Small brachycephalic breeds are especially popular currently. Based on Kennel Club figures, in the 10 years between 2010 and 2019 there was a significant increase in Kennel Club registrations, with a 1527% increase in French Bulldog registrations (Kennel Club, 2020).
The neonatal appearance of the breeds (enlarged forehead, eyes, and head size relative to the trunk) may be at least part of the reason these dogs are found attractive (Sternglanz et al, 1977; Packer et al, 2017). Facial morphology may increase the frequency of eye disorders (Packer et al, 2015a), and ophthalmological disease is the most prevalent group-level disease in Pugs (16.25% prevalence) with corneal disorder being the second most prevalent diagnosis-level disorder (8.72%) after obesity (O‘Neill et al, 2016).
What is brachycephalic ocular syndrome?
The term brachycephalic ocular syndrome (BOS) is used to describe the eye problems, associated with conformation (exophthalmia, shallow orbit, lagophthalmia, euryblepharon, trichiasis, medial lower lid entropion, exoptropia and involution of the medial canthus) in small brachycephalic breeds such as the Pug or French bulldog. These dogs often present with poor corneal health and poor-quality tear films (Carrington et al. 1989; Krohne, 2008; Stades and Van Der Woerdt, 2013) (Figure 1).
The problems associated with BOS
BOS may result in corneal disease such as ulceration and pigmentation. In addition, the eyes are more vulnerable to proptosis.
Brachycephalic breeds have been reported to be up to 20 times more likely to be affected by corneal ulceration than non-brachycephalic breeds (Packer et al, 2015a). Corneal rupture and loss of the eye is a likely sequela to ulceration unless appropriately treated (Figure 2).
Corneal pigmentation
Corneal pigmentation is regarded as a symptom, developing as a result of irritating stimuli, such as chronic abrasion, as part of wound healing or keratoconjunctivitis sicca (Labelle et al, 2013). The incidence of corneal pigmentation in Pugs is high: 82.4% of Pugs in one study (Labelle et al, 2013) and 91.9% in another study (Maini et al, 2019) (Figures 3 and 4). Corneal pigmentation may be a genetic disease in Pugs modified by other factors (Labelle et al, 2013). The exact risk factors for corneal pigmentation are uncertain, for example associations with ocular discharge, registration status (registered dogs being more likely to have pigmentation), sex (spayed female Pugs being less likely to have pigmentation) and coat colour (fawn Pugs being more likely to have corneal pigmentation) (Labelle et al, 2013), and age (Maini et al, 2019) have been suggested. Entropion has been found to be associated with corneal pigmentation in one study (Maini et al., 2019) but not others (Labelle et al, 2013; Krecny et al, 2015).
Proptosis
The shallow orbits and minimal bony protection of brachycephalic breeds’ eyes means they proptose readily (Gilger et al 1995), often during minor fights with other dogs.
Tears, cornea and eyelids
The tears, cornea and eyelids are a functional unit, a good analogy would be the windscreen of a car, which relies on wipers and washer water with additives to stay clear and functional. The wipers are equivalent to the eyelids and the windscreen the cornea. Tears have three main layers: aqueous, which is equivalent to the water in the washer fluid; and the lipid and mucin layers that equate to the washer fluid additive. There are multiple ways the eyelid, tear and cornea unit may be disturbed in brachycephalic dogs all contributing to the issues seen in BOS.
The brachycephalic breeds have orbits often so shallow the globe has barely any bony protection; short craniofacial ratios are a predisposing factor for corneal ulceration (Packer et al, 2015) (Figures 5 and 6).
The abnormal position of the globe relative to the skull means that the lids are in a position that prohibits efficient tear film distribution and leads to medial entropion (Figure 7). Two recent surveys of Pugs have reported incidences of medial entropion of 94.1% and 100% (Krecny et al, 2015; Maini et al, 2019).
Dogs with a smaller relative fissure width (palpebral fis-sure width/cranial length) have a reduced probability of cor-neal ulceration (Packer et al, 2015a). Increasing scleral exposure (related to both eyelid conformation and orbital depth) is a risk factor for corneal ulceration in brachycephalic dogs (Packer et al, 2015a) (Figure 8).
Dogs with nasal folds are nearly five times more likely to be affected by corneal ulcers than those without (Packer et al, 2015). In some breeds such as the Peking-ese the nasal fold is large and hairy, with hairs rubbing the corneas (Figure 9). In other breeds there may not be direct contact, but the presence of the fold can lead to ‘crowding’ of the medial canthal area, or may be an indicator of brachycephaly.
