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Effect of a Laryngotomy on Upper Airway Mechanics in Exercising Normal Horses

 

W. L. Beard, DVM, MS

K. W. Hinchcliff, BVSc, PhD

Shawn Woods, BS

 

Department of Veterinary Clinical Sciences. The Ohio State University

 

This research was supported by the College of Veterinary Medicine Equine Research Funds.

 

KEY WORDS: Airway mechanics, exercise, laryngotomy, dorsal displacement of soft palate

ABSTRACT
Objective: To determine the effect of a laryngotomy on airway mechanics in normal horses exercising on a treadmill.

Animals: Six adult Standardbred horses.

Procedure: Upper airway mechanics were measured in horses exercising on a treadmill at 5, 8, and 10 m/s before and after a laryngotomy was performed. Pharyngeal and tracheal inspiratory and expiratory pressures were measured by transnasal catheters connected to differential pressure transducers. Airflow was measured by a pneumotachograph mounted on a facemask.

Results: A laryngotomy increased (P <0.05) inspiratory and expiratory airflows and respiratory frequency at all speeds. Pharyngeal and tracheal expiratory resistances were decreased (P <0.05) at all speeds. Inspiratory and expiratory times were decreased (P <0.05) at all speeds.

Conclusions and Clinical Relevance: A laryngotomy alone can alter airway mechanics. Many of the surgical procedures performed for dorsal displacement of the soft palate are performed through a laryngotomy, and it is possible that the observed changes could be attributable to the laryngotomy alone.

Introduction

Dorsal displacement of the soft palate (DDSP) is a common performance-limiting condition in racehorses. The pathogenesis is unclear and could be multifactorial.1,2 Many theories have been advanced to explain the pathogenesis of this problem, including an elongated soft palate,3 caudal retraction of the larynx,4–6 hypoplastic epiglottis,4,7,8 and neuromuscular dysfunction.4,9 To date, none have gained complete acceptance. In an effort to better understand the pathophysiology of DDSP, various studies have investigated the role of airway pressures,10–14 muscle function,15 and nervous function in clinically affected and normal research animals.

Several surgical procedures have been developed based on these theories. The most commonly used procedures include epiglottic augmentation,8 midcervical transection of the sternothyroid and sternohyoid muscles,6 staphylectomy,5 and a combination of the sternothyrohyoid myectomy and staphylectomy.16 Despite the seeming contradictory nature of these procedures, the reported success rates appear to be fairly uniform between the various procedures and range from 50% to 61%.5,6,8,16,17

The apparent uniformity of results obtained in clinical cases with widely varying procedures has aroused skepticism over the benefit of any of the surgical procedures. Additionally, there is a widespread perception that many of these procedures are performed indiscriminately and without an accurate diagnosis, resulting in many normal horses having unnecessary procedures performed. Therefore, a series of studies has been performed to determine the effect on airway mechanics of the various interventions for DDSP. Studies performed in normal horses exercising on a treadmill have examined the effects of a tongue tie,18,20 standing midcervical transection of the sternothyroid and sternohyoid muscles,21 and of a combined staphylectomy and laryngotomy.22 The experimental design in the latter study was a longitudinal repeated-measures design with horses running on the treadmill before and after a laryngotomy combined with a staphylectomy. A sham-operated control group of horses that had only a laryngotomy performed was not included; therefore, it is possible that the effects observed in that study could be attributed to the surgical approach alone. The purpose of the study reported here was to determine the effect of a laryngotomy on upper airway mechanics in normal horses exercising on a treadmill.

Materials and Methods

Horses

Six Standardbred horses, 5 females and 1 castrated male, from 2 to 7 years of age, were used in the study. All horses received paddock exercise for 2 weeks before the study and had ad libitum access to mixed grass hay and water. Horses were housed individually in box stalls during the study. All horses were immunized with equine influenza, rhinopneumonitis, eastern and western equine encephalitis, and Streptococcus equi vaccines. Physical examinations of the horses and endoscopic examinations of the larynx and pharynx were within normal limits. Horses were trained for 16 weeks on the treadmill before the experiment to familiarize the horses with the equipment used in the study and to maintain a consistent level of fitness among the group.

