Diagnosis and Treatment of Dynamic Collapse of the Cricotracheal Ligament in Thoroughbred Racehorses Padraig G. Kelly, MVB, Diplomate ECVS, and Patrick J. Pollock, BVMS, CertES(Soft Tissue), Diplomate ECVS Weipers Centre Equine Hospital, School of Veterinary Medicine, University of Glasgow, Glasgow, UK
Corresponding Author Padraig G. Kelly, MVB, Diplomate ECVS, Weipers Centre Equine Hospital, School of Veterinary Medicine, University of Glasgow, 464 Bearsden Road, Glasgow G611QH, UK. E‐mail: [email protected] Submitted February 2012 Accepted July 2012 DOI:10.1111/j.1532-950X.2014.12262.x
Objective: To describe (1) diagnosis of dynamic collapse of the cricotracheal ligament in a group of horses and (2) treatment and outcome of affected horses. Study Design: Retrospective case series. Animals: Thoroughbred horses (n ¼ 8). Methods: Of 600 over ground dynamic endoscopic examinations performed, 8 Thoroughbred horses had cricotracheal ligament collapse (CTLC); 5 were 2 years old and in early training and 2 were mature horses in full work. CTLC was diagnosed if circumferential collapse of the cricotracheal ligament was identified during exercise. Seven horses had repeat endoscopic examination. Two horses unresponsive to conservative management were treated surgically. Results: Multiple abnormalities of the upper portion of the respiratory tract were identified along with CTLC in all five 2‐year‐old horses and resolution of CTLC was observed after treatment for upper airway inflammation. No concurrent respiratory abnormality was identified in the 2 mature horses. Surgical reduction of the cricotracheal space and imbrication of the cricotracheal ligament of these 2 horses resulted in resolution of clinical signs of CTLC. Conclusions: CTLC is a rare cause of dynamic obstruction in Thoroughbred racehorses. Resolution may occur after adaptation to training and after inflammation of the respiratory tract is resolved, but for horses with persistent CTLC, surgical reduction of the cricotracheal space and imbrication of the cricotracheal ligament may result in resolution of clinical signs.
The cricotracheal ligament (ligamentum cricotracheale) is a dense, elastic ligament that connects the caudal border of the cricoid cartilage to the cranial border of the 1st tracheal ring.1 The cricotracheal space is readily palpable in horses because it is wider than any of the interannular ligaments of the trachea and is considerably less tense. The ligament can be readily pushed into the airway, allowing it to be seen during endoscopic examination of the upper airway. Some authors have speculated that excessive length and slackness of the ligament, combined with the sub‐atmospheric inspiratory airway pressures that occur during high‐speed exercise may lead to collapse of the ligament into the airway.2–5 Collapse of the cricotracheal ligament (CTLC) may be so severe that the reduced diameter of the airway lumen results in abnormal respiratory noise and poor performance.2 The condition has only been described in Thoroughbreds and is thought to result from a congenitally, abnormally wide space between the cricoid cartilage and the 1st tracheal ring or as the result of abnormally increased negative pressure within the trachea.2,3 We are unaware of reports of this disorder being diagnosed during dynamic, endoscopic examination under normal exercise conditions.
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We report the clinical presentation and outcome of 7 Thoroughbred horses with CTLC identified during serial, dynamic, endoscopic examinations of the upper airway during high‐speed exercise and report outcome after surgical treatment in 2 horses refractory to conservative management.
MATERIALS AND METHODS Case Selection Medical records (2008–2011) of 600 Thoroughbred racehorses presented for dynamic endoscopic examination of the upper airway were reviewed. Horses with dynamic CTLC identified during dynamic endoscopic examination were identified and only those that had 1 or more repeat dynamic, endoscopic examinations were included in the study. Dynamic Endoscopic Examination of the Upper Airway Dynamic, over‐ground, endoscopic examination was performed using a dynamic, respiratory endoscope DRS1
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
Kelly and Pollock
(Optomed, Les Ulis, France). Examination was carried out in accordance with the horse’s fitness and training regimen at the time of examination, ensuring the test resulted in fatigue of each horse. Horses were fitted with the custom saddle‐cloth, containing the recording medium and battery, fitted under a saddle. A nose twitch was applied to the horse for placement of the DRS. The insertion tube of the endoscope was placed through the ventral meatus of the right nasal cavity into the nasopharynx and positioned just rostral to the epiglottis allowing a clear view of the larynx and caudal portion of the soft palate. Initial positioning and attachment to the bridle was crucially important to ensure the image remained in the center of the screen during exercise. After the DRS was positioned, it was retroflexed at the level of the right nostril and attached to a custom bridle by using clips and cable ties. After the DRS was adequately positioned and secured, the rider mounted the horse. Correct positioning of the image was confirmed, and video recording and a wrist‐mounted GPS device (Garmin Forerunner 305, Olathe, KS) were activated simultaneously. DRS The DRS consisted of 5 distinct parts: (1) a semi‐rigid, malleable insertion tube (9.8‐mm diameter) with a head section containing a light‐emitting diode (LED) light‐source, bending section, and lens‐cleaning system; (2) bridle with securing mounts which fitted over standard tack; (3) a 3‐kg processor containing a battery with 120 minutes of life, a light source with 2 light levels, a wireless transmitting device, and recording medium (i.e., a secure digital micro USB in mp4 HD format) all contained within a customized saddle pad; (4) a pump, tubing, and bottle for flushing (1.5 mL flush every 30 seconds); and (5) PVC video‐display, wireless, control box operating on battery or AC with an effective range of 500 m in optimal conditions. The selected color temperature (4000– 6000°K) provided high‐quality images. A remote control with playback, stop, and start functions initiated the recordings.
