Exercise induced pulmonary hemorrhage

Pulmonary hemorrhage

Pulmonary hemorrhage is an acute bleeding from the lung, especially in the upper respiratory tract and the endotracheal tube. When evident clinically, the condition is usually massive, associated with bleeding in other sites as well as more than one third of the lungs...

(EIPH), also known as "bleeding" or a "bleeding attack", refers to the presence of blood in the airways of the lung in association with exercise. EIPH is common in horse

Horse

The horse is one of two extant subspecies of Equus ferus, or the wild horse. It is a single-hooved mammal belonging to the taxonomic family Equidae. The horse has evolved over the past 45 to 55 million years from a small multi-toed creature into the large, single-toed animal of today...

s undertaking intense exercise, but it has also been reported in human athletes, racing camel

Camel racing

Camel racing is a popular sport in India, Pakistan, Saudi Arabia, Egypt, Bahrain, Jordan, Qatar, United Arab Emirates, Oman, Australia, and Mongolia. Professional camel racing, like horse racing, is an event for betting and tourist attraction...

s and racing greyhound

Greyhound

The Greyhound is a breed of sighthound that has been primarily bred for coursing game and racing, and the breed has also recently seen a resurgence in its popularity as a pedigree show dog and family pet. It is a gentle and intelligent breed...

s. Horses that experience EIPH may also be referred to as “bleeders” or as having “broken a blood vessel”. In the majority of cases EIPH is not apparent unless an endoscopic examination of the airways is performed following exercise. However, a small proportion of horses may show bleeding at the nostrils after exercise, which is known as epistaxis.

EIPH in Horses

EIPH has been reported to occur in a variety of race horse

Horse racing

Horse racing is an equestrian sport that has a long history. Archaeological records indicate that horse racing occurred in ancient Babylon, Syria, and Egypt. Both chariot and mounted horse racing were events in the ancient Greek Olympics by 648 BC...

 breeds including racing Thoroughbreds (both racing on the flat and over jumps) , American Quarter Horses (incidence of 50-75%), Standardbreds (incidence of 40-60%), Arabians

Arabian horse

The Arabian or Arab horse is a breed of horse that originated on the Arabian Peninsula. With a distinctive head shape and high tail carriage, the Arabian is one of the most easily recognizable horse breeds in the world. It is also one of the oldest breeds, with archaeological evidence of horses...

, and Appaloosa

Appaloosa

The Appaloosa is a horse breed best known for its colorful leopard-spotted coat pattern. There is a wide range of body types within the breed, stemming from the influence of multiple breeds of horses throughout its history. Each horse's color pattern is genetically the result of various spotting...

s. EIPH has also been reported in eventers, jumpers

Show jumping

Show jumping, also known as "stadium jumping," "open jumping," or "jumpers," is a member of a family of English riding equestrian events that also includes dressage, eventing, hunters, and equitation. Jumping classes commonly are seen at horse shows throughout the world, including the Olympics...

, polo ponies

Polo

Polo is a team sport played on horseback in which the objective is to score goals against an opposing team. Sometimes called, "The Sport of Kings", it was highly popularized by the British. Players score by driving a small white plastic or wooden ball into the opposing team's goal using a...

, endurance horses

Endurance riding

Endurance riding is an equestrian sport based on controlled long-distance races. It is one of the international competitions recognized by the FEI. There are endurance rides worldwide....

, draft horse

Draft horse

A draft horse , draught horse or dray horse , less often called a work horse or heavy horse, is a large horse bred for hard, heavy tasks such as ploughing and farm labour...

s that pull competitively

Horse pulling

Horse pulling is a draft horse competition where horses in harness, usually one or two animals, pull a stone-boat or weighted sled and the winner is the team or animal that can pull the most weight for a short distance....

, and horses taking part in Western speed events

Western riding

Western riding is a style of horseback riding which evolved from the ranching and warfare traditions brought to the Americas by the Spanish Conquistadors, and both equipment and riding style evolved to meet the working needs of the cowboy in the American West...

 such as reining

Reining

Reining is a western riding competition for horses where the riders guide the horses through a precise pattern of circles, spins, and stops. All work is done at the lope and gallop; the fastest of the horse gaits...

, cutting

Cutting (sport)

Cutting is an equestrian event in the western riding style where a horse and rider are judged on their ability to separate a single animal away from a cattle herd and keep it away for a short period of time.-Description:...

 and barrel racing

Barrel racing

Barrel racing is a rodeo event in which a horse and rider attempt to complete a clover-leaf pattern around preset barrels in the fastest time. Though both boys and girls compete at the youth level and men compete in some amateur venues, in collegiate and professional ranks, it is primarily a rodeo...