Instrumentation

Horses were instrumented to measure inspiratory and expiratory tracheal and pharyngeal pressures while running on a treadmill as described.21 Transnasal pharyngeal and transnasal tracheal catheters were passed through the left nares and secured to the muzzle with adhesive tape. Two 176-cm sidehole Teflon (FEP Teflon tubing, A Daiger Scientific Division, Wheeling, IL) catheters (inner diameter, 2.38 mm; outer diameter, 3.97 mm) were used. The tip of the pharyngeal catheter was positioned at the level of the opening of the left guttural pouch. The tip of the tracheal catheter was positioned at the junction of the proximal and middle third of the cervical trachea. Each catheter was made with 4 side holes, beginning a distance of 8 catheter diameters from the sealed tip. Catheters were phase-matched at 5, 10, and 15 Hz.23 Tracheal and pharyngeal pressures were measured using differential pressure transducers (DP–45, Validyne Engineering Sales Corporation, Northridge, CA) and recorded on a physiograph (VR 12 Physiologic Monitoring Systems, PPG Biomedical Systems, Bensalem, PA). Before each trial, the transducers were calibrated at pressures from 0 to 30 cm of H2O using a water manometer. A 15-cm pneumotachograph (TZ-7 Laminar flow element, Meriam Instrument Co, Cleveland, OH) was mounted on an airtight facemask, which was placed on the horse’s head over the catheters with the catheters exiting the caudal aspect of the mask. The facemask was constructed of injection-molded plastic and was form-fitted to the horse’s head by use of insulation foam so that the rostral end of the mask did not impede nostril dilation. A halter was incorporated around the facemask to support it and to secure it to the horse’s head. The pneumotachograph was calibrated before each horse ran on the treadmill by forcing a known airflow through the facemask system and measuring flows with a rotameter flow meter (Full View Flow Meter Model FV110C, Brooks Instrument Division, Hatfield, PA), capable of measuring airflow up to 90 L/s.

Respiratory variables, including respiratory rate, tracheal and pharyngeal pressure, translaryngeal pressure, airflow, and inspiratory and expiratory times, were determined by use of a data acquisition system (Buxco Biosystem XA, version 0.9.3, Buxco Electronics Inc., Sharon, CT)  the program of which calculated resistance (peak pressure divided by peak flow). Recordings were examined to eliminate artifactual values and 10 consecutive breaths were averaged to determine a data point for each horse at each speed during each of the 4 trials.

Exercise Protocol

Horses were exercised on a 00 incline treadmill for 5 minutes before the experiment began; horses walked for 1 minute (2 m/s), trotted for 2 minutes (5 m/s), and cantered for 2 minutes (10 m/s). Horses were then instrumented with transnasal pharyngeal and tracheal catheters and the airtight facemask. Horses were then exercised on the treadmill at 5, 8, and 10 m/s for 2 minutes at each speed. The tracheal and pharyngeal catheters were flushed with air at 20 psi for 15 seconds at the beginning of each speed transition to clear the catheters of any exudate. The pneumotachograph was dried with pressurized air after each trial in each horse to remove any particulate material or condensation that might have accumulated during the experiment.

Data were collected for each horse during each of 4 trials. Two presurgery trials were completed on consecutive days and the 2 postsurgery trials were performed on days 45 and 47 postlaryngotomy. Horses maintained the same 3 times/week exercise regimen during the interval between the pre- and postsurgery trials.

Surgical Technique

A laryngotomy was performed on horses under general anesthesia (xylazine, 1.1 mg/kg of body weight intravenously followed by 2.2 mg/kg ketamine intravenously) and positioned in dorsal recumbency with the head extended. A 5-cm skin incision was made on the ventral midline from the junction of the paired thyroid cartilages caudally to the cricoid cartilage. The paired sternohyoideus muscles were separated on midline to expose the cricothyroid ligament, which was sharply incised to enter the larynx. A Weitlaner retractor (Weitlaner blunt, Spectrum Surgical Instruments Co., Stow, OH)was placed in the laryngotomy incision to spread the thyroid cartilages. No other manipulations were performed. The laryngotomy incision was left to heal by second intention. Phenylbutazone (4.4 mg/kg orally every 24 hours) was administered for 5 days. Laryngotomy incisions were cleaned daily until they healed by day 30.