Dynamic Collapse of the Cricotracheal Ligament
Variables Recorded The following variables were recorded: history of respiratory disease and treatment; tack used; weather conditions; whether the horse was ridden alone or with others; whether the jockey observed any abnormalities during exercise (particularly abnormal noises); and any complications with the equipment, horse, or rider that occurred during testing. Speed, distance, and altitude were recorded while the horse exercised, by using a GPS receiver (Garmin Forerunner 305) mounted on the wrist of the rider. The GPS receiver was synchronized with the DRS recording and collected data at intervals of 1 Hz. Endoscopic images were reviewed after testing, at normal playback speed, in slow motion, and if necessary, frame by frame, by 2 veterinary surgeons (P.J.P. and P.K.) blinded to the horse’s history. Abnormalities of the upper airway were identified, described, and entered into a database (Excel 2003). Data obtained from the GPS were downloaded via a dedicated software program (Garmin Training Center) and a graph of elevation and speed achieved was recorded. If abnormalities were identified, speed and position of the horse in the exercise test were recorded; alteration in speed associated with the occurrence of the abnormality was assessed and recorded. The percentage CTLC obstruction was calculated using measurements obtained from digital image editing software (Adobe Creative Suite 5.5; Adobe Systems, Inc., San Jose, CA).
Diagnostic Criteria CTLC was diagnosed when circumferential collapse of the cricotracheal ligament was evident during dynamic endoscopic examination (Fig 1). Accurate positioning of the endoscope is required to allow a circumferential view of the proximal aspect of the trachea. Where suboptimal positioning resulted in a portion of the proximal trachea being obscured, a positive diagnosis of CTLC could not be achieved.
Figure 1 Still images of the upper airway acquired during over‐ground dynamic examination demonstrating circumferential collapse of the cricotracheal ligament in 2 horses.
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
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Surgical Procedure For 2 horses, CTLC was reported on more than 1 endoscopic examination and was associated with a loud inspiratory noise and reduction in speed during maximal exercise. These 2 horses were treated surgically. Each was sedated with romifidine (0.08 mg/kg intravenously [IV]) and morphine sulfate (0.1 mg/kg IV), and anesthesia was induced with ketamine (2.2 mg/kg IV) in combination with diazepam (0.05 mg/kg IV) and maintained with a mixture of isoflurane in oxygen delivered via a circle system. Horses were positioned in dorsal recumbency, the hair clipped, and skin prepared for aseptic surgery. A 10‐cm, longitudinal, skin incision was created on the ventral midline from the level of the caudal aspect of the thyroid cartilage to the 3rd tracheal ring. The incision was extended through the subcutaneous tissue and paired sternohyoideus and omohyoideus muscles, by sharp and blunt dissection, to expose the ventral half of the 1st tracheal ring and the cricoid cartilage. The cricotracheal ligament was identified between the caudal aspect of the cricoid cartilage and the 1st tracheal ring, grasped with Allis tissue forceps, and everted. An endoscope was passed to the level of the cricoid cartilage to allow observation of the proximal aspect of the trachea. While ensuring penetration of the tracheal mucosa did not occur, the cricoid cartilage was sutured to the 1st tracheal ring using 3 polyethylene‐based, braided sutures (Fiberwire1, CCS‐1, Arthrex, Naples, FL). The sutures were pre‐placed in a 2 bite double‐loop from caudal to cranial on the caudal margin of the ring of the cricoid cartilage and then from cranial to caudal on the cranial margin of the 1st tracheal ring. Two sutures were placed laterally, and 1 suture was placed on the midline (Fig 2). The sutures were tightened and tied after elevating the head to a vertical position. This resulted in the 1st tracheal ring lying in close apposition to, or partially beneath, the caudal aspect of the cricoid cartilage. The everted cricotracheal membrane was then sutured to the 1st tracheal ring using 3 metric polydioxanone placed in a simple‐ continuous pattern. The incision in the musculature was closed using 3 metric polydioxanone placed in a simple‐continuous pattern, the subcutaneous tissue was closed using the same suture placed in a similar pattern, and the skin incision was closed with 3.5 metric polydioxanone placed in a cruciate pattern. A stent bandage was sutured over the closed incision with 3.5 metric polydioxanone placed in a cruciate pattern. All horses were administered procaine penicillin G (22,000 U/kg intramuscularly [IM] twice daily) and gentamicin (6.6 mg/kg IV once daily) for 72 hours and then trimethoprim‐ sulfonamide (30 mg/kg orally, twice daily) for 5 days. Phenylbutazone (2.2 mg/kg orally, twice daily) was administered for 5 days. Horses were fed from shoulder height, and trainers were advised to continue this practice indefinitely.
RESULTS Eight horses were diagnosed with CTLC, but results of multiple endoscopic examinations were available for only 7 horses, all Thoroughbred racehorses. Five were 2 years old,
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Figure 2 Schematic representation of the surgical procedure to reduce the cricotracheal space and imbricate the cricotracheal ligament.
