Small Animal ENT and Sleep Medicine Lab-Brachycephalic obstructive airway syndrome in dogs

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Brachycephalic obstructive airway syndrome in dogs

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Brachycephalic obstructive airway syndrom (BOAS) refers to a particular set of upper airway tract abnormalities that affects brachycephalic canine breeds such as the pug, the French bulldog, and the bulldog. For centuries, the domestic dog has been selected via breeding to meet the desired traits of human whims. Particularly, in the terms of “flat-faced”and “shortening of skull”, or also known as brachycephalia.

However, the exaggeration in the selective breeding towards the pursuit of the facial features above does not lead to the proportionately reduction of the soft tissues in the skulls, thus causing obstruction of the upper respiratory tract. Prevalence of BOAS varies according to the breeds. As of June 2024, the prevalence of BOAS in French Bulldogs in Taiwan, assessed using respiratory function grading (RFG) scheme, is approximately 50%. Other brachycephalic canine breeds such as Shih Tzu does not have as high prevalence as French Bulldogs.

This type of extreme breeding selection for brachycephalic features has led to deformation of the entire upper respiratory tract, causing obstruction in breathing as well as the external ear canal and the tympanic bulla. In some cases, craniovertebral junction abnormalities such as Syringomyelia and Chiari-like malformation may also occur.

Generally, puppies that are 6 months old and younger do not show BOAS-related signs. Affected dogs usually begin showing BOAS-related signs around the age of one year when they reach anatomical maturity. Clinical signs of BOAS include abnormal respiratory noises, excessive panting, exercise and heat intolerance, cyanosis, and even syncope. Brachycephalic dogs presenting with respiratory signs may also show gastrointestinal signs such as vomiting and regurgitation, which can seriously affect their quality of life. Studies have reported that nearly 60% of the owners of the affected dogs were unable to recognise BOAS. Hence, this may lead to delays in treatment, causing severity or even irreversible consequences.

Routine treatments for BOAS mainly focus on weight control and surgical intervention. The surgical procedures may differ according to the severity and lesion sites of BOAS. The most common post-op complications are regurgitations, aspiratory pneumonia and soft tissue swelling, which that may require further interventions.

Unfortunately, BOAS cannot be completely "cured". It is essential for veterinarians, owners and breeders to identify the signs of BOAS as well as the risk factors such as extreme traits, obesity, and narrowed nostrils.

Pathogenesis
Clinical symptoms
Clinical diagnosis
Treatment and prevention
Pathogenesis
The phenotypes of brachycephalic breeds of dogs are a result of selective breeding by humans. Brachycephalic, meaning "short-headed," refers particularly to the trait of a short muzzle in dogs. The premature closure of the spheno-occipital synchondrosis, primarily expanding longitudinally, is associated with the "short-headed" phenotype, observed more frequently in brachycephalic breeds than in mesocephalic breeds [1, 2].

After prolonged inbreeding to achieve desirable traits, brachycephaly in dogs has become more pronounced. Over time, from approximately 1910 to present, the skull shape of brachycephalic dogs has become much shorter and wider [3], with flatter facial characteristics. The infant-like features, such as larger eyes, flatter face and proportionally larger head in dogs and cats are thought to be more attractive, and thus influence the decision to own them. That says, some owners prioritize the appearance of dogs with little considering welfare-related breed attributes when purchasing them.

Inbreeding programs have resulted not only in a reduction of the gene pool and decreased diversity in the major histocompatibility complex, making modern dogs more susceptible to pathogen infection and autoimmune diseases, but also in conformation-related abnormalities [4]. These extreme brachycephalic traits and features are reported to be related with respiratory, ophthalmic dermatological, birthing, dental and heart issues [4].

