Brachycephalic Obstructive Airway Syndrome (BOAS)

Background: BOAS is short for the term “brachycephalic obstructive airway syndrome”. The term means that the syndrome applies to brachycephalic dogs and that it is manifested by the fact that there is an obstruction, i.e. a constriction, in the airways, which causes the airflow to be obstructed. A “syndrome” is “a condition in which there are deviations and injuries in several of the body’s organs and which have a common cause” (Definition from Karolinska University hospital, my translation from Swedish).

On the web page of Universities Federation for Animal Welfare it says that most likely, all Pugs have BOAS to some degree, simply because of their brachycephalic shape of the head (ufaw 2016). This is confirmed by Dr. Ronja Mock, specialist in throat, nose and ears at the Klinik für Kleintiere at the University of Leipzig, who says that all Pugs to some degree have aberrations in their airways that is due to BOAS (Mock, private communication).

Thus, a dog diagnosed with BOAS has some form of obstruction of the air flow in the airways, and depending on the degree of BOAS, there is a corresponding degree of respiratory distress. Professor Oechtering writes that there has been an excessive selection to produce snub nosed dogs with ever shorter noses in recent decades, which has led to that the “function has been drastically inhibited”, i.e. the syndrome has worsened, and it also occurs at an earlier age (Oechtering 2010: 2).

In the past, three obstructions of the upper respiratory tract were seen in snub nosed dogs: stenotic (cramped) nostrils, an extended soft palate, and everted laryngeal saccules in the upper airways. More recently, a stenosis (narrowing) has also arisen in an inner, invisible part of the nostril. Another obstruction in the upper respiratory tract which is much more common today is that the concha, the folded mucous membrane that causes cooling, has been softened and can penetrate forward due to lack of space and clog the air canal in the nasal cavity. It can penetrate backwards as well and clog the way down to the throat. It has been found that the mucous membranes have thickened in Pugs and that in a Pug of 10 kg they can be twice as thick as in a German Shepherd of 40 kg. Regarding the soft palate, it is not only prolonged, but in many cases it has thickened considerably as well (Oechtering 2010: 3f.).

The larynx can also be affected by BOAS. In Pugs, it can collapse because the cartilage in the larynx lacks stability and resilience. The same problem can be found in the trachea of Pugs. The air tube body consists of cartilage, which can have a lack in stability and therefore collapse. The slackness can also continue in the bronchi, which can collapse as well. (Oechtering 2010: 5f.).

BOAS is a progressive disease, i.e. it gets worse over time. This means that a young dog with BOAS has milder symptoms than it will probably have with increasing age (Bartels et al. 2015: 332). Packer et al. write that dogs that have serious BOAS exhibit little or no activity because they are fully occupied with getting enough oxygen (2015: 3). Stress, arousal, or exercise can cause these dogs severe respiratory distress and even death. BOAS thus to varying degrees, leads to difficulties in activity. Since the folded mucosa that cools the dog does not have enough room in the Pug’s nose, the Pug may not cool off its body like an ordinary dog, and thus it runs the risk of overheating during hot weather and during activity. Another symptom of BOAS is snoring and grunts. The limitations of the respiratory tract can also cause sleep disturbance. Furthermore, the incorrect pressure in the thorax not only leads to BOAS but also to damage in the gastrointestinal tract which is expressed, e.g. through regurgitation and vomiting (Packer et al. 2015: 2-3; Liu et al 2017: 2).

Nappe, left, was a big snorer, had difficulties to de-heat in Summer, and sounded terrible when panting heavily. He breathed good through the nose, so cold weather was better for him.

In general, it can be said that the less brachycephalic, the better the conditions for good breathing. One aspect that recurs among the researchers is that the nose needs to be longer (Oechtering 2010: 9; Bartels et al. 2015: 332; Packer et al. 2015: 1, 8f.). Packer et al. concluded that the risk of BOAS increases sharply in pace with shorter noses in the dog. In their study, only dogs that had a nose length shorter than half the length of the skull were affected by BOAS. (Packer et al. call the relationship between nose length and skull length craniofacial ratio, CFR.) The Pugs that had the shortest nose, with a nose length that was 3% of the skull’s measure from the stop to the occipital protuberance (CFR = 0.03), had a 95% risk of being affected by BOAS . In dogs where the nose length was 21% of the length of the skull (CFR = 0.21) the risk of BOAS was 48% (Packer et al. 2015: 1, 9, 16). Below is an image that shows how the CFR is measured:

Liu et al. also found a covariation between stenotic (narrow) nostrils and BOAS, where 65.3% of the Pugs had stenotic nostrils and 64.6% of them had clinically relevant BOAS (which they call BOAS (+)). The Pugs that had moderate or severe stenotic nostrils had 4.58 times increased risk of BOAS (+) (2017: 6). The researchers advocate that the assessment of the degree of stenosis of the nostrils is something that can be used in the breeding selection, but together with the assessment of the breathing in an exercise test (Liu et al. 2017: 11). In a previous study, they had produced an illustrated scale for assessing stenosis of the respective breed where open and mildly stenotic nostrils were considered non-clinically relevant, whereas moderately and severely stenotic nostrils had a clear connection to clinically relevant BOAS. Here is Liu et al:s illustrated scale:

A large neck girth and a short and wide skull have shown correlation with BOAS as well. In addition, Liu et al. found that the sex affected BOAS since the Pug bitches in their study had 5.35 times higher risk for clinically relevant BOAS (Liu et al. 2017: 5).

As we saw above, Oechtering assesses the degree of BOAS by determining the different stenoses in the airways. The assessment is made by him/the veterinarian at his clinic through the entering of the airways with an endoscope to see what it looks like. The endoscopy examination is supplemented with a CT scan of the dog’s airways. It is an extensive and expensive procedure to do such an examination and it is usually only done on dogs that show so many problems that they may need surgery.

Various researchers have tried to develop other, simpler methods of measurement, and in general, exercise tests and identification of external characteristics that co-vary with BOAS are used. The research group in Cambridge (to which Liu et al. belong) has developed a so-called “whole-body barometric plethysmography (WBBP)”, with which they measure the degree of BOAS. WBBP is a box where you can change the air pressure to see how well the dog’s airways work (Cambridge BOAS group WBBP). It fulfills the same function as an exercise test. The dog is neither sedated nor anesthetized, and thus the method is gentle for the dog.

According to the Cambridge scientist Jane Ladlow, a dog that shows BOAS at an exercise test and one that does not show BOAS at the same test can look about the same on the CT scan images. She points out that a CT is a static analysis method while BOAS is a dynamic disease. Because of this, the Cambridge researchers assess BOAS through the WBBP/an exercise test. However, they also do a CT scan of the brachycephalic dogs that turn out to have BOAS during the exercise test, to identify where in the airways the problems are located (Ladlow, private communication).

The researchers in Cambridge have also developed an exercise test where the dog runs 6–7 km per hour for three minutes. Immediately after the exercise, respiratory patterns, respiratory sounds, etc. are examined. The test is designed to allow veterinarians who do not have access to the WBBP to perform an exercise test, and the form used is accompanied by instructions to the performing veterinarian. You can look at the test form here: Cambridge Pug grading system 2018. This test is among others used by the Tierklinik Hofheim in Germany, for examination of Pugs regarding BOAS. Also several kennel clubs under FCI have begun to use the test.

It is important to note that exercise tests, such as with the plethysmography or by walking or running, provide information about BOAS in terms of function. A dog that has good function can still have aberrations in the airways that are due to BOAS. As mentioned earlier, it is likely that more or less all Pugs have BOAS, and that applies to the findings found with endoscope and/or CT scan, while exercise tests can more often “clear” a Pug from BOAS.

Goal: No Pug shall have more than mild BOAS (BOAS I) at an exercise test designed by specialists and tested by certified testers. (See the degrees of BOAS in the table below.)

Strategy: Since extremely brachycephalic traits are a major risk factor for BOAS, the Pug should be bred towards a less brachycephalic type. As we saw above, Packer et al. write that BOAS only occurs in dogs with a CFR below 0.5. We do not believe that it is realistic, or even feasible, to breed Pugs that have a CFR above 0.5. We estimate that there are no Retro Pugs with a CFR above 0,35. With a CFR above that, the dog has much more genes from the donor breed than Retro Pugs do and probably belong to the F1 Generation (50% Pug and 50% donor breed) as the dog below who is a F1 Pug x Parson Russell mix and whose CFR is 0,58. (The little black animal beside her is a baby rabbit. She helped her mom to take care of the rabbits.)