1 was 4 years old, and 1 was 6 years old. Four were examined while they galloped on an all‐weather surface (TapetaTM Footings, Inc., North East, MD), 2 were examined while they galloped on sand, and 1 was examined while galloping on grass. All horses were tacked in a standard manner. No horse had a history of lower respiratory disease or respiratory surgery, but 3 horses were reported to make abnormal respiratory noise when they exercised. The abnormal noise created by 1 horse was described as a gurgling noise and the other 2 horses made a loud inspiratory noise that became progressively worse during exercise. In all cases dynamic obstruction was gradual in onset and was noted to be progressive as exercise continued, being most severe at the point of maximal exercise intensity. A sudden decline in speed was not noted by the jockeys or from GPS data during any examination. Assessment of the degree of obstruction using digital image editing software (Adobe Creative Suite 5.5; Adobe Systems, Inc.) demonstrated that the degree of obstruction was between 36% and 52% of the area of the tracheal lumen. No correlation between horse age and degree of obstruction was noted. No complications occurred during the examinations. All 2 year olds with CTLC were in the early stages of training and were examined initially while they galloped twice
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
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Dynamic Collapse of the Cricotracheal Ligament
over a distance of 4–6 furlongs. All horses were reported by the trainer to be performing below expected levels. All 2‐year‐old horses were found, during dynamic endoscopic examination of the upper airway to have multiple respiratory abnormalities, including CTLC. All had grade 3 or greater pharyngeal lymphoid hyperplasia (PLH), 3 had mild bilateral axial deviation of the aryepiglottic folds (ADAF), 3 had mild bilateral vocal cord collapse (VCC), and 2 had intermittent dorsal displacement of the soft palate (IDDSP). All of the 2‐year‐old horses were treated by administration of a non‐ steroidal, anti‐inflammatory (phenylbutazone 2.2 mg/kg orally twice daily) for 7 days and were kept in training during treatment. During dynamic endoscopic examination, repeated for each of the 2‐year‐old horses during two 6 furlong gallops 6 weeks after the 1st examination, CTLC was no longer identified in 4 horses. Of these 4 horses, no clinical abnormalities were identified in 3 horses; however, 1 horse was again diagnosed with IDDSP. Abnormalities found at the 2nd examination of the other 2‐year‐old horse were similar to those found at the 1st examination and included grade 3 PLH, mild bilateral ADAF, IDDSP, CTLC, and a gurgling noise. During a third examination conducted 6 weeks after the 2nd examination, no dynamic abnormalities of the upper portion of the respiratory tract were identified and PLH was grade 2 and considered within normal limits (Table 1). One horse that had CTLC was 4 years old, and another was 6 years old. Both were in full work at the time of initial examination and were galloped to fatigue on a circular gallop over 2.6 and 3 miles respectively. Clinical signs in these horses were not identified in early training but at the time of presentation poor performance and a loud progressive inspiratory noise were consistently observed by the trainer. CTLC was the only abnormality identified in the 6‐year‐old horse, but the 4‐year‐old horse developed IDDSP at the end of exercise when pulling up. Both horses were observed to make a loud inspiratory noise during dynamic respiratory examination. During repeat examination, performed at 8 and 12 weeks, respectively, both horses made a loud inspiratory noise and CTLC was the only endoscopic abnormality of the URT noted.
DISCUSSION CTLC identified in all of the 2‐year‐old horses during dynamic endoscopy was no longer observed after reduction of PLH to a severity not considered clinically important (grade 2). Accompanying respiratory abnormalities noted during the 1st examination had also resolved, except for IDDSP, which was noted in 1 horse. Both horses that had surgical treatment for CTLC had resolution of clinical signs and CTLC during dynamic endoscopy of the upper portion of the respiratory tract that was performed after the horses were back in full training. Dynamic collapse of the upper portion of the respiratory tract is a frequent cause of poor performance in the equine athlete.6 Dynamic endoscopy of the upper portion of the respiratory tract, performed with the horse on a high‐speed treadmill or running over ground, has allowed detailed description of common causes of dynamic collapse of the airway.7 CTLC is a rare cause of dynamic obstruction of the respiratory tract of horses2–4 and to our knowledge, prevalence, diagnosis under normal exercising conditions, and definitive resolution of CTLC after treatment have not been described. CTLC is diagnosed when the cricotracheal ligament is seen to collapse circumferentially into the airway resulting in considerable narrowing of the airway. Central positioning of the endoscope is essential to accurately diagnose CTLC because if an oblique image is obtained movement of the 1st tracheal ring in relation to the caudal aspect of the cricoid at high speed exercise may give the impression of CTLC, leading to a false positive diagnosis.
Results of Dynamic Endoscopic Examination of Five 2‐Year‐Old Horses
Table 1
No.
Both horses had surgical treatment, as described above. Resolution of abnormal respiratory noise was reported by the trainer in both cases and no abnormal respiratory noise, or abnormalities of the upper airway were identified during dynamic endoscopic examination performed after the horses had returned to full training. In 1 horse this was performed on 1 occasion 6 months after surgery and in the other horse on 2 occasions (6 and 18 months after surgery; Fig 3). Both horses raced postoperatively.
Age
Sex
1
2
C
2 3 4
2 2 2
C C C
5
2
F
First Endoscopic Examination CTLC, ADAF, VCC, IDDSP, grade 3 PLH CTLC, grade 3 PLH CTLC, grade 3 PLH CTLC, ADAF, VCC, IDDSP, grade 3 PLH, gurgling noise CTLC, ADAF, VCC, grade 3 PLH
S (MPH)
D (F)
Second Endoscopic Examination
S (MPH)
D (F)
Third Endoscopic Examination
S (MPH)
D (F)
29.3
4
IDDSP
31.2
6
N/A
N/A
N/A
28 26.9 27.9
4 4 4
29.7 31.5 30.3
6 6 6
N/A N/A WNL
N/A N/A 31.7
N/A N/A 6
24.3
6
WNL WNL CTLC, ADAF, IDDSP, grade 3 PLH, gurgling noise WNL
26.9
6
N/A
N/A
N/A
S, speed; D, distance; CTLC, cricotracheal ligament collapse; ADAF, axial deviation of the aryepiglottic folds; VCC, vocal cord collapse; IDDSP, intermittent dorsal displacement of the soft palate; PLH, pharyngeal lymphoid hyperplasia; N/A, not applicable; WNL, within normal limits. All horses were exercised over the stated distance twice.
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Figure 3 Pre (A) and 18‐month postoperative (B) still images of the upper airway acquired during dynamic over‐ground endoscopy. The postoperative image demonstrates resolution of circumferential collapse of the cricotracheal ligament.