Data Analysis

Peak tracheal and pharyngeal pressures and airflows were measured on the physiograph tracing. For each variable, 10 consecutive breaths were averaged for each horse at each speed to determine a datapoint. Pharyngeal resistance was defined as (P atmosphere - P pharynx)/peak airflow. Tracheal resistance was defined as (P atmosphere - P tracheal)/peak airflow. Translaryngeal resistance was defined as (P trachea - P larynx)/ peak airflow). Inspiratory and expiratory pharyngeal, tracheal, and translaryngeal airway resistances were calculated as the ratio of peak pressure to peak airflow for each breath.19,24

Data from the 2 trials before laryngotomy were compared by two-way analysis of variance (ANOVA) and the 2 trials after laryngotomy were similarly compared. Significant differences were not observed between the 2 presurgery trials or the 2 postsurgery trials. Therefore, values for each of the 2 presurgery and the 2 postsurgery trials were combined and averaged. The combined presurgery and combined postsurgery trials were used in the statistical analysis. Data were analyzed by two-way ANOVA for repeated measures. Pairwise comparisons were evaluated using the Student-Newman-Keuls’s post-hoc test. The null hypothesis that there was no effect of a laryngotomy was rejected if P <0.05. Results are expressed as mean ± standard error of mean.

Results

Effect of Speed

Increasing treadmill speed caused an increase (P <0.05) in peak inspiratory and expiratory airflows, peak tracheal and pharyngeal inspiratory and expiratory pressures. Translaryngeal inspiratory resistance, frequency, minute volume, and tidal volume increased (P <0.05) with increasing treadmill speed. Inspiratory and expiratory time decreased (P <0.05) with increasing treadmill speed (Table 1).

Effect of Surgery

A laryngotomy increased (P <0.05) inspiratory and expiratory airflows and respiratory frequency at all speeds. Pharyngeal and tracheal expiratory resistances were decreased (P <0.05) at all speeds. Inspiratory and expiratory times were decreased (P <0.05) at all speeds (Table 1).

Discussion

This report is the most recent in a series of studies performed by the authors that measures the effect of the commonly performed surgical procedures on upper airway mechanics in exercising horses. In a prior study, O’Rielly et al.22 reported that a staphylectomy performed through a laryngotomy approach altered airway mechanics in exercising horses. That study did not include a sham-operated control group; therefore, it remained inconclusive if the effects noted were attributable to the laryngotomy alone or the laryngotomy combined with a staphylectomy. A laryngotomy is also routinely performed for other surgical procedures involving the arytenoid cartilages, laryngeal saccules, and epiglottis, providing ample justification for studying the effects of a laryngotomy.

This study found that a laryngotomy decreased tracheal and pharyngeal expiratory resistance, and increased peak inspiratory and expiratory flow and respiratory rate. Results of the present study indicate that a laryngotomy is not innocuous as previously thought. This is in contrast to a previous study in which a laryngotomy and staphylectomy combined caused an increase in resistance across the larynx and increased inspiratory time.22 Those changes are typical of a fixed respiratory obstruction and were interpreted to be potentially detrimental to performance, although the significance of the negative impact in clinical cases could not be determined in a research setting. The null hypothesis for the present study was that a laryngotomy would have no effect on upper airway mechanics. This hypothesis was developed based on our speculation that the deleterious effects observed after a combined laryngotomy and staphylectomy were attributable entirely to the staphylectomy and that the laryngotomy approach is innocuous. The current findings were unexpected.

A potential limitation to this study is the lack of a nonoperated group to control for the effect of time and other associated confounding variables such as temperature and humidity. In this study, each horse served as its own control based on experience from previous studies in which it was found that the variability in measurements between horses is much greater than differences induced by the surgical procedure. To minimize the limitation posed by the lack of a nonoperated control group, several precautions were taken. Horses were trained for 4 months before initiation of the study to ensure a consistent level of fitness and to eliminate a training effect during the study. Horses continued on this training schedule throughout the postoperative period. Several trials were performed before performing the laryngotomy to ensure the repeatability of our measurements over time. The last 2 trials before surgery and 2 trials after surgery were included in the analysis. The preoperative trials were compared by ANOVA and the postoperative trials were similarly compared. No differences were detected; therefore, the preoperative trials were combined for comparison to the combined postoperative trials. Statistical analysis by two-way ANOVA for repeated measures on all combinations of the preoperative and postoperative trials yielded essentially the same results. Therefore, we concluded it unlikely that a spurious measurement influenced our result. We cannot entirely rule out the possibility that time, temperature, humidity, or other confounding variables influenced our results.