Photo: Nina Tissen
Mopszucht von den Herzenshunden

In Packer et al:s study BOAS was reduced to slightly less than 50% when the CFR was 0.21. We suggest that as a first step, at the choice of breeding partner, the average measure of the CFR of both dogs should be 0.2–0.25. Thus, if one of the parties has a short nose this should be compensated through the choice of a partner with a much longer nose. We should assess the nose length of the progeny successively and strive for a CFR that is about 0.3.

The Standard Pug genes are coded for a very short muzzle, but we see from the breeding of the Old German Pug and Retro Pug breeders that it is possible to lengthen the Pug’s nose. There are likely to be several, possibly many, genes involved in the shortening of the muzzle and careful selection, including the addition of a donor breed, makes it possible to gradually and safely lengthen the Pug’s skull and muzzle.

We also need to consider the stenosis of the nostrils and preferably let the Pugs with open and mildly stenotic nostrils be used in breeding. A Pug with moderate stenosis should only bred with if it does not have clinically relevant BOAS. Also, the shape of the skull is important, and there we need to aim for a skull that is more long than wide. If Liu et al:s observation is correct, that bitches run a much higher risk of developing BOAS, it is important to strive even more away from the brachycephalic form in the bitches.

We recommend that all Pugs that are to be bred with should be assessed through an exercise test. We do not see a CT scan and/or endoscopy of the airways as necessary since they do not say anything about the function. As mentioned above, Cambridge researcher Ladlow says that a dog that does not have BOAS and one that does have it, can look more or less the same on a CT scan. CT scan and endoscopy are often necessary methods to assess the treatment of a Pug that has BOAS, but not to assess whether a dog should be used in breeding or not. On the other hand, it can be interesting for the breeding to follow the generations of Pugs in terms of airways via CT scan, to see improvement through breeding.

In our opinion, Pugs that are used in breeding may have at most BOAS I according to the table below. It is often possible to judge at the age of one year how the airways will look like in the adult Pug; at that age, the symptoms of BOAS are usually present which may become more severe due to air resistance. To have a margin, BOAS should earliest be measured at 15 months of age.

Adapted from the grades given by Cambridge BOAS Research group
(http://www.vet.cam.ac.uk/boas/about-boas/recognition-diag nosis)

Through a strategy that takes into account all parts of what has been mentioned above; CFR, nostrils, BOAS exercise test, skull shape and donor breed, we believe that we have great conditions for breeding healthy, sound Pugs with free airways.

Leni vom Minzenbach has widely open nares
and breathes completely freely
Photo: Gitte Babbel

Sources and further reading:

Bartels, A. et al. 2015. ”Brachycephalic problems of pugs relevant to animal welfare”. Animal Welfare 24, 327–333.

Cambridge BOAS Research group. www.vet.cam.ac.uk/boas

Liu, Nai-Chieh et al. 2017. ”Conformational risk factors of brachycephalic obstructive airway syndrome (BOAS) in pugs, French bulldogs, and bulldogs”. PLoS ONE 12, e0181928. doi: 10.1371/journal.pone.0181928.

Oechtering, Gerhard. 2010. “Brachycephalic syndrome – new information on an old congenital disease”. Veterinary Focus 20, 2–9.

Oechtering. Gerhard. 2016. Professor Oechterings lecture about BOAS at the Swedish Kennel Clubs conference in 2016 about brachycephalic dogs.

Packer, Rowena M. A. et al. 2015. “Impact of Facial Conformation on Canine Health: Brachycephalic Obstructive Airway Syndrome”. PLoS ONE 10, e0137496. doi:10.1371/journal.pone.0137496.

ufaw.org.uk. 2015. “Research shows high risk of breathing problems in dogs with short muzzles” http://www.ufaw.org.uk/ufaw-news/news/post/168-research-shows-high-risk-of-breathing-problems-in-dogs-with-short-muzzles

ufaw.org.uk. 2016. “Brachycephalic Airway Obstruction Syndrome (BAOS)” www.ufaw.org.uk/dogs/pug-brachycephalic-airway-obstruction-syndrome

Chapters in Strategies for the breeding of Healthy Pugs