Among all brachycephalic breeds of dogs, the extreme breeds namely English bulldog, French bulldogs and pugs are reported with higher prevalence of health issues in relation to their conformation. For English bulldogs, they were originally bred for bullbaiting. Their undershot jaw is thus for biting forcedly, loose skin for dropping blood away from the eyes during the fight, and wide shoulders are for looking strong. However, these physical traits can lead to issues such as skin fold dermatitis, prolapsed nictitating membrane gland, and mandibular prognathism [5]. The large head-to-pelvis ratio in Bulldogs often results in birthing difficulties, often necessitating a cesarean section [6].

French bulldogs and pugs are favored for their infant-like appearance, which triggers nurturing responses in humans [7]. The French bulldog was originally a cross breed by toy bulldogs and other terrier breeds [8]. Commonly observed disorders in French Bulldogs include brachycephalic obstructive airway syndrome (BOAS), otitis externa and media, skin fold dermatitis, and dystocia [9, 10].

Pugs were historically companion dogs for Chinese imperial families [11]. The most prevalent disorders in Pugs include BOAS, obesity, entropion, keratopathy syndrome, and otitis externa [12, 13, 14].

1. Julian, L.M.; Tyler, W.S.; Hage, T.J.; Gregory, P.W. Premature closure of the spheno‐occipital synchondrosis in the horned Hereford dwarf of the “short‐headed” variety. Am. J. Anat. 1957, 100, 269–287, doi:10.4324/9780203125236-39.

2. Schmidt, M.J.; Volk, H.; Klingler, M.; Failing, K.; Kramer, M.; Ondreka, N. Comparison of closure times for cranial base synchondroses in mesaticephalic, brachycephalic, and cavalier king charles spaniel dogs. Vet. Radiol. Ultrasound 2013, 54, 497–503, doi:10.1111/vru.12072.

3. Koch, D.A.; Sturzenegger, N. Veränderung des Schädels bei brachycephalen Hunden im Verlaufe der letzten 100 Jahre. Kurzmitteilungen | Short Commun. 1 SAT | ASMV 2015, 3, 2014–2016.

4. Packer, R.; O’Neill, D. Health and welfare of brachycephalic (flat-faced) companion animals: a complete guide for veterinary and animal professionals; CRC Press, 2021; ISBN 0429553811.

5. O’Neill, D.G.; Skipper, A.; Packer, R.M.A.; Lacey, C.; Brodbelt, D.C.; Church, D.B.; Pegram, C. English Bulldogs in the UK: a VetCompass study of their disorder predispositions and protections. Canine Med. Genet.2022, 9, 1–14, doi:10.1186/s40575-022-00118-5.

6. Ekenstedt, K.J.; Crosse, K.R.; Risselada, M. Canine Brachycephaly: Anatomy, Pathology, Genetics and Welfare. J. Comp. Pathol. 2020, 176, 109–115, doi:10.1016/j.jcpa.2020.02.008.

7. Paul, E.S.; Packer, R.M.A.; McGreevy, P.D.; Coombe, E.; Mendl, E.; Neville, V. That brachycephalic look: Infant-like facial appearance in short-muzzled dog breeds. Anim. Welf. 2023, 32, doi:10.1017/awf.2022.6.

8. Neill, D.G.O.; Baral, L.; Church, D.B.; Brodbelt, D.C.; Packer, R.M.A. Demography and disorders of the French Bulldog population under primary veterinary care in the UK in 2013. 2018, 1–12.

9. O’Neill, D.G.; Packer, R.M.A.; Francis, P.; Church, D.B.; Brodbelt, D.C.; Pegram, C. French Bulldogs differ to other dogs in the UK in propensity for many common disorders: a VetCompass study. Canine Med. Genet. 2021, 8, 1–14, doi:10.1186/s40575-021-00112-3.

10. O’neill, D.G.; O’sullivan, A.M.; Manson, E.A.; Church, D.B.; Boag, A.K.; Mcgreevy, P.D.; Brodbelt, D.C. Canine dystocia in 50 UK first-opinion emergency care veterinary practices: Prevalence and risk factors. Vet. Rec. 2017, 181, 88, doi:10.1136/vr.104108.