Analysis of GPS data was not considered beneficial in eliciting the clinical importance of this condition, most likely because of the gradual onset and progressive nature of obstruction. In our experience there were 2 presentations of CTLC in horses. These were young immature horses in early training that were not working to the expectations of the trainer and where multiple abnormalities were identified or mature horses in full training with a history of poor performance and loud respiratory noise where CTLC was the only pathology noted. It is recognized that when compared to the mature horse, young immature Thoroughbred racehorses have a greater incidence of pathology of the upper airway including a higher grade of PLH, IDDSP and abnormalities of the epiglottis.8 All of the 2‐year‐old horses with CTLC had 1 or more other abnormalities of the nasopharynx or larynx. Dynamic obstruction at any site in the upper airway results in increased pressure gradients in the rest of the upper airway and increases the incidence of collapse where instability exists,9 therefore increasing the likelihood of CTLC. All horses in which CTLC spontaneously resolved had evidence of nasopharyngeal inflammation (i.e., grade 3 PLH) at the time of initial diagnosis, and this inflammation decreased or resolved when CTLC had resolved. The objective of conservative treatment for all horses was to decrease nasopharyngeal inflammation. Inflammation of the upper airway may result in neuromuscular dysfunction of the intrinsic musculature of the pharynx, thereby altering airway mechanics.10,11 Continued training and maturation of the tissues of the pharynx and larynx with age8 and fitness will also have resulted in improved airway dynamics, thereby decreasing pressure gradients within the trachea and decreasing the incidence of dynamic collapse. The cricotracheal ligament does not have a muscular component and, therefore, an association between CTLC and inflammation may be indirect, either through alteration in tracheal pressure gradients or alteration in laryngohyoid position. The width of the cricotracheal space was not
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measured in any of the horses identified, and therefore, we do not know if excessive length of the cricotracheal ligament was a compounding factor in predisposing the horses to CTLC; however, palpation of the larynx in these horses did not identify any significant abnormalities. Three horses more than 4 years old were identified as suffering from CTLC, but complete follow‐up information was available for only 2 horses. Both of these horses were in full work, and both had a long history of making abnormal respiratory noise and performing poorly. For both of these horses, CTLC was the only cause of dynamic obstruction identified during 2 dynamic endoscopic examinations, and neither horse improved with conservative management. We believe, therefore, that excessive length or flaccidity of the cricotracheal ligament predisposed the ligament to collapse. Surgical treatment to reduce the cricotracheal space and imbricate the cricotracheal ligament resulted in resolution of clinical signs in these horses. Previous descriptions of treatment include removal of a transversely orientated portion of the cricotracheal ligament followed by closure using a series of mattress sutures.2 Other descriptions include imbrication of the ligament alone2 or partial resection of the ligament with partial reduction of the cricotracheal space.12 The surgical technique to reduce the cricotracheal space we describe allows for greater imbrication of the ligament abaxially and reduces the risk of surgical failure caused by excessive tension on imbricating sutures. Observations made whilst practicing the surgical procedure on cadaveric necks suggest that closure of the cricotracheal space on the ventral and ventrolateral aspects results in the 1st tracheal ring lying adjacent to, or within, the caudal aspect of the cricoid throughout its circumference. Dissection and suture placement on the dorsal surface of the trachea was not considered necessary and could result in a greater incidence of inadvertent trauma to the neurovascular structures lying adjacent to the trachea. Ventral and lateral tension created during imbrication of the ligament translates into circumferential tension at the dorsal aspect of the ligament, which prevents dynamic collapse. Eversion of the ligament
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
Kelly and Pollock
Dynamic Collapse of the Cricotracheal Ligament
before reduction of the space was considered important to ensure sufficient tension was achieved during imbrication. Resection of a portion of the ligament requires entering the lumen of the respiratory tract, which would likely result in a greater incidence of complication and might prolong the period of rest required before the horse can be returned to training. CTLC is an uncommon cause of dynamic respiratory obstruction but one which, when present, may be clinically important. The exact cause of CTLC remains uncertain, but the condition in young horses may resolve after inflammation of the respiratory tract resolves. Surgical treatment may offer a good prognosis for return to athletic function and should be considered for horses in which the condition is persistent.
2. Goulden BE: Some unusual cases of abnormal respiratory noises in the horse. N Z Vet J 1977;25:389–390
ACKNOWLEDGMENTS
7. Pollock PJ, Reardon RJM, Parkin TDH, et al: Dynamic respiratory endoscopy in 67 Thoroughbred racehorses training under normal ridden exercise conditions. Equine Vet J 2009;41:354–360
We gratefully acknowledge the help of Jim Schumacher, Mark Johnston, John Martin, and the veterinary surgeons who referred the cases described. We also acknowledge the work of Philippa Broadway for preparation of the line drawings.
DISCLOSURE
3. Dixon PM, Schumacher J, Collins N: Tracheal disorders, in McGorum BC, Dixon PM, Robinson NE, et al (eds): Equine respiratory medicine and surgery. Philadelphia, PA, Saunders, 2007, pp 543–562 4. Franklin SH: Dynamic collapse of the upper respiratory tract: a review. Equine Vet Educ 2008;20:212–224 5. Mair T, Lane J: Diseases of the equine trachea. Equine Vet Educ 2005;17:146–149 6. Martin BB, Reef VB, Parente EJ, et al: Causes of poor performance of horses during training, racing, or showing: 348 cases (1992–1996). J Am Vet Med Assoc 2000;216:554– 558
8. Embertson RM: Evaluation of the young horse upper airway: what is normal, and what is acceptable? Proc Am Assoc Equine Practnr 1998;44:34–38 9. Derksen FJ: Respiratory system, in Auer JA, Stick JA (eds): Equine surgery (ed 3). Philadelphia, PA, Saunders, 1999, pp 516– 521
The authors report no financial or other conflicts related to this report.
