Genetic Welfare Problems of Companion Animals

English Bulldog

Brachycephalic Ocular Syndrome

Related terms: brachycephalic ocular disease, exophthalmos, exposure keratopathy, exposure keratopathy syndrome, keratitis syndrome, pigmentary keratisis, macropalpebral fissure syndrome, medial canthus syndrome

Outline: Because of their extreme brachycephalic (short) head shape and its consequences on the anatomy (shape and positioning) of the eyes and surrounding tissues, English bulldogs are prone to several eye conditions that tend to lead to chronic irritation and pain. It seems likely that prevalence of these diseases will be lower in those with less extremely abnormal head shapes (compared with more typical canine head shape).

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Summary of Information

(for more information click on the links below)

1. Brief description

Brachycephaly is the term used to describe animals that have greatly shortened upper jaws and noses. Decreased depth of the orbits (the bony eye sockets) is also common. Of the dog breeds, the English bulldog has an extreme brachycephalic head shape, with prominent nasal folds and almost complete lack of muzzle.

Brachycephalic ocular disease is the name given to a syndrome seen in brachycephalic animals that often combines lesions of the eyelid, conjunctiva (the tissues lining the eyeballs and eyelids) and cornea (the tissue forming the clear front surface to the eyeball) (Maggs et al 2008).

Dogs affected by this syndrome may show various conformational abnormalities of the eye including exophthalmos (abnormal protrusion of the eyes), macropalpebral fissure (an excessively wide opening of the eyelids compared to the size of the eye) and lagophthalmia (inability to close the eyelids completely) (Maggs et al 2008, Bedford and Jones 2001). The abnormal head shape may lead to other problems also including: lower medial entropion (inward rotation of the eyelid or eyelid fur which rubs on the eye), nasal fold trichiasis (skin fold and hairs on the nose comes in constant direct contact with the corneas), distichiasis (abnormally placed eyelashes that rub on the eye), poor tear production and/or quality (which means the cornea is more prone to damage as potential abrasive particles that come into contact with it are not washed away), pigmentary keratitis or exposure keratopathy (long term damage to the corneas), and epiphora (tears running onto the face) (Maggs et al 2008).

Depending on the type and severity of the above problems, affected dogs can show signs that include: excessive tear production (lacrimation), holding of their eyelids partially closed, excessive blinking and sensitivity to light, discharge from the eyes, inflammation and redness of the conjunctiva, damage to the cornea which may lead to partial or complete blindness, frequent rubbing at the face and eyes, and tear staining on the face. 

2. Intensity of welfare impact   

Without treatment, the various conditions, outlined above, that make up brachycephalic ocular syndrome, lead to irritation of the cornea and surrounding tissues causing constant discomfort, pain and possibly blindness.

Surgical treatments may help, although some bulldogs may need multiple operations which themselves can cause distress and discomfort. Despite surgery, many dogs will need ongoing veterinary visits and frequent topical eye medications. For some individuals both of these are difficult and distressing.

3. Duration of welfare impact

Without surgical treatment brachycephalic ocular syndrome is life-long. Surgery cannot correct all the anatomical defects involved in this syndrome. Life-long medical treatment may alleviate some signs.

4. Number of animals affected

Many English bulldogs have this condition to some degree. From data on estimates of total dog population in the UK and on the percentage of all micro-chip registered dogs that are English bulldogs (Lucy Asher, 2011, personal communication), we estimate that the UK population size of this breed may be around 50,000.

5. Diagnosis

Brachycephalic ocular syndrome is suspected in any English bulldog showing any of the signs outlined. Diagnosis of the extent and severity of the abnormalities requires thorough examination of the eyes.

6. Genetics

Brachycephalic ocular syndrome is a result of selective breeding for brachycephaly – abnormal, short-muzzled, head shape. As far as we are aware, the genetic changes that underlie this inherited defect are not fully understood but at least two genes are thought to be significantly involved.

7. How do you know if an animal is a carrier or likely to become affected?

All English bulldogs have a brachycephalic head shape therefore many are affected with brachycephalic ocular syndrome to a greater or lesser extent. Examination of any puppy prior to purchase is essential, along with its dam and sire. Dogs showing any signs of brachycephalic ocular syndrome, or whose parents have any signs or have had surgical procedures or medical treatments to alleviate the condition should not be purchased (because if there is, instead, a demand for unaffected animals, the population will soon be comprised of healthier relatives less at risk of these chronic and serious painful conditions).

