DISCUSSION
This manuscript describes a novel exercise-related (dynamic) disorder of
the epiglottis induced during periods of poll flexion in harness
racehorses. Compression of the base of the epiglottis appeared visually
during the first phase of induced poll flexion (phase 2) in all 18
horses. In all cases, whether unilateral or bilateral, it appeared
videoendoscopically as if there was extraluminal compression of the base
of the epiglottis from the lateral nasopharyngeal wall (green arrows in
figures) locally on the affected side(s), potentially caused by a change
in position of the larynx/hyoid apparatus within the intermandibular
space during poll flexion. In most cases the compression of the
epiglottis was of a magnitude that it visually obscured the abducted
vocal fold(s) on the affected side(s). In certain cases, the lateral
margins of the epiglottis displayed progressive inward deviation with
prolonged duration of exercise, potentially due to greater inspiratory
luminal pressures in the region of the larynx.
Poll flexion during exercise, defined as a decreased angle between the
mandible and ventral neck, affects upper airway function in horses
competing in multiple athletic disciplines (Petsche et al. 1995; Strand
et al. 2009; Davidson et al. 2011). Harness racehorses perform in a
position of “high” poll flexion, due to the overcheck which prevents
lowering of the head and neck and aids steering the horse tactically in
races. These horses are gathered onto the bit with long reins and are
restrained from premature exhaustion or galloping. Poll flexion during
maximal exercise in clinically normal Standardbreds causes an increase
in inspiratory impedance and greater negative inspiratory pressures (7-8
cm H2O difference), relative to when these horses are
exercised in free head carriage (head and neck extended), creating a
mild inspiratory obstruction (Petsche et al. 1995). Similar findings (6
cm H2O difference) have been documented in clinically
normal elite Norwegian-Swedish coldblooded trotters during maximal
exercise in poll flexion relative to maximal exercise with free head
carriage (Strand et al. 2009). This physiologic event is explained by
the Bernoulli principle and Venturi effect, occurring as a consequence
of narrowing of the URT during poll flexion (Cehak et al. 2010).
Narrowing of a region of the URT will lead to increased velocity of air
through the constricted region and therefore lower intraluminal
pressures according to Poiseuille’s Law (fluid dynamics notation). If a
form of URT obstruction is present, local narrowing (collapse) of the
region can become self-perpetuating with progressive lowering of
inspiratory pressures over time and worsening of the obstruction. This
has been demonstrated to occur in harness racehorses diagnosed with DLC
(Strand et al. 2009).
Poll flexion can also induce or exacerbate both simple and complex forms
of exercise-induced URT disorders reported in harness racehorses (Strand
et al. 2004; Fjordbakk et al. 2008; Strand et al. 2012). Exacerbation of
already existing URT disorders during poll flexion may be due to the
increase in airway turbulence, impedance and intraluminal pressures
occurring during poll flexion, while the pathophysiology behind
induction of new URT disorders solely evident during poll flexion is
likely more complex.
In addition to altering airway dynamics, poll flexion also causes
anatomical conformational changes of the laryngohyoid apparatus which
can be readily measured from lateral radiographs of the region
(McCluskie et al. 2008; Fjordbakk et al. 2013). The larynx moves
rostrally in relation to the hyoid apparatus during poll flexion;
McCluskie et al. (McCluskie et al. 2008) demonstrated a rostral
advancement of the ossified portion of the thyroid cartilage in relation
to the thyrohyoid bone. Achieving this local conformation change is the
basis of the “laryngeal tie-forward” procedure for treating iDDSP
(Woodie et al. 2005).
Fjordbakk et al. (2013) demonstrated that horses affected by DLC showed
a statistically significantly greater rostral advancement of the larynx
in relation to the thyrohyoid bone during poll flexion compared to
unaffected control horses. This rostral advancement within the
intermandibular space resulted in external compression of the larynx as
shown by the authors in form of a reduced laryngeal lumen width in
affected horses measured ultrasonographically (Fjordbakk et al. 2013).
Though DLC to this date has been diagnosed in a number of different
breeds and disciplines, the aforementioned study and more recent
research into genetics illustrate that URT disorders occurring solely
during poll flexion often result from a combination of phenotypic
predisposition along with the consequences of a rostral laryngohyoid
displacement (Fjordbakk et al. 2013; Velie et al. 2020).