A laryngotomy is typically allowed to heal by second intention. The surgical incision successively passes through skin, fascia, sternohyoid muscle, omohyoid muscle, and cricothyroid ligament. Second-intention healing begins with fibroplasia, which forms a bed of granulation tissue that effectively fuses all of these muscle and fascial layers together in accordance with the one wound–one scar theory. This granulation tissue matures through a remodeling process that decreases vascularity and cellularity, and increases collagen cross-linking to become fibrous connective tissue. Cross-linking of collagen in the wound causes the resultant scar to contract, which effectively shortens the scar and pulls on the omohyoid and sternohyoid muscles, which attach to the hyoid bone approximately 2 to 3 cm rostral to the laryngotomy site.

The position of the hyoid apparatus is determined by the net result of forces exerted by opposing muscle groups. The genioglossus and geniohyoid muscles pull the hyoid apparatus cranially and are opposed by caudal traction exerted by the omohyoid, sternohyoid, and sternothyroid muscles. Simultaneous contraction of all of these accessory muscles of respiration displaces the hyoid apparatus ventrally and tenses the pharyngeal wall. Thus stabilized, the upper airway is able to resist dynamic collapse and decrease upper airway resistance. This is consistent with a study by Holcombe et al.,21 which demonstrated that midcervical transection of the sternothyroid and sternohyoid muscles increases airway resistance, presumably as a result of a loss of pharyngeal dilation. The omohyoid and sternohyoid muscles are known to be pharyngeal dilators in other species. These muscles could be functionally shortened by incorporation within a fibrous scar at the laryngotomy site, which is only a few centimeters caudal to their normal insertion on the basihyoid bone. Tension on these muscles secondary to contraction of scar tissue would presumably result in pharyngeal dilation and decreased airway resistance. Although the amount of fibrous connective tissue deposited is sufficiently small that it is difficult to tell by external palpation; clinical experience gained by examination of horses that have had repeat laryngotomies performed has confirmed that the surgical site contains dense fibrous scar tissue that results in fusion of the normal tissue planes. Confirmation that the effects of a laryngotomy are the result of functional shortening of the sternohyoid and omohyoid would require measurements of the position of the hyoid apparatus or muscle tension, neither of which were done in this study.

It is uncertain what, if anything, a staphylectomy does. To date, there has been no satisfactory explanation of why a staphylectomy results in clinical improvement, if in fact it does. It was assumed that a laryngotomy was innocuous, and that any effects were attributable to whatever procedure is performed through this approach. Results of this study indicate otherwise. Increased inspiratory and expiratory airflow and decreased expiratory resistance were observed after a laryngotomy. It is difficult to extrapolate these results to the clinical setting for surgical treatment for DDSP for a number of reasons. Normal horses might not yield the same result as clinically affected animals. The instrumentation used to measure respiratory variables in fact influence the measurements, thereby complicating the interpretation of such information because horses wearing a facemask breathe differently than noninstrumented horses. There is also considerable individual variation in surgical technique. Nevertheless, these results indicate that in instrumented horses under experimental conditions, a laryngotomy alone will alter airway mechanics.

References

1. Holcombe S, Derksen F, Stick J, et al: Pathophysiology of dorsal displacement of the soft palate in horses. Equine Vet J Suppl 30:45–48, 1999.

2. Haynes PF: Dorsal displacement of the soft palate and epiglottic entrapment: diagnosis, management, and interrelationship. Compend Contin Educ Pract Vet 5:S379–S389, 1983.

3. Shappell KK, Caron JP, Stick JA, et al: Staphylectomy for the treatment of dorsal displacement of the soft palate in two foals. J Am Vet Med Assoc 195:1395–1398, 1989.

4. Cook WR: Some observations on the form and function of the equine upper airway in health and disease: II. Proc Am Assoc Eq Pract 1981:355–391.

5. Anderson JD, Tulleners EP, Johnston JK, et al: Sternothyrohyoideus myectomy or staphylectomy for treatment of intermittent dorsal displacement of the soft palate in racehorses: 209 cases (1986–1991). J Am Vet Med Assoc 206:1909–1912, 1995.

6. Harrison IW, Raker CW: Sternothyrohyoideus myectomy in horses: 17 cases (1984–1985). J Am Vet Med Assoc 193:1299–1302, 1988.