8. Methods and prospects for elimination of the problem

As brachycephalic ocular syndrome is a consequence of the brachycephalic head shape, it seems unlikely that it will be possible to elimination the condition from English bulldogs without changing the conformation of the breed (and their breed standard) significantly, although it may be possible to select for lines that are less severely affected. Unfortunately, as the English bulldog is one of the most severely brachycephalic of breeds, it may be impossible to eliminate this problem, or to do so in a reasonable time, without out-crossing to breeds that are less, or are not, brachycephalic. Opinions differ as to whether it is ethically acceptable to breed animals whose welfare is likely to be compromised.

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For further details about this condition, please click on the following:
(these link to items down this page)

• Clinical and pathological effects
• Intensity of welfare impact
• Duration of welfare impact
• Number of animals affected
• Diagnosis
• Genetics
• How do you know if an animal is a carrier or likely to become affected?
• Methods and prospects for elimination of the problem
• Acknowledgements
• References

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1. Clinical and pathological effects

The term “brachycephaly” comes from the Greek words for short and head. The term applies to all breeds of dog (and cat) with short heads. The brachycephalic dog and cat breeds include: Pugs, English bulldogs, Pekingese, French bulldogs, Lhasa Apsos, Boxers, Shih Tzus, Boston terriers and Persian cats.

The brachycephalic head shape is due to an inherited defect in development of the bones of the skull (Stockard 1941). The length is markedly reduced, with severe shortening of the muzzle and skull (Stockard 1941). However, the soft tissues of the head are not similarly reduced in size. There are a number of serious medical conditions associated with the brachycephalic shape – these include brachycephalic airway obstruction syndrome (BAOS) (discussed in detail elsewhere, see BAOS in English bulldog), difficulties giving birth (see foetal pelvic disproportion in Boston terriers), dental problems caused by maxillary brachygnathism (the top jaw is abnormally short), and exophthalmos and brachycephalic ocular syndrome discussed here.

Figure 1. The brachycephalic skull is characterised by its shortening, particularly of the muzzle, and by shallow eye sockets and deformed jaw. This image depicts an English Bulldog. Similar characteristics are shown, to varying degrees, by all brachycephalic breeds. 

 

Figure 2. Comparing a brachycephalic breed  (Figure 1) with a mesocephalic (or non-brachcephalic) breed further illustrates the differences in skull conformation and highlights the shortened muzzle and excess soft tissue, leading to skin folds, in brachycephalic breeds.

(Figures 1 and 2 are property of Rowena Packer, to whom we are grateful for permission to reproduce them here).

Exophthalmos is abnormal protrusion of the eyeball and in brachycephalic breeds (Bedford and Jones 2001) it is due to the shallowness of the orbits (the bony eye sockets in the skull). Dogs with exophthalmos characteristically have large, round, prominent eyes, which leads to lagophthalmos(inability to close the eyelids completely) and macroblepharon (an exceptionally large eyelid opening). These abnormalities have come to be considered by some to be “normal” in brachycephalic dogs (Canine Inherited Disorders Database 2004, Bedford and Jones 2001).

Such anatomical abnormalities make brachycephalic breeds very prone to eye problems causing pain and chronic discomfort. The English bulldog, like some other breeds (including Pekingese, Pug and Shih Tzu) have an extreme form of brachycephaly which makes for more severe problems. Their nasal bones are so short they have little or no muzzle. The soft tissues of the head show proportionally less shrinkage and this leads to an excess of skin on the nose which folds up and these folds often come in direct contact with the prominent eyes.

Various terms are used for the ocular problems commonly seen in brachycephalic dogs: macropalpebral fissure syndrome, medical canthus syndrome and exposure keratopathy syndrome, however here these are included under the umbrella term “brachycephalic ocular syndrome”, as this seems most appropriate and all encompassing.

Figure 3.  A Pug displaying exophthalmos. The wrinkled skin around the muzzle caused by skull deformity and excess soft tissue can come in to contact with the protruding eyes resulting in irritation and abrasion of them. (Image property of Joel Mills).