10. Holcombe SJ, Derksen FJ: Stick JA, et al: Pathophysiology of dorsal displacement of the soft palate in horses. Equine Vet J Suppl 1999;30:45–48
REFERENCES
11. Holcombe SJ, Derksen FJ, Stick JA, et al: Effect of bilateral blockade of the pharyngeal branch of the vagus nerve on soft palate function in horses. Am J Vet Res 1998;59:504–508
1. Hare WCD: Equine respiratory system, in Sisson S, Grossman JD, Getty R, (eds): Sisson and Grossman the anatomy of the domestic animals (ed 5, Vol. 1), Philadelphia, PA, Saunders, 1975, pp 498–523
12. Terron‐Canedo N, McCluskie LL, Tremaine HW, et al: Cricotracheal membrane collapse: an uncommon dynamic respiratory obstruction diagnosed in two thoroughbred racehorses. Proceedings of the 4th World Equine Airways Symposium, 2009, p 251
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Corresponding Author Padraig G. Kelly, MVB, Diplomate ECVS, Weipers Centre Equine Hospital, School of Veterinary Medicine, University of Glasgow, 464 Bearsden Road, Glasgow G611QH, UK. E‐mail: [email protected] Submitted February 2012 Accepted July 2012 DOI:10.1111/j.1532-950X.2014.12262.x
Objective: To describe (1) diagnosis of dynamic collapse of the cricotracheal ligament in a group of horses and (2) treatment and outcome of affected horses. Study Design: Retrospective case series. Animals: Thoroughbred horses (n ¼ 8). Methods: Of 600 over ground dynamic endoscopic examinations performed, 8 Thoroughbred horses had cricotracheal ligament collapse (CTLC); 5 were 2 years old and in early training and 2 were mature horses in full work. CTLC was diagnosed if circumferential collapse of the cricotracheal ligament was identified during exercise. Seven horses had repeat endoscopic examination. Two horses unresponsive to conservative management were treated surgically. Results: Multiple abnormalities of the upper portion of the respiratory tract were identified along with CTLC in all five 2‐year‐old horses and resolution of CTLC was observed after treatment for upper airway inflammation. No concurrent respiratory abnormality was identified in the 2 mature horses. Surgical reduction of the cricotracheal space and imbrication of the cricotracheal ligament of these 2 horses resulted in resolution of clinical signs of CTLC. Conclusions: CTLC is a rare cause of dynamic obstruction in Thoroughbred racehorses. Resolution may occur after adaptation to training and after inflammation of the respiratory tract is resolved, but for horses with persistent CTLC, surgical reduction of the cricotracheal space and imbrication of the cricotracheal ligament may result in resolution of clinical signs.
The cricotracheal ligament (ligamentum cricotracheale) is a dense, elastic ligament that connects the caudal border of the cricoid cartilage to the cranial border of the 1st tracheal ring.1 The cricotracheal space is readily palpable in horses because it is wider than any of the interannular ligaments of the trachea and is considerably less tense. The ligament can be readily pushed into the airway, allowing it to be seen during endoscopic examination of the upper airway. Some authors have speculated that excessive length and slackness of the ligament, combined with the sub‐atmospheric inspiratory airway pressures that occur during high‐speed exercise may lead to collapse of the ligament into the airway.2–5 Collapse of the cricotracheal ligament (CTLC) may be so severe that the reduced diameter of the airway lumen results in abnormal respiratory noise and poor performance.2 The condition has only been described in Thoroughbreds and is thought to result from a congenitally, abnormally wide space between the cricoid cartilage and the 1st tracheal ring or as the result of abnormally increased negative pressure within the trachea.2,3 We are unaware of reports of this disorder being diagnosed during dynamic, endoscopic examination under normal exercise conditions.
162
We report the clinical presentation and outcome of 7 Thoroughbred horses with CTLC identified during serial, dynamic, endoscopic examinations of the upper airway during high‐speed exercise and report outcome after surgical treatment in 2 horses refractory to conservative management.
MATERIALS AND METHODS Case Selection Medical records (2008–2011) of 600 Thoroughbred racehorses presented for dynamic endoscopic examination of the upper airway were reviewed. Horses with dynamic CTLC identified during dynamic endoscopic examination were identified and only those that had 1 or more repeat dynamic, endoscopic examinations were included in the study. Dynamic Endoscopic Examination of the Upper Airway Dynamic, over‐ground, endoscopic examination was performed using a dynamic, respiratory endoscope DRS1
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
Kelly and Pollock
(Optomed, Les Ulis, France). Examination was carried out in accordance with the horse’s fitness and training regimen at the time of examination, ensuring the test resulted in fatigue of each horse. Horses were fitted with the custom saddle‐cloth, containing the recording medium and battery, fitted under a saddle. A nose twitch was applied to the horse for placement of the DRS. The insertion tube of the endoscope was placed through the ventral meatus of the right nasal cavity into the nasopharynx and positioned just rostral to the epiglottis allowing a clear view of the larynx and caudal portion of the soft palate. Initial positioning and attachment to the bridle was crucially important to ensure the image remained in the center of the screen during exercise. After the DRS was positioned, it was retroflexed at the level of the right nostril and attached to a custom bridle by using clips and cable ties. After the DRS was adequately positioned and secured, the rider mounted the horse. Correct positioning of the image was confirmed, and video recording and a wrist‐mounted GPS device (Garmin Forerunner 305, Olathe, KS) were activated simultaneously. DRS The DRS consisted of 5 distinct parts: (1) a semi‐rigid, malleable insertion tube (9.8‐mm diameter) with a head section containing a light‐emitting diode (LED) light‐source, bending section, and lens‐cleaning system; (2) bridle with securing mounts which fitted over standard tack; (3) a 3‐kg processor containing a battery with 120 minutes of life, a light source with 2 light levels, a wireless transmitting device, and recording medium (i.e., a secure digital micro USB in mp4 HD format) all contained within a customized saddle pad; (4) a pump, tubing, and bottle for flushing (1.5 mL flush every 30 seconds); and (5) PVC video‐display, wireless, control box operating on battery or AC with an effective range of 500 m in optimal conditions. The selected color temperature (4000– 6000°K) provided high‐quality images. A remote control with playback, stop, and start functions initiated the recordings.
Dynamic Collapse of the Cricotracheal Ligament
Variables Recorded The following variables were recorded: history of respiratory disease and treatment; tack used; weather conditions; whether the horse was ridden alone or with others; whether the jockey observed any abnormalities during exercise (particularly abnormal noises); and any complications with the equipment, horse, or rider that occurred during testing. Speed, distance, and altitude were recorded while the horse exercised, by using a GPS receiver (Garmin Forerunner 305) mounted on the wrist of the rider. The GPS receiver was synchronized with the DRS recording and collected data at intervals of 1 Hz. Endoscopic images were reviewed after testing, at normal playback speed, in slow motion, and if necessary, frame by frame, by 2 veterinary surgeons (P.J.P. and P.K.) blinded to the horse’s history. Abnormalities of the upper airway were identified, described, and entered into a database (Excel 2003). Data obtained from the GPS were downloaded via a dedicated software program (Garmin Training Center) and a graph of elevation and speed achieved was recorded. If abnormalities were identified, speed and position of the horse in the exercise test were recorded; alteration in speed associated with the occurrence of the abnormality was assessed and recorded. The percentage CTLC obstruction was calculated using measurements obtained from digital image editing software (Adobe Creative Suite 5.5; Adobe Systems, Inc., San Jose, CA).
