A captive 7-year-old sexually intact female blue crane (Anthropoides paradiseus) weighing 3.7 kg (8.1 lb) was brought to the Department of Conservation Medicine at the International Crane Foundation because of acute respiratory distress. Initial physical examination revealed a clear glottis, dyspnea, mild cyanosis of the mucous membranes, and a bilateral decrease in respiratory sounds in the lungs and abdominal air sacs.
To allow further examination, anesthesia was induced with 5% isoflurane in oxygen (2 L/min) delivered via mask, endotracheal intubation was performed with a silicone cuffed endotracheal tube (internal diameter, 5.0 mm), and anesthesia was maintained with isoflurane, with intermittent positive pressure ventilation provided. The endotracheal cuff was not inflated. Rigid endoscopya,b of the trachea and oropharynx revealed no abnormalities. However, the tracheoscope was only 25 cm long, limiting visualization of the full trachea. Right lateral radiography revealed a mineral opacity foreign body causing deformation of the distal cervical portion of the trachea (Figure 1).
Right lateral radiographic view of a blue crane (Anthropoides paradiseus) evaluated because of sudden signs of respiratory distress. A mineral opacity foreign body (arrow) is seen causing deformation of the distal cervical portion of the trachea. The crane's head is to the bottom of the image.
Citation: Journal of the American Veterinary Medical Association 256, 11; 10.2460/javma.256.11.1262
Given the radiographic findings, tracheotomy was pursued to remove the foreign body. For the procedure, the crane was positioned in dorsal recumbency and the ventral cervical region was aseptically prepared. An approximately 3-cm incision was made into skin overlying the position of the intratracheal foreign body. The subcutaneous tissue was bluntly dissected, exposing the trachea. A transverse, full-thickness tracheal incision was made incorporating 50% of the diameter of the trachea, and a rock was identified within the lumen of the trachea. Stay sutures of 2-0 polypropylenec were placed around the adjacent tracheal ring on each side of the tracheotomy site. Several attempts were made to remove the rock with forceps without success. A 22-gauge, 2.5-cm needle was inserted through the trachea caudal to the rock to prevent the rock from falling farther down the trachea while the crane was repositioned to make a second incision, but the rock slipped past the needle and farther down the trachea. A second tracheotomy site was created 3 cm caudal to the original site in a similar fashion to the first procedure, and the rock was successfully removed with Hartmann alligator forceps. Both tracheotomy sites were closed in a full-thickness simple interrupted pattern with absorbable 4-0 polyglyconate.d The subcutaneous and skin layers were closed in a simple cutaneous pattern with absorbable 4-0 polyglyconate.e
Following surgery, the crane received meloxicamf (0.54 mg/kg [0.245 mg/lb], IM), ceftiofur crystalline free acidg (21.6 mg/kg [9.82 mg/lb], SC), and lactated Ringer solutionh (150 mL, SC). The crane resumed sternal recumbency within 5 minutes after extubation and was returned to its enclosure within 2 hours after surgery had begun.
The next day during attempts to capture the crane for reevaluation, it collided with the enclosure wall. On capture, the crane was manually restrained and noted to have moist rales. Oral examination revealed fresh blood originating from the trachea. The crane's head was lowered, and an estimated 5 mL of frank blood drained from the glottis. The surgical site appeared to be intact, with no evidence of skin suture dehiscence. The source of the fresh blood was undetermined, but the blood was suspected to be from internal bleeding at the surgical site due to handling. The crane received meloxicam (0.54 mg/kg, IM) and lactated Ringer solution (100 mL, SC) prior to release into its exhibit space. Itraconazolei (10 mg/kg [4.5 mg/lb], PO, q 24 h for 14 days) was prescribed for prophylactic antifungal treatment as well as piroxicamj (1 mg/kg [0.45 mg/lb], PO, q 24 h for 7 days).