. EIPH is now considered to be an inevitable consequence of moderate to intense exercise in horses and other athletic animals. The lowest intensities of exercise which have been reported to cause EIPH are intense trotting (40-60% maximal oxygen uptake) and cantering at speeds of 16–19 mph (7.2–8.5 ).

It occurs less frequently in stallions than mares

Mareš

Mareš is a Czech surname and may refer to:* František Mareš, Czechoslovak professor of physiology and philosophy, and nationalist politician* Jakub Mareš, Czech football player* Jaroslav Mareš, Czech biologist, traveller and writer....

 or geldings, but it is associated with airway inflammation

Recurrent Airway Obstruction

Recurrent airway obstruction, also known as broken wind, heaves, or sometimes by the term usually used for humans , is a respiratory disease in horses...

 and increasing age.

The affliction occurs when blood

Blood

Blood is a specialized bodily fluid in animals that delivers necessary substances such as nutrients and oxygen to the cells and transports metabolic waste products away from those same cells....

 enters the air passages of a horse's lung

Lung

The lung is the essential respiration organ in many air-breathing animals, including most tetrapods, a few fish and a few snails. In mammals and the more complex life forms, the two lungs are located near the backbone on either side of the heart...

, due to fractured lung capillaries. Blood is sometimes evident discharging from a horse's nostrils (epistaxis), however, epitaxis usually only occurs in 5% of bleeders. If a horse does not exhibit epistaxis but is suspected to have EIPH, an endoscopic exam

Endoscopy

Endoscopy means looking inside and typically refers to looking inside the body for medical reasons using an endoscope , an instrument used to examine the interior of a hollow organ or cavity of the body. Unlike most other medical imaging devices, endoscopes are inserted directly into the organ...

 is performed soon after the horse is exercised.

Prevalence of EIPH in Horses

Based on surveys of horses examined endoscopically following racing, around 40 to 70% of horses have been reported to have blood in the trachea

Vertebrate trachea

In tetrapod anatomy the trachea, or windpipe, is a tube that connects the pharynx or larynx to the lungs, allowing the passage of air. It is lined with pseudostratified ciliated columnar epithelium cells with goblet cells that produce mucus...

 following a single post-race examination. One of the more recent and larger studies found an overall prevalence of just under 60%. The time at which the examination is carried out can determine whether or not blood is seen. The usual time for examination is 30–40 minutes following exercise. If examination is carried out too soon after exercise then blood may not have progressed from the dorso-caudal (top and back) of the lung into the trachea. If the examination is carried out too long after exercise then any blood may have moved up the trachea and been swallowed and therefore not be visible at the time of examination. In one study (Birks et al. 2002), when horses were endoscoped on at least three separate occasions following racing, all horses had blood in the trachea on at least one occasion.

Epistaxis (blood coming from one or both nostrils) is much less common. In a survey of over 220,000 horse starts in UK Flat and National Hunt (jump) racing, 185 cases of epistaxis were identified giving a frequency of 0.83/1000 starts. Similar frequencies have been reported for epistaxis in Japan (1.5 per 1000 starts) and South Africa (1.65 per 1000 starts). However a study of racehorses in Korea reported a much higher frequency (8.4 per 1000 starts).

It is believed that nearly all horses experience EIPH when exposed to strenuous exercise, and it has the potential to decrease lung function over time. However, there are no documented cases of bleeding in wild horses when rounded up with helicopters from mountain tops in pens miles away.

Clinical signs

Epistaxis is diagnosed when blood is visible at either or both nostrils during or following exercise. To confirm whether the blood is from the upper or lower airway requires further examination by endoscopy, although in some cases it is not possible to determine the location. In the majority of epistaxis cases, the blood originates from the lung. Epistaxis during or following exercise can less commonly occur as a result of upper airway hemorrhage, for example following head trauma. Poor athletic performance, frequent swallowing and coughing in the immediate post-exercise recovery period may be suggestive of EIPH. But, a definitive diagnosis can only be made by endoscopic examination of the trachea. In the case where no blood is visible in the trachea, EIPH in the small airways may still be present and can be confirmed by a broncho-alveolar lavage.

