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Beyond OSA—Part 1 by Dr. Michael K. DeLuke

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Categories: Orthodontics; Pediatric; Sleep Medicine;
Beyond OSA 

Understanding the full spectrum of pediatric sleep-disordered breathing

by Dr. Michael K. DeLuke

Introduction
While it is universally recognized that quality sleep is central to a healthy childhood, the role of the dental professional in detecting and managing pediatric airway compromise can be a contentious topic. Many believe that dental professionals are the best first line of defense to detect and address airway issues in children, while others argue they should have little to no involvement with airway management, as it is the role of our medical colleagues. Interestingly, the articles that attempt to dissuade dental professionals from playing a role in airway management focus almost solely on obstructive sleep apnea (OSA). In doing so, they neglect to recognize the fact that airway disease does not begin and end with a diagnosis of OSA. Rather, it exists across a spectrum commonly referred to as sleep-disordered breathing (SDB), with primary snoring on one end and OSA on the other.

The purpose of this two-part series is to help dental practitioners gain a greater understanding of the essential role they can and should play in the detection and management of pediatric sleep-disordered breathing (pSDB), with the ultimate goal of preventing the progression of the disease to OSA. Here, in Part I, we will discuss what SDB is, why using the apnea-hypopnea index (AHI) as the sole determinant of airway compromise in children is a flawed methodology, the multitude of issues associated with pediatric sleep studies and the comorbidities of pediatric sleep-disordered breathing (pSDB). In a future issue, Part II will review how to detect the signs and symptoms of pSDB during the clinical and radiographic exam and will explain what dental practitioners can do when they suspect their patient is suffering from pSDB.

Once you understand these concepts and develop a more whole-health approach to patient care, you will be equipped with the tools necessary to improve the quality of life of your pediatric patients and their families in ways you never imagined possible.


A spectrum of breathing disorders
Sleep-disordered breathing is a general term used to describe the disruption of normal respiratory patterns and ventilation during sleep. It encompasses a spectrum of breathing disorders, including primary snoring, upper-airway resistance syndrome (UARS), sleep-related hypoventilation and, ultimately, OSA.1 The etiology of SDB is multifactorial,2 and the diagnosis relies on symptoms (medical history and physical exam), as there is no specific set of diagnostic criteria.3 It is estimated that approximately 10% to 14% of children suffer from pSDB, although some studies state the prevalence is much higher as it is often undiagnosed.4,5
Beyond OSA—Part 1
Fig. 1: Clinical spectrum of SDB

pSDB has been found to cause physical and mental health issues and can be a major psychosocial stressor for children and their families, yet the full scope of its effect on health remains underappreciated by many clinicians.6,7 Furthermore, it is important to note that disease severity often progresses across the spectrum of pSDB, as children who suffer from primary snoring are at increased risk of developing OSA in the future.8 OSA, the most severe form of SDB, is a condition in which part or all of the airway is repeatedly obstructed during sleep, leading to impaired breathing and abnormal changes in blood gas.9 A diagnosis of OSA is made using polysomnography (PSG) to determine the number of apneas (complete cessation of breathing) and hypopneas (partial cessation of breathing) lasting 10 or more seconds in a one-hour period averaged over a night of sleep. This is referred to as the apnea hypopnea index, or AHI (Fig. 1). Additionally, in 2007, the American Academy of Sleep Medicine (AASM) recommended that in children, an apnea or hypopnea of at least two breaths duration be considered an obstructive event.10 The first full account of OSA using PSG was published in 1973 by Guilleminault et al., and it is estimated that 1% to 5% of children have OSA.11,12
Beyond OSA—Part 1
Fig. 2: Apnea Hypopnea Index

Interestingly, while many dental practitioners are familiar with the comorbidities, signs and symptoms of OSA, the same cannot be said for SDB. In fact, most studies in the dental and orthodontic literature don’t even mention SDB, or sleep-related breathing disorders (SRBD), as it is sometimes called. This is a significant flaw of the 2019 AAO White Paper, titled Obstructive Sleep Apnea and Orthodontics, which mentions OSA 276 times but SDB/SRBD only 15 times, mostly in appendices and references.13 As such, the authors neglect to acknowledge the spectrum of diseases that comprise SDB and instead focus solely on end-stage disease, or OSA. Further, they overlooked the serious medical, dental, behavioral and neurocognitive comorbidities of pSDB, and missed a valuable opportunity to highlight the critical role the dental professional can play in preventing a child from developing OSA in the first place.