Over the next 7 weeks, keepers reported observing progressive respiratory signs consisting of voice changes, open-mouth breathing, raspy breaths, and coughing. Because of the worsening clinical signs, a CBC and serum biochemical analysis were performed (51 days after surgery), revealing mild leukocytosis (33.3 × 103 WBCs/L [global species reference interval, 3.1 × 103 to 29.09 × 103 WBCs/L]) and no biochemical abnormalities. No obvious external abnormalities were appreciated at the previous surgical site, and no discharge was observed from the glottis.
The crane was transported to the University of Wisconsin-Madison School of Veterinary Medicine for advanced imaging of the respiratory tract. For the procedure, it was anesthetized as described previously. A 22-gauge IV catheter was placed in the left medial metatarsal vein for IV fluid and medication administration. Full-body, transverse plane CTk images collimated to 0.625-cm-thick slices were obtained. Images were reformatted by use of a high-frequency detail soft tissue algorithm. Sagittal and dorsal plane reconstructions were made from the soft tissue detail volumes. The tracheal lumen appeared bilaterally compressed immediately cranial to the coelomic cavity inlet, resulting in a substantially reduced cross-sectional area over a distance of approximately 3.5 cm (Figure 2). A few focal discontinuities along the ventral aspect of the tracheal rings at the level of the stenosis allowed for overriding fragments of the trachea. The remaining aspects of the trachea appeared unremarkable, with continuous, circular tracheal rings surrounding a uniform luminal cross-sectional area. No other abnormalities were appreciated in the remainder of the upper and lower respiratory systems.
A 3-D reconstructed sagittal CT image of the crane in Figure 1 showing tracheal stenosis. The cranial aspect of the crane is oriented to the left of the image, and the caudal aspect is located on the right. The stenotic tracheal area (arrow) resulted in a substantial reduction in luminal diameter at the site where tracheotomy had previously been performed to remove the rock.
Citation: Journal of the American Veterinary Medical Association 256, 11; 10.2460/javma.256.11.1262
The crane was positioned in right lateral recumbency for placement of an air sac cannula prior to tracheoscopic evaluation. The feathers over the left lateral aspect of the coelomic cavity were plucked. One-inch white tapel was placed at the borders of the caudalmost left rib, the flexor cruris medialis muscle, and the pubic bone, and the skin within these borders was aseptically prepared. The bevel of an 18-gauge, 1.5-inch needle was used to make a 1-cm skin incision at the center of the triangle bordered by the tape, and a sterile Kelly hemostatic forceps was used to bluntly dissect into the caudal left abdominal air sac. An endotracheal tube (internal diameter, 6.0 mm) was placed into the air sac and sutured to the skin with 3-0 polyglyconatee in a purse-string pattern. Isoflurane (2% to 3%) in oxygen was delivered into the caudal abdominal air sac for the tracheoscopy procedure.
Tracheoscopy was performed by use of a flexible fiberoptic bronchoscopem (diameter, 3.1 mm). Substantial edema and erythema of the tracheal mucosa were visible at the stenotic site. A portion of suture material was seen emerging from the center of the stenosis, and the tracheal diameter appeared reduced to 10% of the normal luminal diameter at the affected site (Figure 3).
Tracheoscopic image of the crane in Figure 1 showing tracheal stricture at the tracheotomy site. Suture material from the previous surgery is visible within the tracheal lumen, the diameter of which has been reduced to 10% of the normal tracheal diameter at the affected site.
Citation: Journal of the American Veterinary Medical Association 256, 11; 10.2460/javma.256.11.1262
Owing to the poor prognosis for long-term survival, excision of the stenotic portion of the trachea was elected. The crane was positioned in dorsal recumbency, and the ventral neck region was aseptically prepared for TRA. A 6-cm midline incision was made over the distal cervical portion of the trachea. A combination of sharp and blunt dissection was used to separate the superficial neck muscles and scar tissue overlying the trachea. Substantial fibrosis and adhesions surrounding the trachea made visualization of the jugular vein, recurrent laryngeal nerve, and carotid sheath difficult. After much of the fibrous material was removed, the left and right recurrent laryngeal nerves were seen firmly adhered to the lateral aspects of the trachea. A curved mosquito hemostatic forceps was used to bluntly dissect the nerves away from the trachea. An approximately 3-cm-long portion of trachea was discolored and narrowed, with associated suture material from the previous tracheotomy visible within the scar tissue (Figure 4). An approximately 4-cm length of trachea was resected transversely between the tracheal rings with a No. 11 scalpel blade. Simple interrupted sutures of 4-0 polyglyconated were preplaced at 2- to 3-mm intervals around the entire circumference of the trachea around the tracheal ring adjacent to the site of anastomosis. Four additional tension-relieving, interrupted sutures of 4-0 polyglyconate were placed across the anastomosis, incorporating the second closest tracheal ring cranial and caudal to the anastomosis site.