11. Moses, P.A. Welfare of Brachycephalic Dogs. North Am. Vet. Conf. 2016, 359–363.

12. O’Neill, D.G.; Darwent, E.C.; Church, D.B.; Brodbelt, D.C. Demography and health of Pugs under primary veterinary care in England. Canine Genet. Epidemiol. 2016, 3, 1–12, doi:10.1186/s40575-016-0035-z.

13. Asher, L.; Diesel, G.; Summers, J.F.; McGreevy, P.D.; Collins, L.M. Inherited defects in pedigree dogs. Part 1: Disorders related to breed standards. Vet. J. 2009, 182, 402–411, doi:10.1016/j.tvjl.2009.08.033.

14. Packer, R.M.A.; Hendricks, A.; Burn, C.C. Impact of facial conformation on canine health: Corneal ulceration. PLoS One 2015, 10, 1–16, doi:10.1371/journal.pone.0123827.
Clinical symptoms
This disease is characterized by clinical signs such as respiratory noise, dyspnea, exercise intolerance, heat intolerance, sleep disorders, regurgitation, vomiting, and cyanosis [1–5].

The anatomical features of BOAS include stenotic nares, elongated soft palate, nasopharyngeal turbinates, everted tonsils, everted laryngeal saccules, and laryngeal collapse [6]. Abnormal anatomy of the upper airway increases negative pressure during inspiration, leading to nasopharyngeal mucosal hyperplasia, narrowing of the airway tract, and eventual laryngeal collapse [7]. Stenotic nares, visible lesions in BOAS, can easily cause obstruction of the nasal meatus [7]. The incidence rate of stenotic nares ranges from 50% to 100% in brachycephalic dogs [8]. Elongated soft palate, present in 86% to 94% of BOAS-affected dogs, contributes to respiratory obstruction [9,10]. It weakens the palatine muscles, eventually leading to nasopharyngeal collapse [11].

The respiratory obstruction in brachycephalic breeds can also affect the gastrointestinal and cardiovascular systems. Upper airway obstruction increases luminal resistance, leading to regurgitation and vomiting due to increased thoracic negative pressure. Studies have found that 74% of brachycephalic dogs present with both respiratory and gastrointestinal symptoms [12,13]. The BOAS-related gastrointestinal lesions have been identified including hiatal hernias, pyloric stenosis, and esophageal deviation. Without treatment, BOAS can progress to pulmonary hypertension and right-sided heart failure, posing life-threatening risks to affected dogs over their lifetime [14]. The morbidity of BOAS is estimated to be around 20-40%, with brachycephalic dogs having a lower life expectancy of 3-4 years compared to other breeds [15].

While the prevalence is high in the extreme brachycephalic breeds, clinical signs of BOAS (e.g., snoring and exercise intolerance) are often normalized by the owners, with approximately 60% of the owner of affected dogs did not recognize the breathing problems of their dogs [16]. This has caused serious welfare concerns that many affected dogs are suffering from air hunger, acid reflux and sleep deprivation if their BOAS is left untreated.

1. Roedler, F.S.; Pohl, S.; Oechtering, G.U. How does severe brachycephaly affect dog’s lives? Results of a structured preoperative owner questionnaire. Vet. J. 2013, 198, 606–610, doi:10.1016/j.tvjl.2013.09.009.

2. Robertshaw, D. Mechanisms for the control of respiratory evaporative heat loss in panting animals. J. Appl. Physiol. 2006, 101, 664–668, doi:10.1152/japplphysiol.01380.2005.

3. Lilja-Maula, L.; Lappalainen, A.K.; Hyytiäinen, H.K.; Kuusela, E.; Kaimio, M.; Schildt, K.; Mölsä, S.; Morelius, M.; Rajamäki, M.M. Comparison of submaximal exercise test results and severity of brachycephalic obstructive airway syndrome in English bulldogs. Vet. J. 2017, 219, 22–26, doi:10.1016/j.tvjl.2016.11.019.