 

In brachycephalic ocular syndrome, often there are lesions of the eyelid, conjunctiva (the tissues surrounding the eye and lining the eyelids) and cornea (the clear front lining of the eye). (Maggs et al 2008).

All brachycephalic dogs have, to a greater or lesser extent, exophthalmos (protruding eyeballs), macropalpebral fissure (an excessively wide opening of the eyelids), lagophthalmia (inability to close the eyelids completely) and limited passive movement of the third eyelid (Maggs et al 2008, Bedford and Jones 2001). These abnormalities can be accompanied by combinations of the following features (Maggs et al 2008):

• Lower medial entropion. Entropion is the inward rotation of the eyelid, and in this case the side of the lower eyelid nearest the nose rotates inwards causing the hairs from the face to constantly rubbing on the cornea (the clear surface of the eye) which may lead to pigmentation or ulceration of the cornea (see pigmentary keratitis below).This is common in English bulldogs (Renwick 2007). Lund (2007) suggests they are over 23 times more at risk of this than the average dog.

Figure 4. In cases of entropion - the edge of the eyelid is rolled inwards causing the hairs on the eyelid to come in to contact with the cornea. This can lead to ulceration and discomfort. In brachcephalic breeds this commonly occurs on the lower lid nearest the nose due to the excessive skin wrinkling.

 

(Image property of Susan Jacobi at www.vision4pets.com, to whom we are grateful for permission to reproduce it here).

• Nasal fold trichiasis. In this condition, the hairs of nasal skin folds come in direct contact (which can be constant) with the cornea of the eye. This leads to corneal irritation and possibly to pigmentary keratitis and ulceration as discussed below. It only occurs in the more extreme brachycephalic breeds, due to the excessive nasal skin folds on their short noses and the protrusion of the eyes (Gelatt and Peterson Gelatt 2001); in the English bulldog the problem tends to be due to prominent nasal folds rather than excessively protruding eyes.

Figure 5. An example of nasal fold trichiasis resulting in pigmentary keratitis, characterised by the discolouration of the cornea and presence of blood vessels on the eyeball.

 

 

(Image property of Susan Jacobi at www.vision4pets.com, to whom we are grateful for the permission to reproduce it here).

• Distichiasis. In this condition, abnormally growing eyelashes touch the surface of the eye (Lawson 1973), leading to irritation of the tissues, conjunctival inflammation, and chronic irritation of the cornea (see below).McCalla (no date) suggests English bull dogs are prone to this condition.

Figure 6. Distichiasis is the condition in which eyelashes grow in the direction of the surface of the eye. This is another common feature of brachycephalic ocular syndrome. The dog in this figure has not yet developed keratitis or other complications as a result of distichiasis.

 

(Image property of Susan Jacobi at www.vision4pets.com, to whom we are grateful for the permission to reproduce it here).

• Impaired pre-occular tear film dynamics (Gelatt 2001). Brachycephalic dogs are considered to have often have poor tear qualityand instability of the tear film.
• Pigmentary keratitis / exposure keratopathy and corneal ulcers.  The cornea of the eye – that is, its front surface - is normally clear. Because it usually lacks blood vessels, when it is irritated it reacts differently to other tissues. It may become cloudy, scarred, pigmented, ulcerated and have blood vessels growing into it. This is called pigmentary keratitis. All of the anatomical abnormalities outlined above that are associated with extreme brachycephaly can combine to cause this pigmentary keratitis is often not detected early by owners, as overt discomfort tends not to be noticed in brachycephalics, possibly due to decreased corneal sensitivity. However, it is usually detected once more extensive when signs of blindness become apparent.

Figure 7                                                              Figure 8

Figures 7 and 8. Pigmentary keratitis (pigmented inflammation of the cornea) occurs as a result of chronic irritation of the surface of the eye caused by the skin, eyelid and eye position abnormalities associated with brachycephalic head shape. (Images property of Susan Jacobi at wwmw.vision4pets.com, to whom we are grateful for permission to reproduce them here).

