Vet Clin Equine 19 (2003) 87–100

Exercise-induced pulmonary hemorrhage

Eric K. Birks, DVM, PhDa,*,
Mary M. Durando, DVM, PhDb,
Steve McBride, DVM, MSc
a
Sports Medicine and Imaging, Department of Clinical Studies, New Bolton Center,
School of Veterinary Medicine, University of Pennsylvania, 382 West Street Road,
Kennett Square, PA 19348-1692, USA
b
Department of Veterinary Medicine and Epidemiology, Veterinary Medical Teaching Hospital,
University of California–Davis, One Shields Avenue, Davis, CA 95616-8747, USA
c
Eastern Thoroughbred Racing Associates, Philadelphia Park,
3001 Street Road, Bensalem, PA 19020, USA

Exercise-induced pulmonary hemorrhage (EIPH) is considered by many

to be a major cause of reduced athletic performance and is one of the most
often treated medical ‘‘conditions’’ in athletic horses. In the United States,
most Thoroughbred and Standardbred racehorses compete after adminis-
tration of some form of pharmacologic or dietary therapy purported to
reduce the incidence and/or severity of EIPH. As such, EIPH is not only
a major health concern for the horse but also has a significant economic
impact on the entire equine industry. Because of this importance, many
studies have investigated the etiology and possible therapies that might
prevent or limit EIPH in equine athletes. Over the past several decades,
numerous excellent reviews have been published that detail this research
progress [1–5]. The purpose of this article is to summarize the most recent
advances in our understanding of EIPH.

Epidemiologic perspectives
EIPH has most commonly been observed in Thoroughbred, Standard-
bred, and Quarter Horse racehorses, however, it has also been reported in
virtually all equine breeds during different forms of intense exercise, in-
cluding steeplechasing, 3-day eventing, show jumping, polo, barrel racing,
reining, cutting, and draft horses [5,6]. Studies have shown that its

* Corresponding author.
E-mail address: ebirks@vet.upenn.edu (E.K. Birks).

0749-0739/03/$ - see front matter Ó 2003, Elsevier Science (USA). All rights reserved.
doi:10.1016/S0749-0739(02)00068-8
88 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100

prevalence is related to intensity of exercise rather than to duration of

exercise or breed. Although a significant association between the frequency
of EIPH as diagnosed by postexercise endoscopy and gender was not found
in several studies [5,6], an increased frequency of epistaxis in female versus
intact male horses was recently reported [7]. Several authors have reported
an association between EIPH and age, with the incidence apparently in-
creasing in older horses [5,7,8].
Historically, EIPH was diagnosed by evidence of blood at one or both
nostrils (epistaxis). In a recent report of more than 250,000 race starts, epi-
staxis was observed in 0.15% of the horses after racing [7]. The incidence of
epistaxis in racehorses reported in other studies ranges from 0.2% to 13%
[6,8,9]. With the advent of the flexible endoscope, routine examination of
the upper airway has become commonplace. The incidence of EIPH as diag-
nosed by endoscopic examination of the upper airway is now reported to
be as high as 75% to 100% when the identifying criteria for diagnosing
EIPH is extended to include the presence of blood in the trachea [5,8,10,11].
Studies have also shown that the frequency of detecting blood in the trachea
of horses after exercise increases if individual horses are examined endo-
scopically after multiple exercise bouts [5,10]. If the diagnostic criterion for
EIPH is the observation of erythrocytes or hemosiderophages in either
tracheal wash or bronchoalveolar lavage (BAL) fluid, the incidence of EIPH
is virtually 100% in all horses involved in intense exercise [12].