7. Linford RL, O’Brien TA, Wheat JD, et al: Radiographic assessment of epiglottic length and pharyngeal and laryngeal diameters in the Thoroughbred. Am J Vet Res 44:1660–1666, 1983.

8. Tulleners E, Hamir A: Evaluation of epiglottic augmentation by use of a polytetrafluoroethylene paste in horses. Am J Vet Res 52:1908–1916, 1991.

9. Holcombe S, Derksen F, Stick J, et al: Effect of bilateral blockade of the pharyngeal branch of the vagus nerve on soft palate function in horses. Am J Vet Res 59:504–508, 1998.

10. Williams JW, Meagher DM, Pascoe JR, et al: Upper airway function during maximal exercise in horses with obstructive upper airway lesions. Vet Surg 19:142–147, 1990.

11. Rehder R, Ducharme N, Hackett R, et al: Measurement of upper airway pressures in exercising horses with dorsal displacement of the soft palate. Am J Vet Res 56:269–274, 1995.

12. Neilan GJ, Rehder RS, Ducharme NG, et al: Measurement of tracheal static pressure in exercising horses. Vet Surg 21:423–428, 1992.

13. Hackett RP, Ducharme NG, Mitchell L: The role of treadmill endoscopy in diagnosis of dynamic obstruction of the upper airway. Proceedings Am Assoc Eq Pract 40:83, 1994.

14. Ducharme NG, Hackett RP, Ainsworth DA, Erb HN, Mitchell L, Soderholm V: The value of pressure profiles in exercising horses [Abstract]. Vet Surg 21:387, 1992.

15. Holcombe S, Derksen F, Stick J, et al: Effect of bilateral tenectomy of the tensor veli palatini muscle on soft palate function in horses. Am J Vet Res 58:317–321, 1997.

16. Anderson J, Tulleners E, Johnston J, et al: Sternothyrohyoideus myectomy and staphylectomy for treatment of dorsal displacement of the soft palate in horses: 218 cases (1986–1991). Vet Surg 22:371, 1993.

17. Carter BG, Robertson JT, Beard WL, Moore RM: Sternothyrohyoideus myectomy, tenectomy and staphylectomy for the treatment of dorsal displacement of the soft palate in horses [Abstract]. Vet Surg 22:374, 1993.

18. Robertson J, Copelan R: Surgery of the upper respiratory tract in the racehorse. Vet Clin North Am Equine Pract 6:197–222, 1990.

19. Cornelisse C, Holcombe S, Derksen F, et al: The effect of a tongue-tie on upper airway mechanics in horses during exercise. Am J Vet Res 62:775–778, 2001.

20. Beard W, Holcombe S, Hinchcliff K: Effect of a tongue-tie on upper airway mechanics during exercise following sternothyrohyoid myectomy in clinically normal horses. Am J Vet Res 62:779–782, 2001.

21. Holcombe SJ, Beard WL, Hinchcliff KW, et al: Effect of sternothyrohyoid myectomy on upper airway mechanics in normal horses. J Appl Physiol 77:2812–2816, 1994.

22. O’Rielly J, Beard W, Renn T, et al: Effect of a combined staphylectomy and laryngotomy on upper airway mechanics in clinically normal horses. Am J Vet Res 58:1018–1021, 1997.

23. Derksen F, Robinson N: Esophageal and intrapleural pressures in the healthy conscious pony. Am J Vet Res 41:1756–1761, 1980.

24. Shappell K, Derksen F, Stick J, et al: Effects of ventriculectomy, prosthetic laryngoplasty, and exercise on upper airway function in horses with induced left laryngeal hemiplegia. Am J Vet Res 49:1760–1765, 1988.