Endoscopy

EIPH is most commonly diagnosed by endoscopic

Endoscopy

Endoscopy means looking inside and typically refers to looking inside the body for medical reasons using an endoscope , an instrument used to examine the interior of a hollow organ or cavity of the body. Unlike most other medical imaging devices, endoscopes are inserted directly into the organ...

 examination of the trachea

Vertebrate trachea

In tetrapod anatomy the trachea, or windpipe, is a tube that connects the pharynx or larynx to the lungs, allowing the passage of air. It is lined with pseudostratified ciliated columnar epithelium cells with goblet cells that produce mucus...

 following exercise although a small proportion of horses will have blood at the nostrils (epistaxis) during or following intense exercise. Sometimes epistaxis may not be apparent until the horse has lowered its head, aiding drainage of the blood. In severe cases blood may be visible in the trachea immediately upon endoscopic examination soon after exercise. The most common current practice is to perform endoscopy of the trachea around 30–60 minutes after exercise. As the hemorrhage most commonly originates in the dorsal caudal (top-back) part of the lung it may not appear in the trachea immediately. With time it may travel to the trachea under the influence of mucociliary clearance, gravity and ventilation. Blood may be visible in the trachea for several days following a bout of intense exercise and moderate to severe EIPH. The amount of blood visible in the trachea at the time of examination is most commonly graded on a 0 (no blood) to 4 (airways awash with blood) scale.

Bronchoalveolar lavage (BAL)

If blood is not visible in the trachea, then examination of the smaller airways in the lung may reveal hemorrhage. In this procedure sedation is commonly used and the endoscope is advanced past the carina into the smaller bronchi. Local anaesthetic is usually instilled into the airways to reduce coughing. BAL is performed and if a horse has experienced EIPH then the fluid that is recovered can be observed to be pink or red in colour. This fluid can be submitted for cytopathogy and the number of red blood counted. Whereas scoring of the amount of blood during endoscopic examination of the trachea is semi-quantitative, quantitative counts of the numbers of red blood cells in BAL represent a quantitative estimate of the severity of EIPH. BAL red blood cell counts are more sensitive for detecting EIPH than visualisation of blood in the trachea, but may be less useful in the case of severe hemorrhage.

Cytopathology

Even if blood is not visible in the airways, two types of cells that can be seen under cytological

Cytology

Cytology means "the study of cells".Cytology is that branch of life science, which deals with the study of cells in terms of structure, function and chemistry.Based on usage it can refer to:...

 examination of either a tracheal wash or bronchoalveolar sample can indicate that EIPH has occurred. It may be possible to visualise red blood cells directly under a microscope. The number of red blood cells present can be quantified using a haemocytometer. Whilst some red blood cells may be present in a lung wash sample, this is normally very low and in the order of less than 10 red blood cells/ul of fluid. In the case of EIPH, the numbers will be several magnitudes or more higher. The presence of high numbers of hemosiderophages also indicate that hemorrhage has occurred in the lung at some time in the past. Hemosiderophages are alveolar macrophage

Macrophage

Macrophages are cells produced by the differentiation of monocytes in tissues. Human macrophages are about in diameter. Monocytes and macrophages are phagocytes. Macrophages function in both non-specific defense as well as help initiate specific defense mechanisms of vertebrate animals...

s that have ingested and digested red blood cells from previous episodes of EIPH. The end product of the digestion of the red blood cells is an iron-storage complex known as hemosiderin

Hemosiderin

thumb|Hemosiderin image of a kidney viewed under a microscope. The brown areas represent hemosiderinHemosiderin or haemosiderin is an iron-storage complex. It is always found within cells and appears to be a complex of ferritin, denatured ferritin and other material...

.

Radiography

Radiography of the chest to image the lungs has limited use in detecting either acute EIPH or damage to the lung as a result of repeated episodes of EIPH. The main benefit of taking chest radiographs as part of the clinical investigation of EIPH is to rule out other disease conditions.

Pulmonary scintigraphy

Pulmonary scintigraphy may detect moderate to severe alterations in the perfusion and possibly ventilation of the dorso-caudal lung (O‘Callaghan et al., 1987). The use of radio-labelled red blood cells and scintigraphy to localise and or quantify hemorrhage is not useful due to general sequestration of labeled RBC by the lung, even in the absence of hemorrhage.

Post mortem

Lungs of horses that have experienced repeated episodes of EIPH show a characteristic blue-gray-brown staining when examined post mortem. The staining is due to the presence of haemosiderin. The staining is usually most intense in the dorso-caudal region of the left and right diaphragmatic lobes. There are often distinct borders between healthy lung tissue and those parts of the lungs that have been affected by EIPH.

