wes Baumgartner, DVM, Scott Reed, DVM, Dipl ABVP, Thomas N. Tully, DVM, MS, Dipl ABVP (Avian), Dipl ECZM (Avian), Cheryl Hedlund, DVM, MS, Dipl ACVS, Geoff Hennig, DVM, MS, and Jennifer Huck, DVM

From the Department of Exotic Animal Medicine, Surgery and Pathology at Louisiana State University, School of Veterinary Medicine, Skip Bertman Dr, Baton Rouge, LA 70803, USA. Present address (Jankowski): Chicago Zoological Society, 3300 Golf Rd, Brookfield, IL 60513, USA.
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