4. Venker-van Haagen, A. Ear, nose, throat, and tracheobronchial diseases in dogs and cats; Schlütersche, 2010; ISBN 3899930932.

5. Della Maggiore, A. An Update on Tracheal and Airway Collapse in Dogs. Vet. Clin. North Am. - Small Anim. Pract. 2020, 50, 419–430, doi:10.1016/j.cvsm.2019.11.003.

6. Riggs, J.; Liu, N.C.; Sutton, D.R.; Sargan, D.; Ladlow, J.F. Validation of exercise testing and laryngeal auscultation for grading brachycephalic obstructive airway syndrome in pugs, French bulldogs, and English bulldogs by using whole-body barometric plethysmography. Vet. Surg. 2019, 48, 488–496, doi:10.1111/vsu.13159.

7. Koch, D.A.; Arnold, S.; Hubler, M.; Montavon, P.M. Brachycephalic syndrome in dogs. Compend. Contin. Educ. Pract. Vet. 2003, 25, 48–55.

8. Lorenzi, D. De; Bertoncello, D.; Drigo, M. Bronchial abnormalities found in a consecutive series of 40 brachycephalic dogs. October 2008, 835–840.

9. Wardlaw, J.L.; Givaruangsawat, S. Brachycephalic airway obstructive syndrome in dogs: 90 cases (1991–2008). J. Am. Vet. Med. Assoc. 2010, 237, 2008–2011.

10. Torrez, C. V.; Hunt, G.B. Results of surgical correction of abnormalities associated with brachycephalic airway obstruction syndrome in dogs in Australia. J. Small Anim. Pract. 2006, 47, 150–154, doi:10.1111/j.1748-5827.2006.00059.x.

11. Crosse, K.R.; Bray, J.P.; Orbell, G.M.B.; Preston, C.A. Histological evaluation of the soft palate in dogs affected by brachycephalic obstructive airway syndrome. N. Z. Vet. J. 2015, 63, 319–325.

12. Poncet, C.M.; Dupre, G.P.; Freiche, V.G.; Estrada, M.M.; Poubanne, Y.A.; Bouvy, B.M. Prevalence of gastrointestinal tract lesions in 73 brachycephalic dogs with upper respiratory syndrome. J. Small Anim. Pract. 2005, 46, 273–279, doi:10.1111/j.1748-5827.2005.tb00320.x.

13. Poncet, C.M.; Dupre, G.P.; Freiche, V.G.; Bouvy, B.M. Long-term results of upper respiratory syndrome surgery and gastrointestinal tract medical treatment in 51 brachycephalic dogs. J. Small Anim. Pract.2006, 47, 137–142, doi:10.1111/j.1748-5827.2006.00057.x.

14. Hendricks, J.C. Brachycephalic airway syndrome. In Textbook of respiratory disease in dogs and cats; Elsevier, 2004; pp. 310–318.

15. Packer, R.; O’Neill, D. Health and welfare of brachycephalic (flat-faced) companion animals: a complete guide for veterinary and animal professionals; CRC Press, 2021; ISBN 0429553811.

16. Liu, N.C.; Sargan, D.R.; Adams, V.J.; Ladlow, J.F. Characterisation of brachycephalic obstructive airway syndrome in French bulldogs using whole-body barometric plethysmography. PLoS One 2015, 10, doi:10.1371/journal.pone.0130741.
Clinical diagnosis
Exercise performance phenotypic test is the simplest and commonly used physical examination in diagnosis for BOAS in dogs. For example, the 3-minute trot test and the 5-minute walk test, followed by pharyngolaryngeal auscultation and physical examination. The sensitivity of the 3-minute trot test was higher than the 5-minute walk test in French bulldogs, English bulldogs, and pugs when detecting clinically relevant BOAS [1]. Another diagnosis in the same study of BOAS is auscultation for laryngeal noise. The specificity of auscultation for laryngeal stridor to predict laryngeal collapse was 100%. That is to say, the 3-minute trot test with pharyngolaryngeal auscultation for grading the severity of BOAS in French bulldogs, English bulldogs, and pugs is recommended.