Diagnostic Criteria CTLC was diagnosed when circumferential collapse of the cricotracheal ligament was evident during dynamic endoscopic examination (Fig 1). Accurate positioning of the endoscope is required to allow a circumferential view of the proximal aspect of the trachea. Where suboptimal positioning resulted in a portion of the proximal trachea being obscured, a positive diagnosis of CTLC could not be achieved.
Figure 1 Still images of the upper airway acquired during over‐ground dynamic examination demonstrating circumferential collapse of the cricotracheal ligament in 2 horses.
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Dynamic Collapse of the Cricotracheal Ligament
Kelly and Pollock
Surgical Procedure For 2 horses, CTLC was reported on more than 1 endoscopic examination and was associated with a loud inspiratory noise and reduction in speed during maximal exercise. These 2 horses were treated surgically. Each was sedated with romifidine (0.08 mg/kg intravenously [IV]) and morphine sulfate (0.1 mg/kg IV), and anesthesia was induced with ketamine (2.2 mg/kg IV) in combination with diazepam (0.05 mg/kg IV) and maintained with a mixture of isoflurane in oxygen delivered via a circle system. Horses were positioned in dorsal recumbency, the hair clipped, and skin prepared for aseptic surgery. A 10‐cm, longitudinal, skin incision was created on the ventral midline from the level of the caudal aspect of the thyroid cartilage to the 3rd tracheal ring. The incision was extended through the subcutaneous tissue and paired sternohyoideus and omohyoideus muscles, by sharp and blunt dissection, to expose the ventral half of the 1st tracheal ring and the cricoid cartilage. The cricotracheal ligament was identified between the caudal aspect of the cricoid cartilage and the 1st tracheal ring, grasped with Allis tissue forceps, and everted. An endoscope was passed to the level of the cricoid cartilage to allow observation of the proximal aspect of the trachea. While ensuring penetration of the tracheal mucosa did not occur, the cricoid cartilage was sutured to the 1st tracheal ring using 3 polyethylene‐based, braided sutures (Fiberwire1, CCS‐1, Arthrex, Naples, FL). The sutures were pre‐placed in a 2 bite double‐loop from caudal to cranial on the caudal margin of the ring of the cricoid cartilage and then from cranial to caudal on the cranial margin of the 1st tracheal ring. Two sutures were placed laterally, and 1 suture was placed on the midline (Fig 2). The sutures were tightened and tied after elevating the head to a vertical position. This resulted in the 1st tracheal ring lying in close apposition to, or partially beneath, the caudal aspect of the cricoid cartilage. The everted cricotracheal membrane was then sutured to the 1st tracheal ring using 3 metric polydioxanone placed in a simple‐ continuous pattern. The incision in the musculature was closed using 3 metric polydioxanone placed in a simple‐continuous pattern, the subcutaneous tissue was closed using the same suture placed in a similar pattern, and the skin incision was closed with 3.5 metric polydioxanone placed in a cruciate pattern. A stent bandage was sutured over the closed incision with 3.5 metric polydioxanone placed in a cruciate pattern. All horses were administered procaine penicillin G (22,000 U/kg intramuscularly [IM] twice daily) and gentamicin (6.6 mg/kg IV once daily) for 72 hours and then trimethoprim‐ sulfonamide (30 mg/kg orally, twice daily) for 5 days. Phenylbutazone (2.2 mg/kg orally, twice daily) was administered for 5 days. Horses were fed from shoulder height, and trainers were advised to continue this practice indefinitely.
RESULTS Eight horses were diagnosed with CTLC, but results of multiple endoscopic examinations were available for only 7 horses, all Thoroughbred racehorses. Five were 2 years old,
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Figure 2 Schematic representation of the surgical procedure to reduce the cricotracheal space and imbricate the cricotracheal ligament.
1 was 4 years old, and 1 was 6 years old. Four were examined while they galloped on an all‐weather surface (TapetaTM Footings, Inc., North East, MD), 2 were examined while they galloped on sand, and 1 was examined while galloping on grass. All horses were tacked in a standard manner. No horse had a history of lower respiratory disease or respiratory surgery, but 3 horses were reported to make abnormal respiratory noise when they exercised. The abnormal noise created by 1 horse was described as a gurgling noise and the other 2 horses made a loud inspiratory noise that became progressively worse during exercise. In all cases dynamic obstruction was gradual in onset and was noted to be progressive as exercise continued, being most severe at the point of maximal exercise intensity. A sudden decline in speed was not noted by the jockeys or from GPS data during any examination. Assessment of the degree of obstruction using digital image editing software (Adobe Creative Suite 5.5; Adobe Systems, Inc.) demonstrated that the degree of obstruction was between 36% and 52% of the area of the tracheal lumen. No correlation between horse age and degree of obstruction was noted. No complications occurred during the examinations. All 2 year olds with CTLC were in the early stages of training and were examined initially while they galloped twice
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
Kelly and Pollock
Dynamic Collapse of the Cricotracheal Ligament
over a distance of 4–6 furlongs. All horses were reported by the trainer to be performing below expected levels. All 2‐year‐old horses were found, during dynamic endoscopic examination of the upper airway to have multiple respiratory abnormalities, including CTLC. All had grade 3 or greater pharyngeal lymphoid hyperplasia (PLH), 3 had mild bilateral axial deviation of the aryepiglottic folds (ADAF), 3 had mild bilateral vocal cord collapse (VCC), and 2 had intermittent dorsal displacement of the soft palate (IDDSP). All of the 2‐year‐old horses were treated by administration of a non‐ steroidal, anti‐inflammatory (phenylbutazone 2.2 mg/kg orally twice daily) for 7 days and were kept in training during treatment. During dynamic endoscopic examination, repeated for each of the 2‐year‐old horses during two 6 furlong gallops 6 weeks after the 1st examination, CTLC was no longer identified in 4 horses. Of these 4 horses, no clinical abnormalities were identified in 3 horses; however, 1 horse was again diagnosed with IDDSP. Abnormalities found at the 2nd examination of the other 2‐year‐old horse were similar to those found at the 1st examination and included grade 3 PLH, mild bilateral ADAF, IDDSP, CTLC, and a gurgling noise. During a third examination conducted 6 weeks after the 2nd examination, no dynamic abnormalities of the upper portion of the respiratory tract were identified and PLH was grade 2 and considered within normal limits (Table 1). One horse that had CTLC was 4 years old, and another was 6 years old. Both were in full work at the time of initial examination and were galloped to fatigue on a circular gallop over 2.6 and 3 miles respectively. Clinical signs in these horses were not identified in early training but at the time of presentation poor performance and a loud progressive inspiratory noise were consistently observed by the trainer. CTLC was the only abnormality identified in the 6‐year‐old horse, but the 4‐year‐old horse developed IDDSP at the end of exercise when pulling up. Both horses were observed to make a loud inspiratory noise during dynamic respiratory examination. During repeat examination, performed at 8 and 12 weeks, respectively, both horses made a loud inspiratory noise and CTLC was the only endoscopic abnormality of the URT noted.