 

 

 

 

 

 

Table 1. Measurement of Airway Variables in Horses Exercising at 5, 8, and 10 m/s on a treadmill Before and After a Laryngotomy

 

                                                                                 Before Surgery           After surgery

Variable                                                      Speed                         ± SEM                              ± SEM 

Peak inspiratory flow                                5 m/s             43.4            ±3.2              54.7             ±3.1*

(L/s)                                                         8 m/s†            65.1            ±4.3              80.1             ±4.3*

                                                               10 m/s†‡          79.4             ±5                96.9             ±4.1*

 

Peak expiratory flow                                 5 m/s             46.1             ±5                63.9             ±4.7*

(L/s)                                                         8 m/s†            64.4            ±3.2              86.8             ±5.7*

                                                               10 m/s†‡           75             ±3.2               98               ±4.1*

 

Peak tracheal inspiratory                          5 m/s            -15.6           ±1.2             -12.9             ±1.3

pressure (cm of H2O)                               8 m/s†           -23.9           ±1.9             -22.3             ±1.9

                                                               10 m/s†‡         -30.3            ±2               -30.9             ±2.4

 

Peak tracheal expiratory                           5 m/s             28.5            ±2.6              24.5              ±1.6

pressure (cm of H2O)                               8 m/s†            33.8            ±2.5              32.1              ±2.7

                                                                10 m/s†           34.7            ±2.8              32.7              ±2.2

 

Peak  pharyngeal inspiratory                    5 m/s            -13.7           ±1.4             -11.7             ±1.3

pressure (cm of H2O)                               8 m/s†           -19.5           ±1.8             -18.1             ±1.7

                                                               10 m/s†‡         -22.6           ±1.6             -21.2             ±1.3

 

Peak pharyngeal expiratory                      5 m/s             24.5             ±3                19.6              ±2.1

pressure (cm of H2O)                               8 m/s†            29.8            ±3.3              28.6              ±3.2

                                                                10 m/s†           30.5            ±3.6              28.3              ±2.7

 

Tracheal Inspiratory                                  5 m/s             0.41           ±0.06             0.25             ±0.02

resistance (cm of H2O/L/s)                      8 m/s             0.46            ±0.1              0.29             ±0.03

                                                                 10 m/s             0.4            ±0.03             0.33             ±0.03

 

Tracheal Expiratory                                   5 m/s             0.85           ±0.12              0.5             ±0.06*

resistance (cm of H2O/L/s)                      8 m/s             0.78           ±0.15             0.48            ±0.07*

                                                                 10 m/s            0.62           ±0.08              0.4             ±0.03*

 

Pharyngeal Inspiratory                              5 m/s             0.37           ±0.05             0.22             ±0.03

resistance (cm of H2O/L/s)                      8 m/s             0.39            ±0.1              0.23             ±0.03

                                                                 10 m/s             0.3            ±0.04             0.23             ±0.03

 

Pharyngeal Expiratory                               5 m/s             0.77           ±0.13              0.4             ±0.06*

resistance (cm of H2O/L/s)                       8 m/s             0.68           ±0.14             0.44            ±0.08*

                                                                 10 m/s            0.55           ±0.09             0.34            ±0.03*

 

Translaryngeal inspiratory                        5 m/s             0.06           ±0.02             0.04             ±0.01

resistance (cm of H2O/L/s)                       8 m/s             0.07           ±0.01             0.06             ±0.01

                                                               10 m/s†‡           0.1            ±0.02              0.1              ±0.02

 

Translaryngeal expiratory                         5 m/s             0.12           ±0.01             0.09             ±0.01

resistance (cm of H2O/L/s)                       8 m/s             0.12           ±0.03             0.05             ±0.01

                                                                 10 m/s            0.07           ±0.01             0.05             ±0.01

 

Frequency (breaths/min)                          5 m/s              55               ±5                 70                ±9*

                                                                 8 m/s†             70               ±9                 78                ±8*

                                                               10 m/s†‡           79              ±13                96               ±10*

 

Tidal volume (L)                                         5 m/s              17             ±1.1               18                ±1.8

                                                                 8 m/s†             22             ±2.1               25                ±2.4

                                                                10 m/s†            25             ±3.4               26                ±3.1

 

Inspiratory time (s)                                    5 m/s             0.58           ±0.08             0.49            ±0.08*

                                                                 8 m/s†            0.48           ±0.08             0.42            ±0.06*

                                                                10 m/s†           0.45           ±0.08             0.35            ±0.05*

 

Expiratory time (s)                                     5 m/s             0.58           ±0.05             0.47            ±0.06*

                                                                 8 m/s†            0.48           ±0.05             0.39            ±0.03*

                                                                10 m/s†           0.41           ±0.05             0.34            ±0.03*

*Significantly different (P<0.05) from presurgical value at the same speed.

† significantly different (P<0.05) with speed effect from 5 m/s value.

‡ significantly different (P<0.05) with speed effect from 8 m/s value.

 

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