Genetic Welfare Problems of Companion Animals

Shih Tzu

Brachycephalic Airway Obstruction Syndrome (BAOS)

Related terms: Brachycephalic Onstructive Airway Syndrome (BOAS), Brachycephalic Airway Syndrome (BAS), Brachycephalic Airway Disease (BAD), Brachycephalic disease

Outline: The short-nosed shape of the Shih tzu causes breathing difficulties and ‘knock-on’ effects which cause chronic discomfort and prevent it exercising normally.

Summary of Information

(for more information click on the links below)

1. Brief description

Brachycephalic Airway Obstruction Syndrome (BAOS) occurs in all dog breeds with brachycephaly. Brachycephaly is characterised by greatly shortened upper jaws and noses, but the soft tissues of the nose and throat remain unchanged, thus these tissues are squeezed into a substantially smaller space. This leads to narrowing and increased resistance in the respiratory system. BAOS describes the clinical problems caused by this. The main congenital abnormalities (those present from birth) seen are stenotic nares (abnormally narrowed nostrils), excessively long soft palate in relation to head shape and tracheal hypoplasia (abnormally narrowed windpipe). The permanent narrowing and obstruction of the airways makes breathing harder. The constantly increased respiratory effort leads to secondary changes which further narrow the air passages, including collapse of the larynx (the voice box, the opening to the windpipe). BAOS leads to snoring, respiratory noise, mouth breathing, respiratory distress with rapid breathing and struggling for breath, and can lead to collapse and death. Dogs with BAOS are unable to take even moderate amounts of exercise, are very prone to heat stroke and have constantly disrupted sleep.

2. Intensity of welfare impact  

This is a major welfare problem with bouts of severe respiratory distress. Even mildly affected dogs are likely to suffer disrupted sleep and are prevented from carrying out normal canine behaviours such as running and exercising due to compromised breathing.

3. Duration of welfare impact

BAOS is a progressive, life-long condition. It can affect immature dogs under 6 months of age.

4. Number of animals affected

We are not aware of published data on the proportion of Shih tzus that are affected by BAOS but since the condition is directly connected to brachycephaly, which is part of the breed standard, many Shih tzus are likely to have this condition to some degree.

5. Diagnosis

BAOS may be suspected in any Shih tzu showing the typical signs, as it is a common problem. However, specific diagnosis of most of the abnormalities, that together form the syndrome, requires examination under anaesthetic, plus radiographs (x-rays) and possibly endoscopy (examination of the airways with a fibre optic tube). These procedures have to be performed under anaesthesia. This creates a dilemma as dogs with BAOS have a substantially increased risk of dying under anaesthesia because of their compromised respiration.

6. Genetics

BAOS is caused by brachycephaly. This inherited defect is a consequence of selection for the abnormal head shape of these breeds.

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

Many Shih tzus are affected with BAOS to a greater or lesser extent. Examination of any puppy prior to purchase is essential, along with its dam and sire. To avoid the risk of perpetuating the welfare problems associated with this condition, dogs showing any signs of BAOS, or whose parents have any signs or have had surgical procedures to alleviate the condition should not be purchased.

8. Methods and prospects for elimination of the problem

As BAOS is completely linked to the brachycephalic head shape, it seems unlikely that it will be possible to eliminate the condition without changing this conformation (and the breed standard). As many Shih tzus have this condition, to a greater or lesser extent, this would mean out-crossing to non-brachycephalic breeds. Opinions differ as to whether it is ethically acceptable to breed animals whose welfare is likely to be compromised.

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

1. Clinical and pathological effects

The term “brachycephaly” comes from the Greek words meaning short and head. The term is applied to all breeds of dog (and cat) with this abnormality. Some brachycephalic breeds include Pugs, English bulldogs Pekingese, French bulldogs, Lhasa apsos, Shih tzus, Boston terriers and, in cats, Persians.