DISCUSSION CTLC identified in all of the 2‐year‐old horses during dynamic endoscopy was no longer observed after reduction of PLH to a severity not considered clinically important (grade 2). Accompanying respiratory abnormalities noted during the 1st examination had also resolved, except for IDDSP, which was noted in 1 horse. Both horses that had surgical treatment for CTLC had resolution of clinical signs and CTLC during dynamic endoscopy of the upper portion of the respiratory tract that was performed after the horses were back in full training. Dynamic collapse of the upper portion of the respiratory tract is a frequent cause of poor performance in the equine athlete.6 Dynamic endoscopy of the upper portion of the respiratory tract, performed with the horse on a high‐speed treadmill or running over ground, has allowed detailed description of common causes of dynamic collapse of the airway.7 CTLC is a rare cause of dynamic obstruction of the respiratory tract of horses2–4 and to our knowledge, prevalence, diagnosis under normal exercising conditions, and definitive resolution of CTLC after treatment have not been described. CTLC is diagnosed when the cricotracheal ligament is seen to collapse circumferentially into the airway resulting in considerable narrowing of the airway. Central positioning of the endoscope is essential to accurately diagnose CTLC because if an oblique image is obtained movement of the 1st tracheal ring in relation to the caudal aspect of the cricoid at high speed exercise may give the impression of CTLC, leading to a false positive diagnosis.
Results of Dynamic Endoscopic Examination of Five 2‐Year‐Old Horses
Table 1
No.
Both horses had surgical treatment, as described above. Resolution of abnormal respiratory noise was reported by the trainer in both cases and no abnormal respiratory noise, or abnormalities of the upper airway were identified during dynamic endoscopic examination performed after the horses had returned to full training. In 1 horse this was performed on 1 occasion 6 months after surgery and in the other horse on 2 occasions (6 and 18 months after surgery; Fig 3). Both horses raced postoperatively.
Age
Sex
1
2
C
2 3 4
2 2 2
C C C
5
2
F
First Endoscopic Examination CTLC, ADAF, VCC, IDDSP, grade 3 PLH CTLC, grade 3 PLH CTLC, grade 3 PLH CTLC, ADAF, VCC, IDDSP, grade 3 PLH, gurgling noise CTLC, ADAF, VCC, grade 3 PLH
S (MPH)
D (F)
Second Endoscopic Examination
S (MPH)
D (F)
Third Endoscopic Examination
S (MPH)
D (F)
29.3
4
IDDSP
31.2
6
N/A
N/A
N/A
28 26.9 27.9
4 4 4
29.7 31.5 30.3
6 6 6
N/A N/A WNL
N/A N/A 31.7
N/A N/A 6
24.3
6
WNL WNL CTLC, ADAF, IDDSP, grade 3 PLH, gurgling noise WNL
26.9
6
N/A
N/A
N/A
S, speed; D, distance; CTLC, cricotracheal ligament collapse; ADAF, axial deviation of the aryepiglottic folds; VCC, vocal cord collapse; IDDSP, intermittent dorsal displacement of the soft palate; PLH, pharyngeal lymphoid hyperplasia; N/A, not applicable; WNL, within normal limits. All horses were exercised over the stated distance twice.
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
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Dynamic Collapse of the Cricotracheal Ligament
Kelly and Pollock
Figure 3 Pre (A) and 18‐month postoperative (B) still images of the upper airway acquired during dynamic over‐ground endoscopy. The postoperative image demonstrates resolution of circumferential collapse of the cricotracheal ligament.