Clinical findings and effect on performance

The clinical findings associated with EIPH are often quite vague and
generally relate more to the success of the athlete than to specific clinical
signs (ie, a horse is more likely to be evaluated when it competes unsuc-
cessfully). Although epistaxis may be part of the presenting complaint, as
noted previously, this is uncommon. Much more common are complaints of
not performing up to expectations, which is often associated with sudden
losses of ‘‘speed’’ during competition and is accompanied by coughing
and/or increased swallowing efforts after intense exercise or racing. When
those horses that have competed successfully have been randomly examined
(usually by endoscopic inspection of the upper airway), most if not all also
exhibit some degree of EIPH. Thus, the clinical presentation of EIPH is
most likely to be related to either the observation of epistaxis or an un-
successful competition with no other obvious cause for poor performance.
When randomly evaluating horses completing a competition, most studies
have found no relation between the occurrence and/or severity of EIPH and
racing success [5,8,10].
As noted previously, it is generally believed that the occurrence of EIPH
is detrimental to athletic performance. Even early reports of epistaxis asso-
ciated with racing concern horses that were obviously winning athletes
 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100 89

despite the bleeding. Numerous anecdotal reports can be found of the

winning horse in a competition showing either epistaxis or severe endo-
scopically diagnosed EIPH. Pascoe et al [8] reported no relation be-
tween visual bleeding score and finish position. Similar results have been
reported elsewhere [5]. Most recently, we have published the results of
a study that showed a trend toward a negative relation between winning
position and bleeding score (Fig. 1) [10]. Proponents of quantifying EIPH
with erythrocyte counts in BAL fluid have suggested that the lack of a
relation between finish position and EIPH severity may simply be the result
of failure of the visual system to quantify the severity of EIPH correctly
[11,13].

Causes/pathophysiology of exercise-induced pulmonary hemorrhage

A number of hypotheses have been proposed to explain the origin of
blood observed at one or both nostrils (epistaxis). From early published
reports of epistaxis after racing, the bleeding was commonly believed to
originate from the head or nasal cavity. In 1974, Cook [9] reported that
blood seen at the nostrils and in the trachea most likely originated within the
lung. This finding was confirmed by Pascoe et al [8], who suggested that the
term exercise-induced pulmonary hemorrhage be used to describe the bleeding

Fig. 1. Relation between endoscopic exercise-induced pulmonary hemorrhage bleeding score

and finish position for Thoroughbreds (open bars) and Standardbreds (solid bars). (Adapted from
Birks EK, Shuler KM, Soma LR, et al. EIPH: postrace endoscopic evaluation of Standardbreds
and Thoroughbreds. Equine Vet J Suppl 2002;34:375–8; with permission.)
90 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100