Photographs showing the TRA procedure performed in the crane of Figure 1. A—The stenotic tracheal region from the previous tracheotomy procedure is exposed. The tissue is necrotic and discolored. Notice the presence of stay sutures of 2-0 polypropylene, which were used to elevate the trachea. B—A transverse incision is performed to remove the affected portion of tracheal tissue. C—The excised portion of trachea showing luminal compromise from the previous surgery along with the presence of polyglyconate suture. D—Single interrupted sutures of 4-0 polyglyconate are placed at approximately 4- to 5-mm intervals prior to closure.
Citation: Journal of the American Veterinary Medical Association 256, 11; 10.2460/javma.256.11.1262
The subcutaneous space was closed in a simple continuous pattern with 4-0 glycomer 631,n and the skin was apposed in a buried continuous subcuticular pattern. The crane received lactated Ringer solution (5 mL/kg/h [2.3 mL/lb/h], IV), cefazolino (20 mg/kg [9.1 mg/lb], IV, q 90 min), and meloxicam (0.54 mg/kg, IM) during surgery and ceftiofur crystalline free acid (21.6 mg/kg, SC) after surgery. On completion of the TRA procedure, anesthesia was discontinued, and the air sac cannula was removed once the crane was observed to be breathing normally. Piroxicam (1 mg/kg, PO, q 24 h for 14 days) and itraconazole (10 mg/kg, PO, q 24 h for 14 days) were prescribed.
The crane recovered without complication and was returned to its usual exhibit to limit stress. It was placed in an outdoor run remote from barrier fencing and walls to avoid traumatic impact injury. The crane's respiratory rate and effort markedly improved immediately after surgery. Despite a raspy quality to its voice, the crane was able to vocalize and unison call (a duet performed by a pair of cranes to strengthen their bond and protect their territory).
Histologic examination of the resected tracheal segment revealed mild to moderate inflammation in the lamina propria as indicated by the presence of heterophils, lymphocytes, and plasma cells. The ciliated respiratory epithelium appeared generally mature. At the site of stricture, multiple coalescing nodules of granulomatous inflammation (comprised of heterophils, macrophages, multinucleated macrophages, and peripheral lymphocytes and plasma cells) were evident in the surrounding soft tissue, interspersed between woven bone trabeculae (Figure 5). Central zones of necrosis were noted. Within the largest nodule of inflammation were coccobacilli and septate branching fungal hyphae. Methenamine silver staining confirmed that the fungal hyphae were septate and branching, morphologically consistent with Aspergillus spp. Gram staining revealed a predominance of gram-negative rods admixed with fewer gram-positive cocci. Ovoid structures with a light-brown refractile capsule suggestive of parasite ova were also present within the largest granuloma. These structures had a small amount of granular material within the lumen. A possible operculum was identified at the edge of one of the possible ova.
Photomicrographic images of sections of tracheal tissue resected from the crane in Figure 1. A—Notice the marked narrowing of the tracheal lumen (arrow) and distortion of tracheal rings (asterisks) by a regionally extensive granuloma (outlined). B—Notice that within the granuloma are colonies of coccobacillary bacteria (asterisk), septate branching fungal hyphae (arrows), and ovoid structures with a light-brown refractile capsule (arrowheads), which were suspected of being parasite ova. C—Notice the branching fungal hyphae (arrows) and ovoid refractile structures (arrowheads). H&E stain in panels A and B, and methenamine stain in panel C; bar = 60 μm in all panels.