The brachycephalic head shape is due to an inherited defect in the development of the bones of the skull (Stockard 1941). The head is of a normal width but the length is markedly reduced. However, the soft tissues of the head are not similarly reduced in size and have to be squeezed into a smaller shortened space. This affects the passage of air into the lower airways and lungs (Harvey 1989).

Brachycephalic Airway Obstruction Syndrome (BAOS) is a result of breeding practices that have selected for a shortened facial appearance. Most brachycephalic dogs are affected by upper airway obstruction to some degree (Brown & Gregory 2005). The airways are narrowed in several places due to the shortened facial features and the resultant increased airflow resistance, so affected dogs have to use excessive effort to breathe (Shell 2008). BAOS is the term given to this collection of anatomical effects, the secondary anatomical changes they cause and the clinical signs that result.

There are a number of congenital (present from birth) anatomical abnormalities that form the basis of BAOS and which contribute to the breathing problems:

• Stenotic Nares (abnormally narrow nostrils) – This is usually a bilateral condition (it affects both nostrils), and when present, adds to the airway occlusion, increasing the effort needed for inspiration – for breathing in. This extra effort leads to a further problem as it pulls the soft palate deeper into the larynx (the opening to the airway) and blocks the airway opening further (Shell 2008). Distorted nasal passages are also thought to cause some occlusion of the larynx (Hendricks 1995)
• Elongated soft palate – It is believed that the genetic defect responsible for shortening the nose does not affect the soft tissues, the consequence of which is that the soft palate at the back of the mouth and the tongue are excessively large relative to the size of the head (Venker-van Haagen 1995). In fact, in a dog of the same size with a normal head shape, the soft palate would be the correct length, but in the brachycephalic dog, the overlong soft palate gets pushed backwards, partly obstructing the larynx (the opening to the airway) (Hendricks 1995). The elongated soft palate also increases airflow turbulence and rubs against other tissues, such as the larynx, leading to inflammation and swelling of airway tissues (Torrez & Hunt 2006). As a consequence of this inflammation, the soft palate itself becomes swollen and thickened over time, further blocking the airways (Shell 2008).
• Trachea hypoplasia. Tracheal hypoplasia is abnormal narrowness of the windpipe relative to the size of dog and it is often seen in conjunction with the above abnormalities. (It can also occur with other abnormalities not considered to be part of BAOS including megaoesophagus (abnormally enlarged oesophagus) (Coyne and Fingland 1992)). Opinions vary about the extent to which tracheal hypoplasia plays a part in BAOS. It has been suggested that tracheal hypoplasia makes the prognosis worse (Orsher 1993, Monnet 2003) and predisposes affected animals to chronic or recurrent lower airway and lung infections (Harvey 1989).
• Laryngeal hypoplasia  In this condition, the larynx is small and underdeveloped. The cartilages that form the larynx are soft and not fully developedand the abductor muscles that open the larynx do not function properly (Venker-van Haagen 1995). This is a common cause of laryngeal collapse in brachycephalic breeds according to Venker-van Haagen (1995), although other authors do not to discuss this condition as part of BAOS. Burbidge et al (1988) recorded a case of BAOS with laryngeal malformation and suggested that this may be seen in other cases of BAOS.

Affected dogs usually have some combination of the above defects (Brown & Gregory 2005) and most have more than one defect (Fasanella et al 2010). These anatomical defects increase the workload of the respiratory system leading, over time, to a progression of secondary problems. These include:

• Collapse of the larynx - The increased negative pressure created in the pharyngo-laryngeal (throat) region, as a result of the obstructions described above, ultimately results in distortion and collapse of the larynx (Wykes 1991). Three stages of laryngeal collapse have been described:
  
  In stage I the laryngeal saccules (small sac-like structures in the larynx) balloon and turn inside out (evert). This adds to the airway obstruction.
  