Issues with the pediatric AHI scale
The AHI scale for adults was developed by evaluating the sleep of asymptomatic men and women 40 to 60 years of age.14 The pediatric AHI scale, by contrast, was created by extrapolating the data from the adult scale. In fact, not a single randomized controlled trial was conducted to develop the pediatric AHI scale. As stated by Carroll et al, childhood OSA is not simply adult OSA in smaller people, as OSA in children differs in several important ways from OSA in adults.15 Children have a more rapid respiratory rate and lower functional residual capacity than do adults. Therefore, children are more likely to desaturate with shorter respiratory events and even these short events can be clinically significant.16 Additionally, children have increased central ventilatory drive during sleep which accounts for the increased upper airway reflexes and tone, resulting in less collapsibility than in adults. Thus, children often have a specific breathing pattern of obstructive hypoventilation rather than the discrete, cyclic obstructive pattern that is commonly seen in adult OSA.17

Additionally, as Sedky et al. referenced in 2014, the AHI cutoff limit used to diagnose pOSA remains controversial in the medical community.18 In fact, Rosen et al. found that at least 80% of children with serious sleep-related upper-airway obstruction do not have repetitive, complete obstructive apneas and therefore their airway compromise is not identified by the AHI.19 The authors concluded that adult criteria for OSA based on the number of apneas and hypopneas will fail to identify the majority of children with serious upper-airway obstruction during sleep. Hence, even children who score zero on the AHI after a sleep study may still be suffering from airway obstruction and its associated comorbidities. I have witnessed this on numerous occasions in my clinical practice.

The late Dr. Christian Guilleminault, considered by many to be the godfather of sleep medicine, stated, “Even if a diagnostic PSG is done, a poor understanding of abnormal breathing patterns during sleep in children may lead to underscoring of respiratory events.”20 Further, even though Dr. Guilleminault developed the AHI, he stated that the significant variability in the pediatric AHI directly affects the interpretation of disease severity and the subsequent treatment plan.21 Interestingly, while the medical community openly acknowledges the numerous flaws in using the AHI scale to detect the presence or absence of airway disease in children, the dental community seems to embrace it as an absolute certainty regardless of the preponderance of evidence to prove otherwise.


Challenges associated with conducting sleep studies in children
Another issue with using AHI as a barometer for determining the presence or absence of airway disease in children pertains to obtaining and interpreting sleep studies. Pediatric sleep studies are fraught with challenges (Fig. 3). In a recent conversation with a pediatric otolaryngologist, he described the sleep study industry as the “wild, wild west” and explained that there is a complete lack of standardization across the industry. In fact, one may be surprised to learn that the AASM rules for scoring sleep are neither compulsory nor universally accepted.22 For example, one sleep lab may test for respiratory effort related arousals (RERAs), while another may not. One may count an apnea or hypopnea of 10 seconds or more as an obstructive event in children, another may count two missed breaths, and still another may count both.
Beyond OSA—Part 1
Fig. 3: Challenges associated with conducting sleep studies in children

Additionally, Yoon et al. described a phenomenon known as the “first-night effect,” whereby the first night a child spends in a sleep lab yields inaccurate data since he or she is sleeping in a foreign place, hooked up to numerous electrodes and machinery.23 The authors recommended that sleep centers use two or even three successive nights of PSG recordings and discard the data from the first night. Some cite this as the reason why pediatric sleep studies suffer from poor test-retest reliability.24

Sleep studies are very costly to both conduct and interpret, and the expenses may not be covered by insurance, creating a significant financial obstacle for many families. There can also be logistical issues, including lack of access to a facility and challenges associated with a parent remaining with their child in the sleep lab overnight. It can even be difficult to get the patient’s pediatrician to prescribe a sleep study in the first place, and if they do, there is a shortage of sleep physicians to read and interpret the data, with approximately one sleep physician for every 43,000 sleep studies conducted.25