In some cases exposure keratopathy (chronic inflammation of the cornea because the eyelids do not close properly) develops. This can lead to increased risk of infection, erosion of the surface layer of the cornea and ulceration (where deeper layers of the eyeball are eroded too (Startup 1984, Renwick 1996).Brachycephalic breeds are more vulnerable to corneal damage because of inherited corneal insensitivity, which makes them less responsive to irritants that may cause damage the surface of the eye, e.g. which otherwise would be washed away by blinking and/or tear production (Gelatt 2001). Ulcers in the cornea can deepen until they cause rupture of the eyeball. Deep corneal ulcers or ruptured eyes are veterinary emergencies. Eye rupture may necessitate the surgical removal of the eye.

• Epiphora (tears running onto the face). Normally tears drain through a small opening on the inside of each lower eyelid (puncta), via a canal (the tear duct) which carries the tears into the nose. In affected animals this drainage is disrupted. Epiphora has two main causes: (i) kinking of the tear duct due to the excessive skin folding resulting from the short facial bones but normal length soft tissues), and (ii) blocking of the puncta by the large, protruding eye. Both reduce or stop drainage of tears away from the eye and lead to overflow of tears onto the face, tear-staining of the fur. The constantly wet skin may become inflamed and infected.

Figure 9. Epiphora (poor drainage of tears leading to tear staining of the face) is also associated with brachycephalic ocular syndrome. It is usually caused by excessive facial wrinkling (causing distortion of the tear duct) and/or large, protruding eyes, and can lead to further discomfort through inflammation and infection of the chronically wet skin.

(Image property of Susan Jacobi at www.vision4pets.com, to whom we are grateful for permission to reproduce it here).

• Trichiasis from the medial caruncle and conjunctiva. In this condition, abnormal hairs arising from the very corner of the eye (the angle of the eyelids) or the conjunctiva rub on the cornea and cause irritation (Krohne 2008).
• English bulldogs are also predisposed to ectropion (outward rotation of the eyelids which can lead to conjunctivitis (inflammation of the conjunctiva) and eye infections, and also with prolapse of the third eyelid gland (Rubin 1989; Lund 2007).

All the above conditions lead to chronic (long term) signs of disease which include:

• Excessive tear production (lacrimation), holding of the eyelids partially closed, and excessive blinking and sensitivity to light. These signs of pain are particularly noticeable when the cornea is ulcerated (Renwick 1996).
• Discharge from the eyes.
• Inflammation and redness of the conjunctiva (conjunctivitis).
• Opacity, or pigmentation of the cornea. The surface may look uneven.
• The dog may rub at the face and eyes; a response which is usually regarded as indicating discomfort and irritation.
• Blindness or partial blindness.  Without appropriate treatment, partial or complete blindness is a common consequence of this chronic damage to the eyes. Tear staining on the face.

Treatment of this complex syndrome requires diagnosis of all the possible underlying causes. Several surgical interventions may be necessary to tackle distichiasis, nasal fold trichiasis, entropion and macropalpebral fissure and, if successful, these may halt progression of the corneal damage (Renwick 1996). Surgical intervention may be tried to treat for pigmented and damaged corneas but pigmentation and vascularisation (abnormal presence of blood vessels in the cornea) often return post operatively so vision may not be restored (Renwick 1996, Brogdon 2005).

A life-time of medical treatments (in the form of regular eye drops or ointments) may still be necessary after surgery, in order to try to help protect the vulnerable cornea.

Like other extreme brachycephalic breeds of dog, English bulldogs are also vulnerable to damaging their eyes during normal day-to-day activities, due to the abnormal prominence of their eyes and decreased corneal sensitivity (Renwick 1996).

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2. Intensity of welfare impact

Unless successfully treated, the conditions of brachycephalic ocular syndrome lead to constant irritation of the cornea and the surrounding tissues causing prolonged and persistent discomfort and, in some cases, severe pain. Renwick (1996) found that brachycephalic breeds have a decreased corneal sensitivity, such that affected dogs show less signs of discomfort to these eye conditions compared to other dogs. However, because of this, the cornea is at greater risk of further damage because the ability to detect and perform the appropriate responses to protect the eye, such as blinking and/or tear production, are impaired.

Long-term damage to the cornea causes ulcerations (considered to cause significant pain (Renwick 1996), scarring, pigmentation and blindness and occasionally, to rupture of the eye. Blindness significantly affects a dog’s quality of life.