associated with exercise. In a series of reports resulting from an exten-

sive clinical and postmortem study of lungs from horses with EIPH,
O’Callaghan et al [14] suggested that EIPH resulted from rupture of
pulmonary capillaries that were weakened by inflammatory disease. Ad-
ditional mechanisms that have been proposed include upper airway ob-
structions, coagulopathies, small airway disease, blood flow redistribution
during exercise, altered blood viscosity, and mechanical trauma result-
ing from pressure waves propagated through the body due to the hooves
striking the ground [5,8,11,15–17,50,54]. All these mechanisms may in fact
contribute to EIPH, but for various reasons, they cannot explain the pri-
mary underlying causes of the bleeding. In fact, many horses exhibit EIPH
in the absence of upper airway obstruction or inflammatory airway disease,
with clotting profiles within normal limits and with normal exercise-related
blood viscosities. Although the locomotory impact hypothesis is quite com-
pelling, ex vivo lung perfusion studies showing identical pulmonary capillary
ruptures as those associated with exercise and anecdotal reports of horses
showing EIPH during swimming exercise suggest that the underlying cause of
EIPH is not specifically related to locomotory impact-related lung trauma.
Presently, the most widely accepted hypothesis for the origin of the blood
in EIPH is stress failure of pulmonary capillaries [13,18–20]. Although
postmortem studies suggested that rupture of disease-weakened pulmonary
blood vessels was the source of blood in EIPH [14,21], comparative studies
have shown that equine pulmonary capillaries rupture despite being rel-
atively stronger than those of other species (Fig. 2) [18]. Additionally,
pathologic evidence of EIPH has been reported in yearling horses with no
evidence of prior pulmonary disease [22].
Multiple laboratories have reported extreme pulmonary vascular
pressures in exercising horses [23,24]. It is likely that these pressures, in
combination with increased inspiratory effort related to exercise, lead to
stress failure of the pulmonary capillaries. We have reported an increase in
stress failure of capillaries in an ex vivo perfused lung model as transmural
pressures (the difference between intravascular and extravascular pressures)
were increased from 75 to 100 mm Hg (Fig. 3) [19]. During treadmill
exercise, the severity of EIPH as diagnosed by enumeration of erythrocytes
in BAL fluid was related to pulmonary arterial pressures (Fig. 4) [13,20]. In
these studies, there was a significant increase in erythrocyte numbers from
those horses with pulmonary arterial pressures greater than 80 mm Hg.
Exactly why the pulmonary capillaries fail remains the subject of con-
siderable research, both to understand the underlying physiology of the
equine lung better and to investigate possible treatments to prevent or limit
EIPH. The interaction of various organ systems in the development of EIPH
(eg, cardiac, musculoskeletal) is the topic of many ongoing research efforts.
Currently, many investigators are of the opinion that because virtually all
horses involved in intense exercise have evidence of pulmonary hemorrhage,
EIPH may be an inevitable consequence of equine exercise [4,10,13,25,26].
 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100 91

Fig. 2. Electron micrograph of equine pulmonary capillary showing stress failure of capillary
endothelium (arrows). Note erythrocytes in alveolar space (arrowheads). c ¼ capillary lumen;
a ¼ alveolar space. Bar ¼ 2 lm. (Adapted from Birks EK, Mathieu Costello O, Fu Z, et al. Very
high pressures are required to cause stress failure of pulmonary capillaries in Thoroughbred
racehorses. J Appl Physiol 1997;82:1584–92; with permission.)

Although the effect on performance of single bouts of EIPH is con-

troversial, repeated bouts of EIPH may have a negative impact on per-
formance by means of the resultant chronic lung damage. Because of its
chronic and progressive nature, permanent damage to the lung may occur
over time secondary to local inflammatory responses, interstitial hemosider-
ophages, and increased connective tissue deposition. Hemosiderophages,
fibrosis, and destruction of lung parenchyma may occur secondary to
previous hemorrhage, red blood cells in the interstitium, and macrophage-
induced inflammation. An increase in tissue cellularity may also decrease
lung compliance. The proliferation of bronchial vasculature in these areas
may be part of the normal response to the inflammation. This resultant
inflammatory response to the blood may have more of an impact on
performance than the actual blood in the airways. This may be an area on
which to focus for therapeutic protocols limiting EIPH and its sequela.

Diagnosis
Various methods for diagnosing EIPH have been suggested. Initially,
before the advent of flexible endoscopes, the presence of blood at one or
both nostrils was needed to diagnose EIPH. Direct visualization of the
upper airways and trachea via endoscopy is now routinely used to confirm
92 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100

Fig. 3. Plot of the number of endothelial breaks per millimeter of capillary boundary in lung
samples taken from dorsal (solid circles) and ventral portions of left caudal lung lobes. Values
are means
SEM. (Adapted from Birks EK, Mathieu Costello O, Fu Z, et al. Very high
pressures are required to cause stress failure of pulmonary capillaries in Thoroughbred
racehorses. J Appl Physiol 1997;82:1584–92; with permission.)