Despite these well-documented issues, many dental practitioners continue to rely on PSG and a formal diagnosis of OSA as the sole determinate of the presence or absence of airway disease in children. This mentality fails to acknowledge the spectrum of diseases that comprise pSDB and also allows children who are suffering from pSDB but do not (yet) have a formal diagnosis of pOSA to suffer unnecessarily. To that point, Tan and colleagues stated that measures derived from sleep studies in children, “are often not predictive of SDB-associated comorbidities.”26


Skeletal and dental comorbidities of pSDB
Epigenetics is the process whereby environment and behaviors change gene activity without altering the DNA sequence. An example of this is the impact of mouth breathing on craniofacial growth and development. We have known for more than 150 years that patients who breathe through their mouths experience aberrant craniofacial growth and development. In fact, the term “adenoid facies” was first described in 1870 by Wilhelm Meyer as “a long, lean face with a high-arched palate and dental crowding often seen in children with chronic airway obstruction due to enlarged adenoids.”27 Melvin Moss explained this process in greater detail in 1962 with his functional matrix hypothesis, which states that form follows function and functional demands determine the final shape of the osseous structures in the head and neck.28 Moss later noted that nasal breathing promotes proper dentofacial growth and development, and in 2022, Bromage elaborated on this concept when he stated that the functional matrix of the craniofacial respiratory complex is air.29,30

Harvold demonstrated this with his studies on purebred rhesus monkeys in the 1970s, whereby he plugged their noses with silicone and evaluated their craniofacial growth and development over time.31 He found that the monkeys whose noses had been plugged and were therefore obligate mouth breathers, developed narrower dental arches, more vertical facial growth, more dental crowding and more severe malocclusions. When the plugs were removed, the monkey’s craniofacial growth began to normalize.

Bresolin et al. published a study in the American Journal of Orthodontics in 1983 demonstrating that mouth breathers had a larger anterior facial height, greater angular relationship of S-N, palatal and occlusal planes, larger gonial angle, more retrognathic mandibular, higher palatal vault height, greater overjet, narrower maxillary intermolar width and higher prevalence of posterior crossbite.32 This was echoed by Huyhn et al. in their 2013 publication in American Journal of Orthodontics and Dentofacial Orthopedics.33 Conversely, a study published in 2023 in the Journal of Stomatology and Oral Maxillofacial Surgery found that nasal breathers had greater oropharyngeal airway volume, greater total pharyngeal airway volume and larger intermolar and intercanine width compared to mouth breathers.34

Guilleminault and Huang explained the pathophysiology of these changes in their 2018 article published in Sleep Medicine Reviews, wherein they concluded that mouth breathing leads to the development of a smaller- than-typical upper-airway with an increased risk of collapse during sleep.35 As a result, mouth-breathing patients develop facial dysmorphism that progressively worsens over time, leading to more mouth breathing. This negative feedback loop often leads to the development of OSA—epigenetics and Moss’s functional matrix at work!

Dental professionals must detect and address the signs and symptoms of mouth breathing and snoring in children, even in the absence of a formal diagnosis of OSA. Not doing so can allow for progressive worsening of aberrant craniofacial growth.


Medical and behavioral comorbidities of pSDB
The dental professional must also understand that a child does not need to have OSA to suffer from the behavioral and neurocognitive comorbidities of pSDB, including hyperactivity or ADHD, aggressive behavior, morning headaches, daytime sleepiness, insomnia, learning difficulties or poor school performance, delayed puberty, failure to thrive, recurrent otitis media and other upper respiratory infections, and elevated inflammatory cytokines.36–40 comprehensive list of common nighttime and daytime comorbidities of pSDB can be found in Figure 4.
Beyond OSA—Part 1
Fig. 4: Children with SDB may exhibit