  In stage II there is loss of rigidity and medial displacement of the cuneiform processes of the arytenoid cartilage (part of the cartilage that form the support structure of the larynx) which collapse inwards,
  
  and in stage III there is collapse of the corniculate processes of the arytenoid cartilages - this involves further collapse of the laryngeal structures blocking the airway (Pink et al 2006).
• Bronchial collapse. Laryngeal collapse has been found to be significantly associated with bronchial collapse (collapse of the branching airways in the lungs) (De Lorenzi et al 2009).
• Eversion and hypertrophy of the tonsils – Inflammation of the soft tissues in the throat area leads to the tonsils enlarging, adding to the amount of tissue protruding into the pharynx (the back of the throat) (Fasanella et al 2010).
• Hypertrophy of the pharyngeal muscles – The muscles in the throat become larger and thicker as they are constantly having to work harder to keep the pharynx open to enable the passage of air into the lungs. However, this hypertrophy of the muscles further narrows the pharyngeal cavity.
• Gastrointestinal problems: dysphagia, regurgitation, vomiting and acid reflux – Dysphagia is defined by Poncet et al (2005) as difficult or painful swallowing. They state that it can be associated with regurgitation (bringing up contents of the oesophagus – often saliva in BAOS) and vomiting (bringing up stomach contents). Dysphagia in brachycephalic dogs has been reported by many authors (eg Ducarouge 2002, Dupre and Freiche 2002, Koch and others 2003). Poncet et al (2005) also noted many reports of anatomical defects in the gastrointestinal tract of brachycephalic dogs. For example, hiatus hernias (in which part of the stomach can pass up into the chest through a larger than normal hole in the diaphragm, and pyloric stenosis (in which the stomach exit is narrowed, preventing normal exit of the food from the stomach). They found a correlation between the severity of BAOS and of the gastrointestinal disease and postulated that the severity of respiratory signs affected the severity of gastrointestinal signs and vice versa.
• Heart Failure – This occurs secondarily to inadequate oxygenation of the blood in the lungs, due to the airway obstructions. The body detects that the blood is inadequately oxygenated and narrows (vasoconstricts) the capillaries in parts of the lung that are poorly ventilated. Chronic (long term) vasoconstriction and increased blood pressure in the lungs increases the blood pressure in the right side of the heart and eventually can lead to right-sided heart failure (Monnet 2008).
• Breathing problems affect some brachycephalic bitches during whelping (giving birth) (Harvey 1989) and, for this reason, caesarean sections are sometimes performed in these dogs.

These secondary BAOS changes are progressive, so the signs seen at any one time depend on how many congenital anatomical defects are present, the severity of each and how long the secondary conditions have been progressing. The primary congenital abnormalities cause the signs seen in puppyhood. The mean age at which brachycephalic dogs are presented to vets for treatment of BAOS is 3 to 4 years of age (Monnet 2008). Laryngeal collapse is usually associated with older animals (Harvey 1982a).

Clinical signs in the mildest cases consist of snoring and respiratory noise on inspiration (breathing in), also called stridor (Brown and Gregory 2005, Fasanella et al 2010). Signs in more severe cases include exercise intolerance (inability to cope with exercise), mouth breathing, gagging, restlessness, rapid breathing, cyanosis (blue coloured membranes of the mouth – due to lack of oxygen in the blood), dysphagia, abnormal posture, and intermittent collapse due to respiratory compromise (Shell 2008, Fasanella et al 2010). Vomiting and regurgitation are also frequently seen. (Dupre 2008). Flatulence is common due to aerophagia (swallowing air) (Harvey 1989).

Respiratory crises commonly occur in moderate to severely affected individuals, in which the animals rapidly develop respiratory distress – struggling to breathe - and can collapse and die. Severely affected individuals with laboured breathing, stand with their elbows held away from their chest in an attempt to ease it (Brown & Gregory 2005). With laboured breathing, over inflation of the chest is seen (Dupre 2008).