pulmonary hemorrhage [52,53]. Although tracheal endoscopic scoring sys-

tems have been published to estimate the severity of hemorrhage [5,6,8], no
studies have shown any correlation between visual scoring score and actual
severity of EIPH.
Enumeration of erythrocytes recovered in BAL fluid has been proposed
as a method of semiquantifying the severity of EIPH [11,13]. Conflicting
reports exist as to the reproducibility of this technique, however, and there
are doubts concerning its accuracy as an indication of the severity of
pulmonary hemorrhage [27]. Recent reports have suggested that even when
endoscopically directed, quantification of erythrocytes in recovered BAL
fluid may be too variable to permit the use of this technique to compare the
severity of EIPH after repeated exercise [28–31]. In the authors’ experience,
this variability between repeated measurements can be sufficient to prevent
accurate quantification of pulmonary hemorrhage. Certainly, more experi-
ence, including evaluation under actual competition conditions, is required
to resolve these differing results.
BAL can be conducted either endoscopically (requiring an endoscope >2
m in length) or blindly with special BAL tubing. Reports suggest that a BAL
should be completed 30 to 60 minutes after exercise if erythrocyte enu-
meration is to be used to quantify EIPH. Although endoscopically guided
BAL shows ‘‘promise’’ for research purposes, it is unlikely to be commonly
accepted in racetrack veterinary practices because of time/cost constraints,
the equipment required, and the need for sedation. The primary advantage
of endoscopically guided BAL over that conducted blindly is the ability to
specifically direct the endoscope to a particular location. Direct visualization
 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100 93

Fig. 4. Relation between mean pulmonary arterial pressure (mPAP) and the number of
erythrocytes (RBC) per milliliter recovered in bronchoalveolar lavage fluid. Values are obser-
vations from an individual horse, except for n = 4 for the point representing the resting
condition (mPAP 30 mm Hg). (Adapted from Meyer TS, Fedde MR, Gaughan EM, et al.
Quantification of exercise-induced pulmonary haemorrhage with bronchoalveolar lavage.
Equine Vet J 1998;30:284–8; with permission.)

also reduces the possibility of iatrogenically induced hemorrhage, which

could confuse the diagnosis of EIPH. This technique also allows serial
comparisons of repeated BAL performed in the same area as well as reliably
permitting different areas to be evaluated. The major disadvantages are
the equipment required and the need for heavy sedation, which make the
procedure more expensive, labor-intensive, and time-consuming. The ad-
vantages to performing BAL without an endoscope are the relative ease and
minimal equipment requirements. With this method, although the tubing
generally passes to a similar location, the exact location cannot be con-
trolled. Hemosiderophages remain present in both BAL and tracheal wash
fluids for up to 3 weeks after a single EIPH episode [13,31] and can be used
to detect previous episodes of hemorrhage [31]. Recently, a quantitative
graded hemosiderin scoring system has been proposed as a sensitive method
for detecting EIPH [12]. The advantage of such a diagnostic approach is that
because the hemosiderophages are present in lavage fluid for a prolonged
time, the exact time of collection is relatively unimportant. A presumptive
diagnosis of recent (within the preceding 1–21 days) EIPH can be made if
hemosiderophages are observed in either tracheal wash or BAL fluid if no
other source of pulmonary hemorrhage can be identified. This reduces the
objections to performing BAL immediately after competition, permitting it
to be conducted at a more convenient time.
94 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100