Numerous studies demonstrate the significant and adverse neurocognitive and behavioral sequelae in children which are believed to be because of the intermittent nocturnal hypoxia and sleep fragmentation that occur across the spectrum of pSDB. Bonuck et al. prospectively examined more than 11,000 children from infancy to seven years of age and determined that early-life SDB has strong, persistent and statistically significant detrimental effects on childhood behavior.41 Gozal et al. studied 1,010 children ages 5 to 7 years old and concluded that snoring alone has a significant impact on neurocognitive development.42 Isaiah et al. evaluated the MRIs of 10,140 children enrolled in the Adolescent Brain and Cognitive Development study and found that children who snored or even gasped during sleep had smaller volumes of gray matter in their frontal lobes.43 Menzies conducted a systematic review of 63 studies and concluded that breathing disturbances from snoring to OSA were linked to deficits across all aspects of neurocognitive function, including intelligence, attention, memory, language and visual-spatial skills.44


Summary
Pediatric SDB encompasses a spectrum of breathing disorders with serious dental, skeletal, behavioral and neurocognitive comorbidities and consequences. Additionally, PSG and the AHI are not always reliable indicators of airway disease in children, and as such, children can suffer from airway compromise and the associated comorbidities even in the absence of a formal diagnosis of OSA. Therefore, dental professionals must proactively detect and address SDB in their pediatric patients to minimize both the prevalence and severity of the aforementioned comorbidities, as well as decrease the chances that the airway disease will progress to OSA. As Drs. Kim, Kim and Yoon recently stated, “Through timely targeted interventions to enhance the skeletal framework and upper airway volumes in growing patients, dentists can help prevent or mitigate the progression to OSA.”45

In Part II, we will discuss how to screen your pediatric patients for pSDB, when and how to coordinate care with your medical colleagues, and how normalizing anatomy with interceptive orthodontic treatment can help address airway compromise. OT