Surgical treatments may improve the condition, but some dogs need multiple operations and these can cause distress and discomfort. Despite surgery, many affected dogs will need ongoing veterinary attention and eye medication, administration of which for some individuals will also be difficult and distressing. This is particularly relevant for English bulldogs, as these dogs also suffer frequently from brachycephalic airway obstruction syndrome which makes them particularly vulnerable to respiratory distress as a result of the effects of stress and anaesthesia.

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3. Duration of welfare impact

Dogs with brachycephalic ocular syndrome will experience life-long affects. Depending on the nature, progress and severity of the various particular disease conditions associated with it, and the extent to which these can be surgically or medically managed, the intensity and duration of periods of associated discomfort and pain may vary. Surgical and medical treatments can often improve the situation, but are unlikely to result in complete cures.

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4. Number of animals affected

Brachycephalic ocular syndrome is intimately connected with the breed characteristics in English bulldogs, and many dogs of this breed have the condition to a greater or lesser extent. In a large, epidemiological study from the USA, English bulldogs were found to be over 23 times more at risk of entropion than their control population ie an average dog and 13 times more at risk of ectropion and 9.9 times more at risk of prolapse of the third eyelid gland. However, exact figures on the prevalence of these conditions in English bulldogs are, as far as we are aware, unavailable. From data on estimates of total dog population in the UK and on the percentage of all micro-chip registered dogs that are English bulldogs (Lucy Asher, 2011, personal communication), we estimate that the UK population size of this breed may be around 50,000.

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5. Diagnosis

Brachycephalic ocular syndrome would be suspected in any English bulldog showing any of the signs detailed above. Diagnosis of the extent and severity of the abnormalities requires thorough examination of the eyes.

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6. Genetics

Brachycephalic head shape has long been thought to be the result of an inherited defect (Stockard 1941). Recently the region of the canine genome associated with brachycephaly has been identified. The genes involved are currently unknown but 2 have been implicated (Bannasch et al 2010). The English bulldog, like some other brachycephalic breeds, has been selected for extreme exaggeration of this shape, with lack of a muzzle and prominent nasal skin folds and these features lead to the brachycephalic ocular syndrome in this breed.

A separate polygenic inheritance is suspected for entropion, ectropion (Gelatt 2007, ACVO Genetics Committee 2007) and some form of genetic inheritance is also suspected for macroblepharon (Rubin 1989, ACVO Genetics Committee 2007).

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7. How do you know if an animal is a carrier or likely to become affected?

As the English bulldog is defined by its brachycephalic head shape, all English bulldogs are affected by the inherited defect which causes brachycephaly. As many English bulldogs have some degree of brachycephalic ocular syndrome it may be difficult to identify a puppy that will be free of this condition. Anyone wishing to obtain an English bulldog should ensure that it and its sire and dam are free of signs of brachycephalic ocular disease and that they have not had corrective surgery or medical treatment for the syndrome.

Currently, identifying individuals that have had surgery may be difficult and, in order to tackle this welfare problem, there appears to be a good case for neutering all animals that require corrective surgery. Dogs which have shown any signs of brachycephalic ocular syndrome or have had corrective surgery for it should not be bred from. Purchasing such affected dogs is likely to help perpetuate the welfare problem (because if there is no demand for affected animals, the population will soon be comprised of healthier relatives less at risk of these chronic and serious painful conditions).

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8. Methods and prospects for elimination of the problem

Selection for the distorted, brachycephalic head shape has resulted in the primary anatomical abnormalities that cause brachycephalic ocular syndrome. The practices of Caesarean section and artificial insemination have enabled selection for extreme forms of this defect (Bannasch et al 2010).

Recently there has been debate, about the morality of breeding animals with exaggerated anatomical features that can cause suffering. The brachycephalic head shape is one of the examples that has been highlighted (Rooney & Sargan 2008). The UK Kennel Club’s breed standard for English bulldogs was updated in 2010 and is available at http://www.thekennelclub.org.uk/item/155.  This Kennel Club instigated a ‘breed watch’ for heavy nasal folds and entropion or ectropion (UK Kennel Club 2011).Breed standards do vary worldwide.