In a Finnish study, the 1000-meter distance walk test and 6-minute duration walk test were applied in BOAS diagnosis in English bulldogs [2]. The results showed that BOAS-affected dogs walked significantly shorter distances and more slowly than non-affected dogs.

Whole-body barometric plethysmography (WBBP) detects pressure changes within the chamber during inhalation and exhalation and analyzes volume using Boyle-Mariotte Law. WBBP has been extensively utilized for evaluating various respiratory conditions in both laboratory [3] and small animals [4-13]. It has been used to monitor airway obstruction [9,3-4], airway reactivity [4,15], feline lower airway disease [13,16], and brachycephalic obstructive airway syndrome (BOAS) [1,18]. The technique has been used to quantify the severity of BOAS by generating a BOAS index [19], the severity score from 0 (BOAS free) to 100% (severe BOAS). This objective and non-invasive respiratory function test allowed further studies on evaluating conformation related risk factors for BOAS , assessing surgery effectiveness [20-22], and genetics.

1. Riggs, J.; Liu, N.C.; Sutton, D.R.; Sargan, D.; Ladlow, J.F. Validation of exercise testing and laryngeal auscultation for grading brachycephalic obstructive airway syndrome in pugs, French bulldogs, and English bulldogs by using whole-body barometric plethysmography. Vet. Surg. 2019, 48, 488–496, doi:10.1111/vsu.13159.

2. Lilja-Maula, L.; Lappalainen, A.K.; Hyytiäinen, H.K.; Kuusela, E.; Kaimio, M.; Schildt, K.; Mölsä, S.; Morelius, M.; Rajamäki, M.M. Comparison of submaximal exercise test results and severity of brachycephalic obstructive airway syndrome in English bulldogs. Vet. J. 2017, 219, 22–26, doi:10.1016/j.tvjl.2016.11.019.

3. Hamelmann, E.; Schwarze, J.; Takeda, K.; Oshiba, A.; Larsen, G.L.; Irvin, C.G.; Gelfand, E.W. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 1997, 156, 766–775.

4. Hoffman, A.M.; Dhupa, N.; Cimetti, L. Airway reactivity measured by barometric whole-body plethysmography in healthy cats. Am. J. Vet. Res. 1999, 60, 1487–1492.

5. Halloy, D.J.; Kirschvink, N.A.; Vincke, G.L.; Hamoir, J.N.; Delvaux, F.H.; Gustin, P.G. Whole body barometric plethysmography: a screening method to investigate airway reactivity and acute lung injuries in freely moving pigs. Vet. J. 2004, 168, 276–284.

6. Kirschvink, N.; Leemans, J.; Delvaux, F.; Snaps, F.; Marlin, D.; Sparkes, A.; Clercx, C.; Gustin, P. Non-invasive assessment of growth, gender and time of day related changes of respiratory pattern in healthy cats by use of barometric whole body plethysmography. Vet. J. 2006, 172, 446–454.

7. Talavera, J.; Kirschvink, N.; Schuller, S.; Le Garrérès, A.; Gustin, P.; Detilleux, J.; Clercx, C. Evaluation of respiratory function by barometric whole-body plethysmography in healthy dogs. Vet. J. 2006, 172, 67–77.

8. Hirt, R.A.; Vondrakova, K.; de Arespacochaga, A.G.; Gütl, A.; van den Hoven, R. Effects of cadmium chloride inhalation on airflow limitation to histamine, carbachol and adenosine 5′-monophosphate assessed by barometric whole body plethysmography in healthy dogs. Vet. J. 2007, 173, 62–72.

9. Hirt, R.A.; Leinker, S.; Mosing, M.; Wiederstein, I. Comparison of barometric whole body plethysmography and its derived parameter enhanced pause (PENH) with conventional respiratory mechanics in healthy Beagle dogs. Vet. J. 2008, 176, 232–239.