Epiglottic compression appears soon after inducing poll flexion by
gathering the reins and driving the horse onto the bit, similar to how
DLC visually appears. The authors have seen compression of the
epiglottis manifesting most commonly as part of a DLC diagnosis, and
epiglottic compression may be a variation of a complex array of
exercise-induced laryngeal disorders seen only during phases of poll
flexion. The occurrence of the disorder primarily, without concurrent
DLC, has however not been described before.
Dynamic laryngeal collapse is a form of bilateral arytenoid cartilage
and vocal fold collapse occurring during exercise in poll flexion in
predisposed horses, not associated with recurrent laryngeal neuropathy
(Fjordbakk et al. 2015; Ducharme 2016). It is most commonly diagnosed in
NSCTs but is also reported to be common in the Colombian Criollo Paso
breed (Joó et al. 2021) and other gaited horses that exercise in
“high” poll flexion (Hanche-Olsen et al. 2010; Allen et al. 2011;
McCarrel & Woodie 2015; Hackett & Leise 2018). In DLC, a phenotypic
predisposition combined with rostral laryngohyoid advancement in the
intermandibular space occurring during poll flexion leads to inward
displacement of the arytenoid cartilages with secondary collapse of the
vocal folds (Strand et al. 2004; Fjordbakk et al. 2008). The phenotypic,
or conformational traits include: a rostrally positioned larynx relative
to the vertical ramus of the mandible, a high head and neck position
during exercise, a narrow intermandibular space and an energetic
attitude when driven “onto the bit” (Strand et al. 2004; Velie et al.
2020). A rostrally positioned larynx, relative to the vertical ramus of
the mandible, is a trait of many draft and pony breeds of horses (Hawe
et al. 2001). In the cases presented here, the rostral laryngohyoid
advancement caused by periods of poll flexion leads to compression of
the base of the epiglottis while the arytenoid cartilage’s ability to
abduct is unaffected. As opposed to horses diagnosed with DLC, horses
showing epiglottic compression likely have more compression of a
rostroventrally positioned articulation between the thyrohyoid bone and
thyroid cartilage which is not interfering with the ability of the
cricoarytenoideus dorsalis muscles to abduct the arytenoid cartilages,
as seemingly occurs with DLC (Figure 5) (Strand et al. 2004; Fjordbakk
et al. 2008).
The majority of horses in this study presented for investigation of poor
performance and/or abnormal respiratory noise (Table 1), however one
horse (nr. 3) presented after physical collapse during a pari-mutuel
race. This horse had visually the most severe degree of URT obstruction
of all 18 horses in this review during HSTE with both compression of the
base of the epiglottis and dorsomedial deviation of the epiglottic
margins. This highlights the importance of examining harness racehorses
during exercise using bit, bridle, long reins and overcheck to induce
different head and neck angles similar to what these horses experience
under competition if one is to fully understand the clinical condition.
This can be accomplished using high-speed treadmill videoendoscopy, as
described here, or utilising a vigorous exercise protocol on the
racetrack with overground endoscopy.
Unilateral compression of the base of the epiglottis was seen in 57.1%
of STBs and in 9.1% of NSCTs, whilst bilateral compression was seen in
42.9% of STBs and in 90.9% of NSCTs. This uneven breed distribution
may be related to the low sample size, or to a potential anatomical
conformational difference of the hyoid apparatus and/or thyrohyoid
articulation between these two genetically distinct breeds. Another
plausible cause of unilateral compression of the base of the epiglottis
is uneven head carriage while being driven, but this variable was not
investigated in this study. However, the experienced drivers of the
horses in this study always attempted to drive them evenly onto the bit
during the examination. Additionally, any horses showing signs of
lameness during the examination, a common cause of uneven head carriage
in harness racehorses, were excluded from the study. The position of the
endoscope should also not affect the unilateral appearance of the
disorder as the endoscope was passed via the right ventral meatus in all
cases, and there was an even distribution between left and right
unilateral epiglottic compression. Finally, the compression of the
epiglottis occurred only during phases of poll flexion and was never
evident in phase 1 (free head carriage) prior to first induction of poll
flexion.