Etiology

A variety of different causes of EIPH have been proposed. These include high pulmonary vascular pressure, upper airway obstruction, mechanical trauma, lower airway obstruction, inflammation, abnormalities of blood coagulation, inhomogeneity of ventilation and locomotory trauma. To date most theories have been unable to explain why EIPH occurs in the dorso-caudal lung and the pattern of progression in a cranial direction.

High pulmonary blood pressures

The most widely accepted theory at present is that high transmural pressures lead to pulmonary capillary stress failure. Pulmonary capillary transmural pressure is determined by pulmonary capillary pressure and airway pressure. The horse has very high pulmonary vascular pressures during intense exercise; commonly exceeding 100mmHg in the pulmonary artery during intense exercise. During expiration the high positive pressures in the pulmonary blood vessels pushing out are opposed by high positive airway pressures pushing back and this does not place undue stress on the thin blood vessel walls. During inspiration the high positive pressures in the pulmonary blood vessels pushing out are met by negative pressures distending the blood vessel and placing increased stress on the walls.
Studies in vitro have demonstrated that significant disruption of the pulmonary capillaries occurs at pressures of approximately 80 mmHg. In vivo it has also been shown that significant EIPH occurs above a mean pulmonary artery pressure of around 80-95 mmHg. On the basis of this theory, any factor or disease that would increase pulmonary vascular pressures (e.g. hypervolaemia) or increase the magnitude of the negative pressures in the lung during inspiration (e.g. dynamic upper airway obstruction) would be expected to increase the severity of EIPH. But neither experimentally induced laryngeal hemiplegia nor dorsal displacement of the soft palate increased pulmonary capillary transmural pressure.

Locomotory associated trauma

An alternative theory for EIPH is based on locomotory forces. The theory is based on the fact that during galloping, the absence of any bone attachment of the forelegs to the spine in the horse causes the shoulder to compress the cranial rib cage (Schroter et al. 1998). The compression of the chest initiates a pressure wave of compression and expansion which spreads outwards. However, due to the shape of the lung and reflections off the chest wall, the wave of expansion and compression becomes focussed and amplified in the dorso-caudal lung (Schroter et al. 1999). The alternate expansion and compression at the microscopic level in adjacent areas of lung tissue creates shear stress and capillary disruption. The theory predicts that haemorrhage would be more severe on hard track surfaces.

Veno-Occlusive remodelling

A new proposal as to how high pulmonary venous pressures lead to the capillary rupture and the tissue changes observed has recently been proposed. Regional veno-occlusive remodeling, especially within the caudodorsal lung fields, contributes to the pathogenesis of EIPH, with the venous remodeling leading to regional vascular congestion and hemorrhage, hemosiderin accumulation, fibrosis, and bronchial angiogenesis.
EIPH is most likely a multi-factorial condition involving airway, vascular, cardiac and locomotory components.

Risk Factors for EIPH

Whilst all horses undertaking intense exercise experience some degree of EIPH, some horses consistently experience greater haemorrhage and other horses experience isolated episodes of increased EIPH. In the case of horses that consistently demonstrate greater severity of EIPH this is most likely due to congenital factors, such as very high pulmonary vascular pressures. In horses that experience isolated episodes of increased severity of EIPH, possible contributing factors may include, amongst others, pulmonary infection or atrial fibrillation.

Effects of EIPH on Performance

Epistaxis has been shown to have a marked negative effect on performance. However the effects of endoscopically diagnosed EIPH on performance have been less clear, with conflicting studies reporting a negative, none, and in some cases a positive effect on performance. While single bouts of EIPH may not even be apparent to the rider, owner or trainer of a horse unless an endoscopic examination is undertaken, the effect on performance within a single race appears to be significant but relatively subtle. In a 2005 study, horses finishing races with grade 4 EIPH were on average 6 metres behind those finishing with grade 0. However, the effect of repeated bouts of EIPH that occur with daily training may lead to more significant changes and a greater degree of tissue damage over time with consequent loss of lung function.

Management and Treatment

A wide variety of treatments have been used or suggested for treatment of EIPH, including resting, anti-inflammatories (e.g. corticosteroids), bronchodilators, anti-hypertensive agents (including nitric oxide donors and phosphodiesterase inhibitors), conjugated estrogens (e.g. Premarin

Premarin

Premarin is the commercial name for a compound cream of vaginally administered estrogens, consisting primarily of conjugated estrogens. Isolated from mares' urine , it is manufactured by Wyeth Pharmaceuticals and has been marketed since 1942...