Dogs with more severe BAOS live a precarious existence and minor aggravations can lead to severe respiratory distress and a crisis (Hendricks 1995). Stress, exercise, excitement, all act as aggravators (Hendricks 1995, Dupre 2008). These dogs are very prone to heat stroke (Hendricks 1995).

Hendricks (1995) examined sleep disorders in 20 English bulldogs. All dogs over 2 weeks of age exhibited sleep-disordered breathing including pauses in breathing and blood oxygen levels dropping below normal many times per hour. It is likely that this also occurs in Shih tzus.

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2. Intensity of welfare impact

BAOS has a major welfare impact. Dogs affected by BAOS suffer great distress (which may include apprehension or fear) when struggling to breath, and these crises can be induced by minor occurrences such as “a simple walk in humid weather” (Hendricks 1995). Without major surgical treatment these crises can reoccur and can be life-threatening. Disrupted sleep patterns because of brachycephalic respiratory compromise are probably common. Even those with mild to moderate BAOS are unable to exhibit, what for non-brachycephalic breeds of dogs, is considered normal behaviour such as running and resting comfortably.

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3. Duration of welfare impact

This is a life-long disorder, starting in puppies, progressing throughout life and ultimately often shortening life (Dupre 2008), with the average age of presentation to vets for treatment, for all brachycephalic breeds, being 3-4 years of age (Monnet 2008). Even with surgical treatment life-expectancy can be compromised with some authors recording death or euthanasia due to BAOS in a relatively high percentage of cases.

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4. Number of animals affected

Brown and Gregory (2005) suggest most brachycephalic dogs are affected by upper airway obstruction to some degree. The degree of problem depends on the number and severity of the anatomical abnormalities that are present in any individual dog.

Stenotic nares have been reported to occur in 46 to 50% of dogs with BAOS (Lorinson et al 1997, Harvey 1982a, Fasanella et al 2010).

Elongated soft palate: 96 to 100% of brachycephalic dogs have an overlong soft palate relative to their head size (Harvey 1982b, Dupre 2008, Fasanella et al 2010).

Everted tonsils were seen in 56% of brachycephalic dogs with BAOS (Fasanella et al 2010).

Nasopharyngeal turbinates are found in some brachycephalics, but not commonly in Shih tzus (Ginn et al 2008).

Laryngeal collapse is common in Shih tzus with BAOS. Surgical correction of laryngeal collapse in Shih tzus is more challenging than in larger dogs (Harvey 1982d). Fasanella et al (2010) found that 66% of brachycephalic dogs with BAOS syndrome had everted laryngeal saccules.

Tracheal hypoplasia is common and often severe in some brachycephalic breeds such as English bulldogs and Boston terriers but not in the Shih tzu (Coyne & Fingland 1992). Secondary problems are also common. The reported occurrence of laryngeal problems varies from 30% to 64% (Harvey 1982c, Harvey 1982d, Dupre 2008). In one study of 73 cases of BAOS, on presentation, 97% had oesophageal, gastric or duodenal anomalies and 74% had gastrointestinal problems classed as moderate or severe (Poncet et al 2005).

So it seems likely that most Shih tzus have BAOS to some extent, though some people may consider this “normal”.

Harvey (1989) reported that “The breathing problems caused by these abnormalities [BAOS] are so commonly recognised by breeders of bulldogs and other short-faced breeds that some carry oxygen cylinders with them to shows, and routinely arrange for caesarean section birth of puppies so as not to cause asphyxiation of the whelping bitch.