The tear film is a complex structure traditionally thought of as having aqueous, lipid and mucin layers with several roles in maintaining corneal health (Willcox et al, 2017). There is a complex interface with the cornea at the glycocalyx ‘holding’ the tear film in place, this interaction being dependent on both tear film quality and cornea ‘wettability’ (King-Smith et al, 2018).
Aqueous tear secretion is lower in brachycephalic dogs (Bolzanni et al, 2020) — this is a quantitative tear deficiency (in the analogy the car does not have enough water coming out of the washer reservoir). They also have poorer quality tear films, known as qualitative tear deficiency (Labelle et al, 2013; Palella Gómez et al, 2020) (in the analogy the car does not have enough additive in the washer reservoir for the fluid to clear the windscreen well). There is no one simple tool for tear film assessment (Bolzanni et al, 2020). Assessments are either quantitative or qualitative.
The Schirmer tear test (STT) is the most common quantitative tear film assessment (Featherstone and Heinrich, 2013; Bolzanni et al, 2020).
Tear film break-up time is the most common method of qualitative tear film assessment (Wolffsohn et al, 2017), this is usually performed using fluorescein (Guillon, 1998; Romkes et al, 2014; Wolffsohn et al, 2017; King-Smith et al, 2018). Fluorescein is applied to the eye, the lids blinked, then held open and the time taken for breaks in the tear film to be visible under blue light. Normal is quoted as over 20 seconds, with below 5 seconds as abnormal (Moore, 1990). Fluorescein is also useful in demonstrating corneal ulceration and checking for perforation with the Seidel test.
Brachycephalic dogs have poor corneal sensation, meaning they fail to respond to corneal exposure with eyelid movements or reflex tearing (Barrett et al, 1991; Bolzanni et al, 2020).
In addition to the above distichiasis and ectopic cilia are common findings (Krecny et al, 2015).
Ophthalmic examination in brachycephalic dogs
There are many challenges to handling small brachycephalic dogs for ocular examination, sampling, and topical drug application. Often, they are poorly trained, and their inquisitive personalities mean that they do not stay still for long periods. In addition, many suffer from brachycephalic obstructive airway syndrome (BOAS) (Packer et al, 2015b), often compounded by obesity. Stress caused by veterinary intervention can lead to a dyspnoeic crisis.
It should also be remembered that nasal airflow is poor and that closing of the mouth during restraint for eye examination could potentially lead to distress. Should there be any sign of respiratory distress during any restraint technique it should be abandoned. Tight restraint may also affect some of the measurements gained in an examination, for example tonometry measurements will increase if there is pressure on the jugular veins. In cases of deep corneal ulceration, if blood samples are required it may be safer to use the contra-lateral jugular vein to avoid potential globe rupture. Using a harness helps prevent neck pressure on exercising.
Care should be taken not to pull the facial skin backwards, for example by holding the scruff, as proptosis of the eye may easily occur. Pressure on the eyelids or the eye itself should be avoided as it is so unprotected by the orbit. and just small amounts of extra pressure may be enough to cause a deep, fragile corneal ulcer to rupture.
Splitting the eye examination into short sections can be useful, accepting that a full examination in one sitting is not always possible. Where possible, perform a full ophthalmic examination including examining the intraocular structures and the fundus and tonometry. Assessment of the eyelids for entropion, ectopic cilia and distichiasis, STT and careful examination of the cornea and tear film including with fluorescein with a blue light are of particular importance in the small brachycephalic breeds.
Often various methods of restraint must be tried until one that suits the individual is found. Examples of restraint include:
- Examination on a table with minimal restraint (Figure 10)
- Holding the patient off the examination table, under an assistant's arm with their forelimbs held (Figure 11) — it may be possible for them to have their hindlimbs on the examination table
- Over the shoulder examination, being held by an assistant with the forelimbs resting on a shoulder (Figure 12)
- Held like a baby, cupped in an assistant's arms on their back (Figure 13)
- Wrapped in a towel (Figure 14).
- Where appropriate light sedation — it might be safer to sedate than stress a dog on the verge of a respiratory crisis.
When applying eye drops, try to hold the dog's head upwards so you can simply drop the medication straight onto the eye. Rest your hand gently above the upper eyelid, pulling it open. Try to approach the dog from behind and place the dropper above exposed sclera to avoid the dog seeing the dropper approaching.
It is worth spending time with the owners working out the best way to restrain their dog as these cases usually require ongoing eye drops, for example lubricants.
Treatment options for brachycephalic ocular syndrome
Both medical and surgical treatment are often required, involving management of the causes as well as the problems. Regular re-examinations are needed because of the possibility of rapid deterioration, and nurses are vital in helping to ensure ongoing owner compliance.