), antifibrinolytic

Antifibrinolytic

Antifibrinolytics, such as aminocaproic acid and tranexamic acid are used as inhibitors of fibrinolysis. These lysine-like drugs interfere with the formation of the fibrinolytic enzyme plasmin from its precursor plasminogen by plasminogen activators which takes place mainly in lysine rich areas...

s (e.g. aminocaproic acid and tranexamic acid), snake venom, aspirin, vitamin K, bioflavinoids, diuretics (e.g. furosemide

Furosemide

Furosemide or frusemide is a loop diuretic used in the treatment of congestive heart failure and edema. It is most commonly marketed by Sanofi-Aventis under the brand name Lasix...

, known as Lasix or Salix), nasal strips (e.g. FLAIR™ Nasal Strips), concentrated equine serum (CES) and omega-3 fatty acids. Both the FLAIR Strips and the diuretic furosemide have been shown to have similar efficacy in reducing EIPH under laboratory and field conditions. A single study has shown that concentrated equine serum also reduced EIPH. There is currently no evidence to suggest that rest, bronchodilators, anti-inflammatory drugs, bioflavinoids, oestrogens, antifibrinolytics, aspirin, phosphodieterase inhibitors or surgical correction of upper airway obstructions reduce EIPH. In contrast, nitric oxide and aminocaproic acid have been shown to worsen EIPH.

Furosemide

Furosemide

Furosemide or frusemide is a loop diuretic used in the treatment of congestive heart failure and edema. It is most commonly marketed by Sanofi-Aventis under the brand name Lasix...

 (Lasix) has been used to prevent the condition, although it does not work in 50% of cases, and it is banned in some countries. Other treatments that have been used include bronchodilator

Bronchodilator

A bronchodilator is a substance that dilates the bronchi and bronchioles, decreasing resistance in the respiratory airway and increasing airflow to the lungs. Bronchodilators may be endogenous , or they may be medications administered for the treatment of breathing difficulties...

s, coagulants, and estrogen

Estrogen

Estrogens , oestrogens , or œstrogens, are a group of compounds named for their importance in the estrous cycle of humans and other animals. They are the primary female sex hormones. Natural estrogens are steroid hormones, while some synthetic ones are non-steroidal...

.