Several imaging techniques have been suggested as diagnostic aids for

EIPH. Radiographs have been used to evaluate bleeding; however, they are
neither sensitive nor specific for EIPH or for assessing its severity [5].
O’Callaghan and Goulden [32] saw an increase in interstitial pulmonary
densities peripherally in the caudodorsal lung field, which partially to
completely obscured pulmonary vascular detail. With chronicity, a bronchial
pattern was seen superimposed over the interstitial pattern. The type of
lesion seemed to be related to the timing of the incident. Radiographic
changes may be more likely to be abnormal after repeated episodes of pul-
monary hemorrhage, reflecting chronic parenchymal damage (Fig. 5). These
radiographic findings correlated with lesions observed on postmortem
examination [14]. Nevertheless, it has not been shown that radiographic
changes correlate with clinical signs associated with EIPH. Nuclear scintig-
raphy has also been suggested as a method showing promise to detect and
quantify EIPH [14,33]. Further studies need to be performed before this can
be conclusively established, however. Because of the required equipment,
time, and expense, neither radiographic nor scintigraphic techniques are
likely to be commonly used at racetracks.
For the foreseeable future, tracheal endoscopy, with or without collection
of wash fluid, is likely to remain the primary technique used to diagnose
EIPH. Because the necessary equipment is readily available to most vet-
erinary practices associated with competitions, this procedure rarely re-
quires any more than commonly used physical restraint techniques and is
readily accepted by horse persons. Combined with the observation that most
horses show visual endoscopic evidence of bleeding, this makes tracheal
endoscopy the most likely technique to be used in the clinical diagnosis
of EIPH.

Fig. 5. Lateral radiograph of the thorax of a 5-year-old Thoroughbred racehorse taken the day
after racing, in which the horse was noted to have moderate epistaxis. Note the increased
interstitial density in the dorsocaudal lung field.
 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100 95

Pathologic findings associated with EIPH have been well described.

O’Callaghan et al [14] performed a detailed study correlating clinical, diag-
nostic, and postmortem findings so as to further describe characteristic
lesions. Previous reports supported the dorsal portion of the caudal lobe
as the most prominently affected area, with hemorrhagic lesions present
[21,34]. Mason et al [21] saw bronchiolitis and hemosiderophages in the
discolored regions that occurred bilaterally in the dorsocaudal portion of
the lung. It was suggested that this may be the source of the hemorrhage,
although EIPH had not been confirmed in all these horses. O’Callaghan et al
[14] described the collapsed lungs as having bilaterally symmetric subpleural
staining of the parenchyma. The abnormal-appearing lung was most com-
monly present in the caudal tip of the lung; however, more severely affected
horses had progressively more cranial involvement of the dorsal lung. In
collapsed lungs, the stained areas were denser in consistency and did not
collapse as completely as normal lung. These areas were slower to inflate
than normal lung. There was also an increase in density of subpleural
bronchial arteries in the abnormal areas, with air trapping scattered
throughout the dorsocaudal lung. Histologically, bronchiolitis, peribron-
chial and interstitial fibrous connective tissue, and hemosiderophages in the
interstitium and alveoli were also described.

Treatment
Virtually every trainer, owner, groom, track official, or veterinarian has
a preferred treatment for EIPH. As with any disease, whenever there are
a number of proposed treatments for a disease, it is probably the fact that
none of the treatments is universally successful. With the vast array of
suggested therapies, the treatment regimen prescribed is often determined by
what the veterinarian believes is the cause of EIPH.
The diuretic furosemide (Lasix) has been administered before racing for
almost 30 years to prevent or limit EIPH [51,57]. At the present time, all
racing Thoroughbred and Standardbred horse-racing jurisdictions in the
United States and Canada permit intravenous administration of 250 to 500
mg of furosemide 4 hours before racing. It is also commonly administered
30 to 60 minutes before strenuous training sessions worldwide. Laboratory
studies have demonstrated an attenuation of the increased pressures of the
right atrium, pulmonary artery, and pulmonary capillary associated with
exercise [23,35–37], and several recent studies have also reported a significant
reduction in EIPH (as quantified by erythrocyte counts in postexercise BAL
fluid) in horses administered furosemide before treadmill exercise [38]. Such
remarkable reductions in EIPH have not been observed after racing. Using
a visual endoscopic scoring system, numerous studies conducted after racing
have shown either a slight or no reduction in EIPH in horses administered
furosemide before racing [4,10]. Methodologic differences and/or differences
96 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100