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5. Diagnosis

The syndrome may be suspected in any brachycephalic dog showing the characteristic signs, because it is so common. Diagnosis of stenotic nares can be made on clinical examination, and definitive diagnoses of elongated soft palate, tonsillar hypertrophy and laryngeal collapse can be made on examination under anaesthetic. Diagnoses of tracheal hypoplasia, right sided heart failure and confirmation of elongated palate are made with radiography (x-rays) under anaesthesia and gastrointestinal complications are investigated and confirmed via endoscopy and biopsies, again under anaesthetic (Monnet 2008). Anaesthesia presents substantially greater risks to BAOS sufferers and most authors only recommend anaesthesia for diagnosis when corrective surgical treatment can also be carried out at the same time, under the same anaesthetic, so that these risks during recovery are reduced.

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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 and 2 particular genes have been implicated. The exact gene or genetic defects are currently unknown (Bannasch et al 2010). This inherited defect defines all brachycephalic breeds and without this defect these breeds would no longer exist in their current form. It is because of this defect that Shih tzus are predisposed to BAOS (Hendricks 1995, Dupre 2008, Monnet 2008, Shell 2008).

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

As the Shih tzu is partly defined by its brachycephalic head shape – all Shih tzus are affected by the inherited defect which causes brachycephaly. Most brachycephalic animals have some degree of BAOS (Brown & Gregory 2005), so it is difficult to identify a puppy that will be free of this condition. Anyone wishing to obtain a Shih tzu should ensure that it and its sire and dam are free of signs of BAOS and that they have not had corrective surgery for any of the primary or secondary conditions.

At present, identifying individuals that have had surgery for these conditions is difficult because scars on the nostrils may not be easy to see and the other surgical scars are hidden inside the throat. Because of this, Harvey (1989) supported a policy of simultaneously neutering all animals that had corrective surgery. The extent to which others have pursued this policy is not known but it has certainly not been universal. Puppies with signs of BAOS should not be purchased. If signs appear after purchase, the puppy should be returned to its breeder.

Dogs which have shown any signs of BAOS or which have had corrective surgery for BAOS should not be used for breeding.

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8. Methods and prospects for elimination of the problem

Clear identification and neutering of all dogs which have had surgical interventions seems vital. However, it is the brachycephalic head shape that is the primary anatomical abnormality that causes BAOS. The practices of Caesarean section and artificial insemination that enable some severely brachycephalic dogs to reproduce have facilitated selection for extreme forms of this defect (Bannasch et al 2010).

If Shih tzus with signs of BAOS were excluded from breeding, the remaining gene pool of animals of this breed might be too small to be sustainable (because BAOS is so prevalent) so out-crossing with non-brachycephalic breeds may be the best approach to tackling this problem. 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.

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10. References

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

Brown D and Gregory S (2005) Brachycephalic Airway Disease. In Brockman D & Holt D Eds BSAVA Manual of Canine and Feline Head, Neck and Thoracic Surgery. pp 84. BSAVA: Cheltenham

Burbidge HM, Goulden BE and Dickson LR (1988) Surgical relief of severe laryngeal malformation in an English Bulldog. New Zealand Veterinary Journal 36: 29-31

Coyne B and Fingland R (1992) Hypoplasia of the tracheal in dogs: 103 cases (1974–1990). Journal of the American Veterinary Medical Association 201: 768–772

Ducarouge B (2002) Le syndrome obstructif des voies respiratoires supérieures chez les chiens brachycéphales. Etudes clinique à propos de 27 cas. Doctoral thesis, Lyon

De Lorenzi D, Bertoncello D and Drigo M (2009) Bronchial abnormalities found in a consecutive series of 40 brachycephalic dogs. Journal of American Veterinary Medical Association 235: 835-40

Dupre G (2008) Brachycephalic Syndrome: New Knowledge, New Treatments. Presentation at WSAVA Congress, Dublin, Ireland, 20-24th August 2008 (On-line). Available at http://www.vin.com/proceedings/Proceedings.plx?CID=WSAVA2010&Category=&PID=56236&O=Generic. Accessed 20.7.10

Dupre G and Freiche V (2002) Ronflements et vomissements chez les bouledogues: traitement médical ou chirurgical? Proceedings of the AFVAC Annual Congress. Paris, France, November 10, 2002. pp 235-236