Medical management
Any deficiency in the tear film should be addressed in all cases, even if there is no corneal ulceration present. Ongoing lubrication of brachycephalic corneas is advisable. Hyaluro-nate based products are an attractive tear supplement given its physical properties, retention times (Herring, 2013) and potential protective effects on the corneal epithelium (Mc-Donald, 2002). ‘Crosslinking’ of the hyaluronate molecules has been suggested as advantageous (Williams and Mann, 2013, 2014; Wirostko et al, 2014; Williams et al, 2017).
Ciclosporin is the licensed drug (Optimmune, MSD Animal Health) for aqueous deficiency acting via immune-modulatory and direct lacrimogenic effects (Giuliano, 2013; Herring, 2013). It also has positive effects on tear quality (Moore et al, 2001). It may be useful in limiting corneal pigmentation (Salisbury et al, 1990; Morgan and Abrams, 1991; Rankin, 2013). Tacrolimus may be of use in keratoconjunctivitis sicca cases with very low STTs, refractory to ciclosporin (Berdoulay et al, 2005).
In addition to tear supplementation, the medical treatment regimen for corneal ulcers depends on the cause and the severity. Topical antibiotics should be based on culture and cytology. Pseudomonas spp. for example may cause rapid corneal melting and if suspected, antibiotics with activity should be used, for example gentamicin or a flouroquinolone. Not every ulcer is infected and antibiotic usage in these cases is prophylactic rather than therapeutic. Cytology and culture should be performed ideally on all ulcers. Samples can be collected in a conscious patient following topical anaesthesia provided suitable restraint is possible and the ulcer is not so deep that sampling would risk rupturing the eye. Samples for cytology can be gently taken with the back of a scalpel blade, bacteriology swab, cytobrush or dental micro-applicators (Figure 15). Samples are air-dried following gentle transfer/ rolling onto a clean microscope slide. Examination can be performed in clinic, staining with a rapid Romanowky-type stain such as Diff-Quik.
Cytology of normal samples contains predominately epithelial cells; in bacterial keratitis neutrophils may predominate with bacteria often seen. Bacterial morphology may be helpful in antibiotic selection pending culture results. Samples should also be examined for fungal elements (Figure 16).
Anti-collagenases such as topical serum/plasma can be used to try and prevent corneal melting (Ollivier et al, 2007). The simplest way to prepare serum is to place blood into gel tubes — following routine spinning the serum supernatant can be poured into (ideally) sterilised eye dropper bottles (Figure 17). Alternatively, serum could be drawn up into 1 ml syringes and dispensed from these. Serum can be frozen prior to use (Conway et al, 2015). Serum should be refrigerated and used within 5 to 7 days to avoid contamination (Ollivier et al, 2007), a recent study has, however, suggested that plasma in a dropper bottle can be used for 2 weeks (Strauss et al, 2019). Serum from donor dogs or other species (for example horses) can be used and may be preferable in dogs that are difficult to restrain with fragile eyes.
Analgesia should be provided (for example systemic nonsteroidal anti-inflammatories). Cycloplegic drugs should be used as appropriate if there is reflex miosis — topical atro-pine can reduce tear production, cyclopentolate may be a preferable drug (Costa et al, 2016).
The eye can only hold so much topical drug at any one time, so to increase the drug ‘dosage’ the frequency of drops must be increased. When using multiple drugs, 5 to 10 minutes between eye drops is required to avoid one drug washing out the next.
In cases of corneal melting, intensive frequent application (for example hourly) of topical medications is indicated, often requiring hospitalisation of the patient (Figure 18).
Multiple medications can be difficult for owners to keep track of, and it can be helpful to provide colour coded medication sheets for use at home and when hospitalised.
Surgical management
The surgical options are lid surgery to address the causes and corneal surgeries to repair the effect of BOS. Lid surgery can be performed at the same time as corneal repair, if clinically appropriate.
Eyelid conformation is usually corrected with a medial canthoplasty (reducing the size of the palpebral fissure and correcting the lower medial entropion). Long-term owner satisfaction following medial canthoplasty is good (Yi et al, 2006). A Hotz-Celsus procedure to resolve the lower lid entropion may also be useful and the two procedures can be combined (Figures 19 and 20). Nasal fold excision can be performed if required.
Various corneal surgeries are available for the repair of corneal ulcers including: conjunctival grafts (Figure 21) (Dorbandt et al, 2015), corneo-conjunctival transpositions (CCTs) (Gogova et al, 2020), collagen (Dorbandt et al, 2015) or amnion grafts (Costa et al, 2019), and corneal transplants, both partial thickness (lamellar) and full thickness (penetrating) keratoplasties, can be used (Lacerda et al, 2017). Enucleation may have to be considered in some cases.