Analysis of GPS data was not considered beneficial in eliciting the clinical importance of this condition, most likely because of the gradual onset and progressive nature of obstruction. In our experience there were 2 presentations of CTLC in horses. These were young immature horses in early training that were not working to the expectations of the trainer and where multiple abnormalities were identified or mature horses in full training with a history of poor performance and loud respiratory noise where CTLC was the only pathology noted. It is recognized that when compared to the mature horse, young immature Thoroughbred racehorses have a greater incidence of pathology of the upper airway including a higher grade of PLH, IDDSP and abnormalities of the epiglottis.8 All of the 2‐year‐old horses with CTLC had 1 or more other abnormalities of the nasopharynx or larynx. Dynamic obstruction at any site in the upper airway results in increased pressure gradients in the rest of the upper airway and increases the incidence of collapse where instability exists,9 therefore increasing the likelihood of CTLC. All horses in which CTLC spontaneously resolved had evidence of nasopharyngeal inflammation (i.e., grade 3 PLH) at the time of initial diagnosis, and this inflammation decreased or resolved when CTLC had resolved. The objective of conservative treatment for all horses was to decrease nasopharyngeal inflammation. Inflammation of the upper airway may result in neuromuscular dysfunction of the intrinsic musculature of the pharynx, thereby altering airway mechanics.10,11 Continued training and maturation of the tissues of the pharynx and larynx with age8 and fitness will also have resulted in improved airway dynamics, thereby decreasing pressure gradients within the trachea and decreasing the incidence of dynamic collapse. The cricotracheal ligament does not have a muscular component and, therefore, an association between CTLC and inflammation may be indirect, either through alteration in tracheal pressure gradients or alteration in laryngohyoid position. The width of the cricotracheal space was not
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measured in any of the horses identified, and therefore, we do not know if excessive length of the cricotracheal ligament was a compounding factor in predisposing the horses to CTLC; however, palpation of the larynx in these horses did not identify any significant abnormalities. Three horses more than 4 years old were identified as suffering from CTLC, but complete follow‐up information was available for only 2 horses. Both of these horses were in full work, and both had a long history of making abnormal respiratory noise and performing poorly. For both of these horses, CTLC was the only cause of dynamic obstruction identified during 2 dynamic endoscopic examinations, and neither horse improved with conservative management. We believe, therefore, that excessive length or flaccidity of the cricotracheal ligament predisposed the ligament to collapse. Surgical treatment to reduce the cricotracheal space and imbricate the cricotracheal ligament resulted in resolution of clinical signs in these horses. Previous descriptions of treatment include removal of a transversely orientated portion of the cricotracheal ligament followed by closure using a series of mattress sutures.2 Other descriptions include imbrication of the ligament alone2 or partial resection of the ligament with partial reduction of the cricotracheal space.12 The surgical technique to reduce the cricotracheal space we describe allows for greater imbrication of the ligament abaxially and reduces the risk of surgical failure caused by excessive tension on imbricating sutures. Observations made whilst practicing the surgical procedure on cadaveric necks suggest that closure of the cricotracheal space on the ventral and ventrolateral aspects results in the 1st tracheal ring lying adjacent to, or within, the caudal aspect of the cricoid throughout its circumference. Dissection and suture placement on the dorsal surface of the trachea was not considered necessary and could result in a greater incidence of inadvertent trauma to the neurovascular structures lying adjacent to the trachea. Ventral and lateral tension created during imbrication of the ligament translates into circumferential tension at the dorsal aspect of the ligament, which prevents dynamic collapse. Eversion of the ligament
Veterinary Surgery 44 (2015) 162–167 © Copyright 2014 by The American College of Veterinary Surgeons
Kelly and Pollock
Dynamic Collapse of the Cricotracheal Ligament
before reduction of the space was considered important to ensure sufficient tension was achieved during imbrication. Resection of a portion of the ligament requires entering the lumen of the respiratory tract, which would likely result in a greater incidence of complication and might prolong the period of rest required before the horse can be returned to training. CTLC is an uncommon cause of dynamic respiratory obstruction but one which, when present, may be clinically important. The exact cause of CTLC remains uncertain, but the condition in young horses may resolve after inflammation of the respiratory tract resolves. Surgical treatment may offer a good prognosis for return to athletic function and should be considered for horses in which the condition is persistent.
2. Goulden BE: Some unusual cases of abnormal respiratory noises in the horse. N Z Vet J 1977;25:389–390
ACKNOWLEDGMENTS
7. Pollock PJ, Reardon RJM, Parkin TDH, et al: Dynamic respiratory endoscopy in 67 Thoroughbred racehorses training under normal ridden exercise conditions. Equine Vet J 2009;41:354–360
We gratefully acknowledge the help of Jim Schumacher, Mark Johnston, John Martin, and the veterinary surgeons who referred the cases described. We also acknowledge the work of Philippa Broadway for preparation of the line drawings.
DISCLOSURE
3. Dixon PM, Schumacher J, Collins N: Tracheal disorders, in McGorum BC, Dixon PM, Robinson NE, et al (eds): Equine respiratory medicine and surgery. Philadelphia, PA, Saunders, 2007, pp 543–562 4. Franklin SH: Dynamic collapse of the upper respiratory tract: a review. Equine Vet Educ 2008;20:212–224 5. Mair T, Lane J: Diseases of the equine trachea. Equine Vet Educ 2005;17:146–149 6. Martin BB, Reef VB, Parente EJ, et al: Causes of poor performance of horses during training, racing, or showing: 348 cases (1992–1996). J Am Vet Med Assoc 2000;216:554– 558
8. Embertson RM: Evaluation of the young horse upper airway: what is normal, and what is acceptable? Proc Am Assoc Equine Practnr 1998;44:34–38 9. Derksen FJ: Respiratory system, in Auer JA, Stick JA (eds): Equine surgery (ed 3). Philadelphia, PA, Saunders, 1999, pp 516– 521
The authors report no financial or other conflicts related to this report.
10. Holcombe SJ, Derksen FJ: Stick JA, et al: Pathophysiology of dorsal displacement of the soft palate in horses. Equine Vet J Suppl 1999;30:45–48
REFERENCES
11. Holcombe SJ, Derksen FJ, Stick JA, et al: Effect of bilateral blockade of the pharyngeal branch of the vagus nerve on soft palate function in horses. Am J Vet Res 1998;59:504–508
1. Hare WCD: Equine respiratory system, in Sisson S, Grossman JD, Getty R, (eds): Sisson and Grossman the anatomy of the domestic animals (ed 5, Vol. 1), Philadelphia, PA, Saunders, 1975, pp 498–523
12. Terron‐Canedo N, McCluskie LL, Tremaine HW, et al: Cricotracheal membrane collapse: an uncommon dynamic respiratory obstruction diagnosed in two thoroughbred racehorses. Proceedings of the 4th World Equine Airways Symposium, 2009, p 251
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