Citation: Journal of the American Veterinary Medical Association 256, 11; 10.2460/javma.256.11.1262
Owing to the histopathologic findings, terbinafine hydrochloridep (16.9 mg/kg [7.7 mg/lb], PO, q 24 h for 7 days) was also prescribed. After 14 days of oral medication administration, the crane refused to accept any medications hidden in preferred food items and treatments were discontinued. At the 12-week recheck evaluation, no abnormalities were appreciated and the site of TRA had completely healed.
Discussion
To the authors’ knowledge, the present report represents the first report of successful TRA in a bird of the order Gruiformes. Successful TRA procedures have been reported for other avian species, including a saddle-billed stork (Ardeola ibis), blue-billed curassow (Crax alberti), secretary bird (Sagittarius serpentarius), pied Imperial pigeon (Ducula bicolor), mallard duck (Anas platyrhynchos), white-winged wood duck (Asarcornis scutulata), hybrid goose (Anser sp), blue and gold macaws (Ara ararauna), red-tailed black cockatoo (Calyptorhynchus banksii banksii), and red-tailed hawk (Buteo jamaicensis).1–9 Tracheal resection and anastomosis was attempted in a West African crowned crane (Balearica pavonina) with tracheal stenosis but was not successful.1
The most common reported cause of tracheal stenosis in birds is inflammation secondary to damage to the tracheal mucosa caused by intubation.1,2 Other causes such as neoplasia, external trauma, and inhaled foreign objects have also been reported.1,9–11 After the crane of the present report was released following the original tracheotomy procedure, it collided with its enclosure wall. This impact and a second impact the following day were suspected to have contributed to suture failure and tissue damage at the original surgery site. In addition, the necrotic tracheal tissue was confined to the space between the 2 previous tracheotomy sites. Iatrogenic damage to the segmental tracheal blood supply likely contributed to the necrotic tracheal tissue along with focal pressure from the rock foreign body. Infectious microorganisms found on histologic examination likely represented secondary infection.
Both conservative and surgical options are available for treatment of tracheal stenosis in veterinary species. Common treatment options include balloon catheter dilation, endoscopic laser ablation, stent placement, and TRA. Unlike the mammalian trachea, the avian trachea is composed of closely spaced complete tracheal rings, and the luminal diameter tapers caudally in certain species such as cranes.12 Balloon dilation and endoscopic laser ablation typically provide only temporary relief of clinical signs, and bougienage may cause iatrogenic damage to the tracheal rings in birds.6 Tracheal stent placement is also approached cautiously in avian species because of the potential for complications associated with the relatively more rigid tracheal anatomy. However, stent placement may be considered in birds with tracheal stenosis that is refractory to medical treatment or for tracheal lesions that are too large for TRA.13 A nitinol wire stent was used to treat tracheal stenosis in an eclectus parrot in a previous report,14 but that parrot continued to have clinical signs after stent placement and tracheomalacia was noted at postmortem examination. Given the abnormal tracheal architecture and substantial amount of necrotic tissue at the affected site in the crane of the present report, TRA was considered the most reasonable option.
Tracheal resection and anastomosis can be performed with various surgical approaches and techniques, but end-to-end anastomosis, as was used in the crane, has been the most commonly reported and successful approach.1 The most common complication associated with TRA is formation of a new stricture at the surgical site.7 With the aim of perfect tissue apposition, application of tension-relieving sutures and use of minimally reactive suture can help prevent this complication.15 In the crane of the present report, polyglyconate suture was used to close the tracheal anastomosis. Polydioxanone suture has been more commonly reported for TRA owing to its minimal tissue reactivity, strength, and flexibility.16 Whereas polyglyconate and polydioxanone materials have similar suture characteristics with minimal tissue reaction in dogs and cats, these characteristics have not been compared within avian species.15 We suspect that polyglyconate would be a suitable suture material for TRA in cranes given the lack of postoperative complications observed in the present case.