Surgical treatments for corneal pigmentation including corneal cryo-surgery (Azoulay, 2012), diamond burr debridement (Gradilone et al, 2012) and superficial keratectomy (Gilger et al, 2007) have been described; they should be used alongside correction of underlying causes for example, eyelid surgeries and tear film supplementation as appropriate.
Nursing of surgical brachycephalic ocular syndrome cases
It is important to be careful with anaesthesia, and to preoxygenate (Figure 22) and recover with close supervision, as brachycephalic patients are high risk cases. Be prepared for the worst situation that may happen.
Points to consider for successful anaesthesia and management of surgical cases include:
- Try and operate early in the day to facilitate supervision of their recovery
- Include questions that may indicate the dog suffers from BOAS on the consent forms, for example, asking about a history of collapse, respiratory noise or regurgitation
- Use pre-medication prior to anaesthesia to reduce stress
- Administer a prokinetic (metoclopramide) or an anti-acid (omeprazole) to try and reduce the effects of gastric reflux and regurgitation in the peri-operative period
- Have a wide selection of endotracheal tubes available and laryngoscopes with working lightbulbs
- Be ready to cope with respiratory distress on recovery. Recover in sternal recumbency, leaving the endotracheal tube in for as long as possible. Be prepared to re-intubate if required, and monitor oxygen saturation following extubation
- Consider avoiding non-steroidal anti-inflammatory analgesia until recovered to enable the use of an intravenous steroid should a respiratory crisis develop
- Use of ocular and other facial reflexes, such as jaw tone, are often not possible to monitor during ocular surgery; multi-parameter monitoring as well as more basic options, such as oesophageal stethoscopes, facilitate anaesthetic monitoring. When anaesthetic techniques, such as neuromuscular block to facilitate globe positioning, are being used, advanced monitoring is mandatory
- Lubricate eyes pre-, intra- and post-operatively. STT is affected by anaesthesia especially if over 2 hours long (Herring et al, 2000). Before surgery any hair clipping or trimming around the eye should be done very carefully, as poor technique may cause increased incidence of surgical wound infections. A sterile water-based lubricant, such as carbomer gel, should be used to trap hairs and protect the cornea and conjunctival sac. These can be flushed out before pre-surgical disinfection.
Pre-surgical disinfection should be with povidine solution, not a scrub or alcohol-based preparation, diluted 1:50 with saline (Roberts et al, 1986). Addition of povidine iodine to intravenous fluid bags is a convenient method of preparation — this stock solution should be changed daily. As well as cleaning the periocular skin the conjunctival sac and cornea should be well flushed, including under the third eyelid.
Postoperatively buster collars are a common-sense decision, however, if the collar is causing more problems than it is solving then its use may be inappropriate. Some collar designs are better tolerated than others.
Conclusion
The current continued breeding of brachycephalic dogs means BOS will carry on being a problem in practice. Veterinary professionals should have a thorough understanding of the disease processes and treatment options. Management can be a challenge, requiring gentle handling to avoid respiratory distress and further damage to fragile eyes. Surgery is not curative, ongoing medical management to supplement the tear film and maintain corneal clarity is often required. Veterinary professionals, especially veterinary nurses, need to be involved in providing ongoing support with long-term management, to help prevent the loss of vision or the eyes themselves.
KEY POINTS
- The term brachycephalic ocular syndrome (BOS) describes the eye problems associated with the conformation of the small brachycephalic breeds.
- Corneal ulceration and pigmentation and proptosis of the globe are common presentations of BOS.
- As well as problems resulting from their anatomy, the small brachycephalic breeds are prone to deficiencies in both the quantity and quality of their tears.
- Examination of BOS cases needs to be gentle, to avoid respiratory distress as well as further damage to often fragile eyes. Trying different methods of restraint and rest periods may be required.
- Medical management of cases includes addressing tear deficiencies with both lubricants and lacrimostimulants, appropriate antibiotic use guided by culture and cytology, anti-collagenases such as topical serum and appropriate analgesia. Aggressive treatment with frequent application of multiple eyedrops may be required in cases with corneal melting.
- Surgical treatment to repair corneal defects and improve eyelid anatomy may be required.
- Cases often carry a high anaesthetic risk, and precautions should be taken to manage this.
- Care must be taken to lubricate the eyes of the small brachycephalic breeds before, during and after anaesthesia.
- Ongoing management and support of BOS cases is often required.