10. Kirschvink, N.; Leemans, J.; Delvaux, F.; Snaps, F.; Clercx, C.; Gustin, P. Non-invasive assessment of airway responsiveness in healthy and allergen-sensitised cats by use of barometric whole body plethysmography. Vet. J. 2007, 173, 343–352.

11. Bernaerts, F.; Talavera, J.; Leemans, J.; Hamaide, A.; Claeys, S.; Kirschvink, N.; Clercx, C. Description of original endoscopic findings and respiratory functional assessment using barometric whole-body plethysmography in dogs suffering from brachycephalic airway obstruction syndrome. Vet. J. 2010, 183, 95–102.

12. Manens, J.; Bolognin, M.; Bernaerts, F.; Diez, M.; Kirschvink, N.; Clercx, C. Effects of obesity on lung function and airway reactivity in healthy dogs. Vet. J. 2012, 193, 217–221.

13. Lin, C.-H.; Lee, J.-J.; Liu, C.-H. Functional assessment of expiratory flow pattern in feline lower airway disease. J. Feline Med. Surg. 2014, 16, 616–622.

14. Rozanski, E.A.; Hoffman, A.M. Lung mechanics using plethysmography and spirometry. Textb. Respir. Dis. dogs cats. St Louis Saunders 2004, 175–180.

15. Bergren, D.R. Chronic tobacco smoke exposure increases airway sensitivity to capsaicin in awake guinea pigs. J. Appl. Physiol. 2001, 90, 695–704.

16. Lin, C.; Wu, H.; Lee, J.; Liu, C. Functional phenotype and its correlation with therapeutic response and inflammatory type of bronchoalveolar lavage fluid in feline lower airway disease. J. Vet. Intern. Med.2015, 29, 88–96.

17. Riggs, J.; Liu, N.C.; Sutton, D.R.; Sargan, D.; Ladlow, J.F. Validation of exercise testing and laryngeal auscultation for grading brachycephalic obstructive airway syndrome in pugs, French bulldogs, and English bulldogs by using whole-body barometric plethysmography. Vet. Surg. 2019, 48, 488–496, doi:10.1111/vsu.13159.

18. Liu, N.C.; Sargan, D.R.; Adams, V.J.; Ladlow, J.F. Characterisation of brachycephalic obstructive airway syndrome in French bulldogs using whole-body barometric plethysmography. PLoS One 2015, 10, doi:10.1371/journal.pone.0130741.

19. Liu, N.C.; Adams, V.J.; Kalmar, L.; Ladlow, J.F.; Sargan, D.R. Whole-Body Barometric Plethysmography Characterizes Upper Airway Obstruction in 3 Brachycephalic Breeds of Dogs. J. Vet. Intern. Med. 2016, 30, 853–865, doi:10.1111/jvim.13933.

20. Liu, N.C.; Troconis, E.L.; Kalmar, L.; Price, D.J.; Wright, H.E.; Adams, V.J.; Sargan, D.R.; Ladlow, J.F. Conformational risk factors of brachycephalic obstructive airway syndrome (BOAS) in pugs, French bulldogs, and bulldogs. PLoS One 2017, 12, 1–24, doi:10.1371/journal.pone.0181928.

21. Liu, N.C.; Genain, M.A.; Kalmar, L.; Sargan, D.R.; Ladlow, J.F. Objective effectiveness of and indications for laser-assisted turbinectomy in brachycephalic obstructive airway syndrome. Vet. Surg. 2019, 48, 79–87, doi:10.1111/vsu.13107.

22. Liu, N.C.; Oechtering, G.U.; Adams, V.J.; Kalmar, L.; Sargan, D.R.; Ladlow, J.F. Outcomes and prognostic factors of surgical treatments for brachycephalic obstructive airway syndrome in 3 breeds. Vet. Surg.2017, 46, 271–280, doi:10.1111/vsu.12608.
Treatment and prevention