Sources

• Doucet, M. Y. and L. Viel (2002). "Clinical, radiographic, endoscopic, bronchoalveolar lavage and lung biopsy findings in horses with exercise-induced pulmonary hemorrhage." Can Vet J 43(3): 195-202.
• Epp, T.S., McDonough, P., Padilla, D.J., Gentile, J.M., Edwards, K.L., Erickson, H.H. and Poole, D.C. (2006) Exercise-induced pulmonary haemorrhage during submaximal exercise. Equine Vet J Suppl, 502-507.
• Hackett, R.P., Ducharme, N.G., Ainsworth, D.M., Erickson, B.K., Erb, H.N., Soderholm, L.V. Jr and Thorson, L.M. (1999) Effects of extrathoracic airway obstruction on intrathoracic pressure and pulmonary artery pressure in exercising horses. Am J Vet Res. 1999 Apr;60(4):485-94.
• Hillidge CJ, Lane TJ, Whitlock TW. Exercise-induced pulmonary hemorrhage in the racing Appaloosa horse. J Equine Vet Sci 1985;5:351–353.
• Hinchcliff, K. W., M. A. Jackson, et al. (2005). "Association between exercise-induced pulmonary hemorrhage and performance in Thoroughbred racehorses." J Am Vet Med Assoc 227(5): 768-74.
• Jackson, J.A., Ducharme, N.G., Hackett, R.P., Rehder, R.S., Ainsworth, D.M., Shannon, K.J., Erickson, B.K., Erb, H.N., Jansson, N., Soderholm, L.V. Jr and Thorson, L.M. (1997) Effects of airway obstruction on transmural pulmonary artery pressure in exercising horses. Am J Vet Res. 1997 Aug;58(8):897-903.
• Kim, B., Hwang, Y.K., Kwon, C.J. and Lim, Y.J. (1988) Survey on incidence of exercise induced pulmonary haemorrhage (EIPH) of Thoroughbred racehorses at Seoul Racecourses. Korean J. Vet. Clin. Med. 15, 417-426.
• Langsetmo, I., Meyer, M.R. and Erickson, H.H. (2000) Relationship of pulmonary arterial pressure to pulmonary haemorrhage in exercising horses. Equine Vet J 32, 379-384.
• Lapointe, J. M., A. Vrins, et al. (1994). "A survey of exercise-induced pulmonary haemorrhage in Quebec standardbred racehorses." Equine Vet J 26(6): 482-5.
• MacNamara, B., S. Bauer, et al. (1990). "Endoscopic evaluation of exercise-induced pulmonary hemorrhage and chronic obstructive pulmonary disease in association with poor performance in racing Standardbreds." J Am Vet Med Assoc 196(3): 443-5.
• Mason, D. K., E. A. Collins, et al. (1983). Exercise-induced pulmonary haemorrhage in horses. 1st International Conference on Equine Exercise Physiology, Oxford, UK.
• Meyer, T.S., Fedde, M.R., Gaughan, E.M., Langsetmo, I. and Erickson, H.H. (1998) Quantification of exercise-induced pulmonary haemorrhage with bronchoalveolar lavage. Equine Vet J 30, 284-288.
• Newton, J. R., K. Rogers, et al. (2005). "Risk factors for epistaxis on British racecourses: evidence for locomotory impact-induced trauma contributing to the aetiology of exercise-induced pulmonary haemorrhage." Equine Vet J 37(5): 402-11.
• Pascoe, J. R., G. L. Ferraro, et al. (1981). "Exercise-induced pulmonary hemorrhage in racing thoroughbreds: a preliminary study." American Journal of Veterinary Research 42: 703-707.
• Raphel, C. F. and L. R. Soma (1982). "Exercise-induced pulmonary hemorrhage in Thoroughbreds after racing and breezing." Am J Vet Res 43(7): 1123-7.|publisher=Equistar Publications|isbn=0965446115|date=2004-06-14}}
• Roberts, C.A., Hillidge, C. and Marlin, D.J. (1993) Exerciseinduced pulmonary haemorrhage in racing thoroughbreds in Great Britain. 1st International EIPH Conference, Guelph, Canada, p11.
• Rohrbach, B. W. (1990). "Exercise-induced pulmonary hemorrhage, chronic obstructive pulmonary disease, and racing performance." J Am Vet Med Assoc 196(10): 1563-4.
• Saulez, M.N. (2007) An endoscopic and immunopathological study of respiratory tract disorders in Thoroughbred racehorses. PhD Thesis, Faculty of Veterinary Science, University of Pretoria, South Africa.
• Speirs, V. C., J. C. van Veenendaal, et al. (1982). "Pulmonary haemorrhage in standardbred horses after racing." Aust Vet J 59(2): 38-40.
• Votion

Additional reading

• Birks, E.K., Durando, M.M. and McBride S. (2003) Exercise-induced pulmonary hemorrhage. Vet Clin North Am Equine Pract. Apr;19(1):87-100.

• Epp, T. S. E., K.L.Poole, D.C.Erickson, H.H. (2008). "Effects of conjugated oestrogens and aminocaproic acid upon exercise-induced pulmonary haemorrhage (EIPH)." Comparative Exercise Physiology 5: 95-103.
• Foord, A.J. (1994) Survey of exercise-induced pulmonary haemorrhage as perceived by veterinarians and racehorse trainers in Great Britain. Undergraduate Thesis, Warwickshire College.
• Hinchclif, K.W. (2007) Exercise-Induced Pulmonary Haemorrhage in Equine Respiratory Medicine and Surgery, eds McGorum, Dixon, Robinson and Schumacher, Saunders Elsevier, page 620-621.
• O'Callaghan, M.W., Pascoe, J.R., O'Brien, T.R., Hornof, W.J. and Mason, D.K. (1987) Exercise-induced pulmonary haemorrhage in the horse: results of a detailed clinical, post-mortem and imaging study. VI. Radiological/pathological correlations. Equine Vet J 19, 419-422.
• Schroter, R.C., Marlin, D.J. and Denny, E. (1998) Exercise-induced pulmonary haemorrhage (EIPH) in horses results from locomotory impact-induced trauma - a novel, unifying concept. Equine Vet J, 30(3), 186-192.
• Schroter, R.C., Leeming, A., Denny, E., Bharath, A. and Marlin, D.J. (1999) Modelling impact initiated wave transmission through lung parenchyma in relation to the aetiology of exercise-induced pulmonary haemorrhage. Equine Vet J Suppl 30, 34-38.