in exercise intensity on a treadmill versus during racing may account for

these disparate results. Numerous studies have shown that furosemide
treatment can improve an individual horse’s athletic performance [3,39].
Whether or not this improved performance is related to any limitation of
EIPH is still actively debated.
The ineffectiveness of furosemide in preventing and/or limiting EIPH
is underscored by the many other treatments that have been given either
alone or in combination with furosemide. The list of such treatments is
quite extensive; some of the more popular ones include inspired water
vapor-saturated air, conjugated estrogens, coagulants, cromolyn sodium,
b2-adrenergic receptor agonists, immune products, and a plethora of
herbal/nutritional supplements [4,5,11,40,41]. Many of these have only
anecdotal reports of efficacy, and controlled studies of some of these
therapies have failed to demonstrate any significant improvement. Recently,
the antifibrinolytic drug amino caproic acid (Amicar) has been suggested
to limit EIPH, especially when used in conjunction with furosemide. Con-
trolled studies of this treatment have yet to be conducted, but based on
anecdotal reports that it does not have an effect on athletic performance,
many racing jurisdictions permit Amicar administration on the day of a race.
Nasal dilators (Flair nasal strips) similar to antisnoring strips commonly
used by people have recently been introduced to the horse industry with
claims of limiting EIPH by reducing nasal resistance to airflow. Changes in
airflow dynamics resulting from stabilizing the skin and muscles of the
external nares may alter either the location or severity of airway forces that
contribute to EIPH. Although some studies have reported significant re-
ductions in the severity of EIPH with the use of the Flair nasal strip during
treadmill exercise [11,38,56], conflicting reports exist [42,43].
Another novel therapeutic modality involves the use of nitric oxide or
nitric oxide-like compounds. If extreme pulmonary vascular pressures can
be reduced by administration of these vasodilatory agents, it would be pos-
sible to limit EIPH. Recently, conflicting results have been reported with this
mechanistic approach to reducing pulmonary blood pressure [24,44–49,55].
Further research in this area needs to be conducted to resolve these issues.
All the above-described therapeutic modalities are directed at preventing
or limiting individual EIPH episodes. Given the facts that virtually all
horses exhibit EIPH during strenuous exercise and that attempts at pre-
vention have, to date, been fairly unsuccessful, therapies aimed at limiting
the cumulative lung damage from repeated EIPH episodes may be nec-
essary. These therapies should attempt to limit the inflammatory re-
sponse to blood and hemosiderin that remain in the alveoli and interstitium
after a single episode of EIPH. Although alveolar macrophages are a
necessary part of the cellular defense mechanism of the lung and help
to promote removal of particles not cleared by the mucociliary apparatus,
they may contribute to the overall progressive nature of EIPH and the
destruction of lung parenchyma by the elaboration of inflammatory
 E.K. Birks et al / Vet Clin Equine 19 (2003) 87–100 97

products. This is an area requiring further investigation before specific

recommendations can be made.

Summary
EIPH is a condition affecting virtually all horses during intense exercise
worldwide. The hemorrhage originates from the pulmonary vasculature and
is distributed predominantly bilaterally in the dorsocaudal lung lobes. As
the condition progresses, the lung abnormalities extend cranially along the
dorsal portions of the lung. An inflammatory response occurs in association
with the hemorrhage and may contribute to the chronic sequela. Although
conflicting opinions exist as to its affect on performance, it is a syndrome
that is thought to increase in severity with age. The most commonly per-
formed method to diagnose EIPH at the present time is endoscopy of the
upper airway alone or in combination with tracheal wash analysis for the
presence of erythrocytes and hemosiderophages. Because horses may not
bleed to the same extent every time and the bleeding may originate from
slightly different locations, these diagnostic procedures may not be ex-
tremely sensitive or quantitative. At this time, there is no treatment that
is considered a panacea, and the currently allowed treatments have not
proven to be effective in preventing EIPH. Future directions for therapeutic
intervention may need to include limiting inflammatory responses to blood
remaining within the lungs after EIPH.

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