The English bulldog is a severely affected breed and it may be impossible to eliminate this problem, or to do so in a reasonable time, without out-crossing to breeds that are either less brachycephalic, or not brachycephalic at all. Opinions differ as to whether it is ethically acceptable to breed animals whose welfare is likely to be compromised.

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9. Acknowledgements

UFAW is grateful to Rosie Godfrey BVetMed MRCVS and David Godfrey BVetMed FRCVS for their work in compiling this section and to Stephanie Kaufman for assistance in illustrating it.

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10. References

ACVO Genetics Committee (2007) Ocular disorders presumed to be inherited in purebred dogs, 5th Ed

Bannasch D, Young A, Myers J, Truvé K, Dickinson P et al (2010) Localization of Canine Brachycephaly Using an Across Breed Mapping Approach. PLoS ONE 5(3): e9632. doi:10.1371/journal.pone.0009632

Bedford P and Jones G (2001) Abnormal appearance in R Pieffer and S Peterson Jones (Eds) Small animal ophthalmology: a problem oriented approach. 3rd Ed. Saunders: Philadelphia

Brogdon JD (2005) Corneal Wound Healing. Atlantic Coast Veterinary Conference 2005. Available via VIN Associate. Accessed 31.1.11

Canine Inherited Disorders Database (2004) What is exposure keratopathy syndrome? Available from http://www.upei.ca/cidd/Diseases/ocular%20disorders/exposure%20keratopathy%20syndrome.htm. Accessed 1.2.11

Krohne S (2008) Medial canthus syndrome in dogs – chronic tearing, pigment, medial entropion and Trichiasis. Chronic Diseases – Proceeding of a Symposium Sponsored by Schering-Plough Animal Health. Available from: www.hungarovet.com/wp-content/uploads/2009/.../chronic-tearstaining.pdf.  Accessed 31.1.11

Lund E (2007) Eyelid disease: All dogs are not equal. Data Savant July/ August: 16-20

Gelatt K (2001) Colour altas of veterinary ophthalmology. Lippincott, Williams & Wilkins: Baltimore, USA

Gelatt K (2007) Veterinary Ophthalmology, 4th Ed. Blackwell Publishing, Oxford, UK

Gelatt K and Peterson Gelatt J (2001) Small animal ophthalmic surgery: practical techniques for the veterinarian. Elsevier Science Ltd; Edinburgh

Lawson DD (1973) Canine distichiasis. Journal of Small Animal Practice 14: 469-8

Maggs D, Miller P, Ofri R and Slatter D (2008) Slatter’s Fundamentals of Veterinary Opthamology. 4th Ed. Elsevier Health Sciences: Edinburgh, UK

McCalla T (no date) Macropalpebral Fissure Syndrome. (On-line) Available at http://www.animaleyecare.net/diseases/macropalpebral.htm. Accessed 1.2.11.

Renwick P (1996) Diagnosis and treatment of corneal diseases in dogs. In Practice 18: 315-328

Renwick P (2007) Eyelid surgery in dogs. In Practice 29: 256-271

Rooney N and Sargan D (2008) Pedigree dog breeding in the UK: a major welfare concern? An independent report commissioned by the RSPCA. Available from www.rspca.org.uk/pedigree dogs. Accessed 1.2.11.

Rubin L (1989) Inherited eye diseases in purebred dogs. Williams and Wilkins, Baltimore, USA

Startup F (1984) Corneal ulceration in the dog. Journal of Small Animal Practice 25: 737-752

Stockard (1941)Wistar Institute Monograph. The genetic and endocrine basis for differences in form and behaviour as elucidated by studies of contrasted pure line dog breeds and their hybrids. Animal Anatomical Memoirs No 19,The Wistar Institute

The Kennel Club (UK) (2010) English bulldog Breed Standard. Available from http://www.thekennelclub.org.uk/item/155 Accessed 6.4.11

The Kennel Club (UK) (2011) Breed Watch information for the English bulldog. Available from: http://www.the-kennel-club.org.uk/services/public/breeds/watch/display.aspx?breed=Bulldog. Accessed 6.4.11

© UFAW 2011

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Credit for main photo above:

By Asmadeus (Own work) [Public domain], via Wikimedia Commons