Another commonly reported complication of TRA is injury to the recurrent laryngeal nerves because of their close proximity to the trachea.17 Fortunately, in birds, the recurrent laryngeal nerves do not innervate the larynx but, rather, portions of the esophagus and crop as well as the tracheal and syringeal muscles. Therefore, damage to the recurrent nerves does not result in laryngeal paralysis but may cause vocal changes.17 In the crane of the present report, transection of the recurrent laryngeal nerve or nerves was unlikely to have occurred because no cross-sectional areas of nerve were identified on histologic examination. The noted changes in vocalization following surgery were suspected to have been from iatrogenic trauma to the nerve or nerves during surgery or from previous scar tissue formation. Despite audible changes in the crane's voice, the bird was still able to unison call and no behavioral abnormalities were observed.
Histologic examination revealed a substantial amount of inflammation in the resected tracheal segment with associated bacteria and branching fungal hyphae consistent with Aspergillus spp. Localized growth of Aspergillus spp associated with abnormal tracheal tissue has been previously reported in birds with tracheal stenosis.2,5 We surmise that the tracheal stenosis and resulting change in airflow predisposed the crane to developing Aspergillus growth at the stricture site. Ovoid structures that were suspected to be parasite ova with potential opercular capsules were also found within granulomas at the affected site. Although parasitic diseases of the trachea are not commonly reported in companion avian medicine, they are more commonly reported in wild birds or those housed outdoors.18 Full identification of the type of parasite was not possible; however, a capsule that resembled a trematode ovum was observed on a cut section.19 The crane's outdoor enclosure had a water feature with mollusks and amphibians present, and those animals were the likely intermediate host for the suspected trematode ova that were observed.19
In a case report10 similar to the present one, a whooping crane (Grus americana) aspirated a kernel of corn that was surgically removed. Aspirated foreign bodies represent a challenge in crane species because of their unique respiratory anatomy. Not only do cranes have an elongated cervical tracheal portion owing to their long necks, but they also have extensive coiling of the trachea within the sternum.10,20 This coiling within a bony structure is an area where foreign bodies can lodge and become difficult to remove without surgery. Ideally, tracheal foreign bodies are removed endoscopically, which is less invasive. Endoscopic removal was not possible in the crane because a flexible endoscope of sufficient length was not available at the time of initial evaluation. Furthermore, there was concern that the foreign body was lodged in soft tissue mucosa within the trachea, which would have made endoscopic retrieval more difficult or possibly resulted in substantial damage to the tracheal mucosa during endoscopic removal.
In the present report, we have described a case of successful emergency tracheotomy and subsequent TRA in a blue crane that developed tracheal stenosis after tracheotomy. Despite the unique upper respiratory anatomy of cranes, it appears that TRA may be appropriate for the treatment of tracheal stenosis lesions within the cervical tracheal region.
Acknowledgments
No third-party funding or support was received in connection with this case or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.
ABBREVIATIONS
| TRA | Tracheal resection and anastomosis |
Footnotes
8672.431 2.7-mm 5-degree Panoview Plus sinuscope, Richard Wolf Medical Instruments, Vernon Hills, Ill.
4046 fiber light projector, Richard Wolf Medical Instruments, Vernon Hills, Ill.
Prolene, Ethicon, New Alexandria, Pa.
4-0 Maxon, Covidien, Minneapolis, Minn.
3-0 Maxon, Covidien, Minneapolis, Minn.
Loxicam, Norbrook Inc, Lenexa, Kan.
Excede, Zoetis, Parsippany, NJ.
Baxter, Deerfield, Ill.
Ascend Laboratories LLC, Parsippany, NJ.
Nivagen Pharmaceuticals Inc, Sacramento, Calif.
LightSpeed Utra 8-slice, GE, Fairfield, Conn.
Covidien, Minneapolis, Minn.
Bronchoscope, 3.1 mm, Karl Storz, Tuttlingen, Germany.
Biosyn, Covidien, Minneapolis, Minn.
West-Ward Pharmaceutical Corp, Cherry Hill, NJ.