Fasanella FJ, ShivleyJM, Wardlaw JL and Givaruangsawat S (2010) Brachycephalic airway obstructive syndrome in dogs: 90 cases (1991–2008). Journal of the American Veterinary Medical Association 237: 1048-1051

Ginn JA, Kumar MSA, McKiernan BC and Powers BE (2008) Nasopharyngeal Turbinates in Brachycephalic Dogs and Cats. Journal of the American Animal Hospital Association 44: 243-249

Harvey C (1982a) Upper airway obstruction surgery 1: Stenotic nares surgery in brachycephalic dogs. Journal of American Hospital Association 18: 535-537

Harvey C (1982b) Upper airway obstruction surgery 2: Soft palate resection in brachycephalic dogs. Journal of the American Animal Hospital Association 18: 538-544

Harvey C (1982c) Upper airway obstruction surgery 3: Everted laryngeal saccule surgery in brachycephalic dogs. Journal of the American Animal Hospital Association 18: 545-547

Harvey C (1982d) Upper airway obstruction surgery 4: Partial laryngectomy in brachycephalic dogs. Journal of the American Animal Hospital Association 18: 548-550

Harvey C (1989) Inherited and congenital airway conditions. Journal of Small Animal Practice 30: 184-187

Hendricks J (1995) Recognition and treatment of congenital respiratory tract defects in brachycephalics. In Bonagura, J. (Ed) Kirk’s Current Veterinary Therapy XII small animal practice. Philadelphia: WB Saunders

Koch D, Arnold S, Hubler M and Montavon P (2003) Brachycephalic syndrome in dogs. Compendium on Continuing Education for the Practicing Veterinarian 25: 48-55

Lorinson D, Bright R and White R (1997) Brachycephalic airway obstruction syndrome a review of 118 cases. Canine Practice 22: 18-21

Monnet E (2003) Brachycephalic airway syndrome. In Slatter D (Eds) Textbook of Small Animal Surgery. Philadelphia: WB Saunders

Monnet E (2008) Brachycephalic airway syndrome (CVC Proceedings). (On-line). Available athttp://veterinarycalendar.dvm360.com/avhc/Medicine/Brachycephalic-airway-syndrome-Proceedings/ArticleStandard/Article/detail/587147. Accessed 19th July 2010

Orsher RJ (1993) Brachycephalic airway disease. In Bojrab, M. (Ed) Disease Mechanisms in Small Animal Surgery. Philadelphia: Lea and Febiger

Pink J, Doyle R, Hughes J, Tobin E and Bellenger C (2006) Laryngeal collapse in seven brachycephalic puppies. Journal of Small Animal Practice 47: 131–135

Poncet C, Dupre G, Freiche G, Estrada M, Poubannet Y and Bouvy B (2005) Prevalence of gastrointestinal tract lesions in 73 brachycephalic dogs with upper respiratory syndrome. Journal of Small Animal Practice 46: 273–279

Reicks TW, Birchard SJ and Stephens JA (2007) Surgical correction of brachycephalic syndrome in dogs: 62 cases (1991–2004). Journal of the American Veterinary Medical Association 230: 1324-8

Shell L (2008) Brachycephalic Airway Syndrome. (On-line). Available at http://www.vin.com/Members/Associate/Associate.plx?DiseaseId=564. Accessed 16.7.10

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

Torrez C and Hunt G (2006) Results of surgical correction of abnormalities associated with brachycephalic airway obstruction syndrome in dogs in Australia. Journal of Small Animal Practice 47: 150–154

Venker-van Haagen A (1995) Diseases of the throat. In Ettinger S and Feldman E (Eds) Textbook of Veterinary Internal Medicine. Philadelphia: WB Saunders

Wykes P (1991) Brachycephalic airway obstructive syndrome. Problems in Veterinary Medicine 3(2): 188-97

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