Cipla USA Inc, Sunrise, Fla.
References
1. Sykes JM IV, Neiffer D, Terrell S, et al. Review of 23 cases of postintubation tracheal obstructions in birds. J Zoo Wildl Med 2013;44:700–713.
2. Evans A, Atkins A, Citino SB. Tracheal stenosis in a blue-billed currasow (Crax alberti). J Zoo Wildl Med 2009;40:373–377.
3. Ludwig C, Lueders I, Schmidt V, et al. Tracheal resection in a secretary bird (Sagittarius serpentarius) with granulomatous, foreign-body induced tracheitis. J Avian Med Surg 2017;31:308–313.
4. Guzman DS, Mitchell M, Hedlund CS, et al. Tracheal resection and anastomosis in a mallard duck (Anas platyrhynchos) with traumatic segmental tracheal collapse. J Avian Med Surg 2007;21:150–157.
5. Clippinger TL, Bennett RA. Successful treatment of a traumatic tracheal stenosis in a goose by surgical resection and anastomosis. J Avian Med Surg 1998;12:243–247.
6. De Matos RE, Morrisey JK, Steffey M. Postintubation tracheal stenosis in a blue and gold macaw (Ara ararauna) resolved with tracheal resection and anastomosis. J Avian Med Surg 2006;20:167–174.
7. Jankowski G, Nevarez JG, Beaufrere H, et al. Multiple tracheal resections and anastomoses in a blue and gold macaw (Ara ararauna). J Avian Med Surg 2010;24:322–329.
8. Doneley RJ, Raidal SR. Tracheal resection and anastomosis in a red - tailed black cockatoo (Calyptorhynchus banksii banksii). Aust Vet J 2010; 88:451–454.
9. Monks DJ, Zsivanovits HP, Cooper JE, et al. Successful treatment of tracheal xanthogranulomatosis in a red-tailed hawk (Buteo jamaicensis) by tracheal resection and anastomosis. J Avian Med Surg 2006;20:247–252.
10. Howard PE, Dein FJ, Langenberg JA, et al. Surgical removal of a tracheal foreign body from a whooping crane (Grus americana). J Zoo Wildl Med 1991;22:359–363.
11. Lennox AM. Management of tracheal trauma in birds, in Proceedings. 25th Annu Conf Assoc Avian Vet 2004;339–343.
12. Doneley R. Clinical anatomy and physiology. In: Doneley R, ed. Avian medicine and surgery in practice: companion and aviary birds. London: Manson Publishing, 2010;22.
13. Henry-Guyot E, Langlois I, Lanthier I. Tracheal collapse in a Pekin duck (Anas platyrhynchos domestica). J Avian Med Surg 2016;30:364–367.
14. Mejia-Fava J, Holmes SP, Radlinsky M, et al. Use of a nitinol wire stent for management of severe tracheal stenosis in an eclectus parrot (Eclectus roratus). J Avian Med Surg 2015;29:238–249.
15. Fossum TW. Surgery of the upper respiratory system. In: Fossum TW, ed. Small animal surgery. 5th ed. Maryland Heights, Mo: Mosby, 2019;833–849.
16. Bennett RA, Yaeger MJ, Trapp A. Histologic evaluation of the tissue reaction of five suture materials in the body wall of rock doves (Columbia livia). J Avian Med Surg 1997;11:175–182.
17. Guzman DS. Avian soft tissue surgery. Vet Clin North Am Exot Anim Pract 2016;19:133–157.
18. Morrisey JK. Diseases of the upper respiratory tract of companion birds. J Exot Pet Med 1997; 6:195–200.
19. Huffman JE. Trematodes. In: Atkinson CT, Thomas NJ, Hunter DB, eds. Parasitic diseases of wild birds. Ames, Iowa: Blackwell, 2008;223–245.
20. Schwarz T, Kelley C, Pinkerton ME, et al. Computed tomographic anatomy and characteristics of respiratory aspergillosis in juvenile whooping cranes. Vet Radiol Ultrasound 2016;57:16–23.