References
1.Kheirandish-Gozal L, Gozal D. A comprehensive clinical guide to evaluation and treatment. New York (NY): Springer Science; 2012. Sleep disordered breathing in children. 
2. Marcus CL: Sleep-disordered breathing in children. Curr Opin Pediatr. 2000, 12:208-12.
3. Kim KA, Kim, SJ, Yoon A. Craniofacial anatomical determinants of pediatric sleep-disordered breathing: A comprehensive review. J Prosthodont. 2024 Nov 18. doi: 10.1111/jopr.13984.
4. Paglia, L.; Colombo, S. Perinatal oral health: Focus on the mother. Eur. J. Paediatr. Dent. 2019;20:209–213
5.Lopes MC, Guilleminault C. Chronic snoring and sleep in children: a demonstration of sleep disruption. Pediatrics 2006;118:e741-6.
6. Guilleminault C, Lee JH, Chan A. Pediatric Obstructive Sleep Apnea Syndrome. Arch Pediatr Adolesc Med. 2005;159(8):775–785.
7. Gipson K, Lu M, Kinane TB. Sleep-Disordered Breathing in Children. Pediatr Rev. 2019 Jan;40(1):3-13.
8. American Academy of Sleep Medicine. International classification of sleep disorders: diagnostic and coding manual. 2nd ed. Westchester, IL: American Academy of Sleep Medicine; 2005.
9. American Thoracic Society. Standards and indications for cardiopulmonary sleep studies in children. Am J Respir Crit Care Med. 1996;153:866–878.
10. Iber C, Ancoli-Israel S, Chesson AL Jr., Quan SF; for the American Academy of Sleep Medicine. The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications. 1st ed. Westchester, IL: American Academy of Sleep Medicine, 2007.
11. Guilleminault CB, Eldridge FL, Simmons B, and Dement WC. Sleep Apnea in Eight Children. Pediatrics. 1976;58:23-30.
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14. Guilleminault C, , Van den Hoed L and Mitler M. “Clinical Overview of the Sleep Apnea Syndromes,” In: A. R. Liss, Ed., Sleep Apnea Syndromes, New York, 1978, pp. 1-11.
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17. Isono S, Tanaka A, Ishikawa T, Nishino T. Developmental changes in collapsibility of the passive pharynx during infancy. Am J Respir Crit Care Med 2000;162:832–836.
18. Sedky K, Bennett DS, Carvalho KS. Attention deficit hyperactivity disorder and sleep disordered breathing in pediatric populations: A meta-analysis. Sleep Med Rev. 2014;18:349-56.
19. Rosen CL, D’Andrea L, Haddad GG. Adult criteria for obstructive sleep apnea do not identify children with serious obstruction. Am Rev Respir Dis. 1992;Nov;146(5 Pt 1):1231-4.
20. Guilleminault C, Akhtar F. Pediatric sleep-disordered breathing: New evidence on its development. Sleep Medicine Reviews. 2015;24:46-56.
21. Guilleminault C, Lin CH. Current hypopnea scoring criteria underscore pediatric sleep disordered breathing. Sleep Medicine. 2011;12:720-729.
22. Miano S, Paolino MC, Castaldo R, Villa MP. Visual scoring of sleep: A comparison between the Rechtschaffen and Kales criteria and the American Academy of Sleep Medicine criteria in a pediatric population with obstructive sleep apnea syndrome. Clinical Neurophysiology; 2010,121(1):39-42.
23. Yoon SYR, Jain U, Shapiro C. Sleep in attention-deficit/hyperactivity disorder in children and adults: Past, present, and future. Sleep Medicine Reviews. 2012;16(4):371-388.
24. Villa MP, Pietropaoli N, Supino MC, Vitelli O, Rabasco J, Evangelisti M, Del Pozzo M, Kaditis AG. Diagnosis of Pediatric Obstructive Sleep Apnea Syndrome in Settings With Limited Resources. JAMA Otolaryngol Head Neck Surg. 2015 Nov;141(11):990-6.
25. Watson NF, Rosen IM, Chervin RD. Board of directors of the American Academy of Sleep Medicine. The past is prologue: the future of Sleep Medicine. J Clin Sleep Med. 2017;13(1):127-135.
26. Tan, H.L.; Gozal, D.; Kheirandish-Gozal, L. Obstructive sleep apnea in children: A critical update. Nat. Sci. Sleep. 2013; 5:109–123.
27. Meyer W. On Adenoid Vegetations in the Naso-pharyngeal Cavity: their Pathology, Diagnosis, and Treatment. Med Chir Trans. 1870;53:191-216.
28. Moss ML. The functional matrix. In: Kraus B, Reidel R, editors. Vistas in orthodontics. Philadelphia: Lea and Febiger, 1962:85-98.
29. Moss ML, Salentijn L. The primary role of functional matrices in facial growth. Am J Orthod, 1969;55(6):566-77.
30. Bromage TG. The Functional Matrix Hypothesis Revisited. 5. Orofacial Capsular Matricies Defined. Innovation. September 2022. 1(4):e1. Doi:10.30771/2022.3.
31. Harvold EP, Tomer BS, Vargervik K, Chierici G. Primate experiments on oral respiration. 1981;79(4):359-72.
32. Bresolin D, Shapiro PA, Shapiro GG, Chapko MK, Dassel S. Mouth breathing in allergic children; its relationship to dentofacial development. 1983;83(4)334-40.
33. Huynh NT, Morton PD, Rompré PH, Papadakis A, Remise C. Associations between sleep-disordered breathing symptoms and facial and dental morphometry, assessed with screening examinations. Am J Orthod Dentofacial Orthop. 2011 Dec;140(6):762-70.
34. Habumugisha J, Mohamed AS, Cheng B, Liu L, Zou R, Wang F. Analysis of maxillary arch morphology and its relationship with upper airway in mouth breathing subjects with different sagittal growth patterns. J Stomatol Oral Maxillofac Surg. 2023 Feb;124(1S):101386. 
35. Guilleminault C, Huang YS. From oral facial dysfunction to dysmorphism and the onset of pediatric OSA. Sleep Medicine Reviews. 2018;40:203-214.
36. Ali NJ, Pitson DJ, Stradling JR. Snoring, sleep disturbance, and behaviour in 4-5 year olds. Arch Dis Child. 1993;68:360-6.
37. Halbower AC, Degaonkar M, Barker PB, Earley CJ, Marcus CL, Smith PL, et al. Childhood obstructive sleep apnea associates with neuropsychological deficits and neuronal brain injury. PLoS Med. 2006;3:1391-402.
38. Mitchell RB, Pereira KD, Friedman NR. Sleep-disordered breathing in children: survey of current practice. Laryngoscope. 2006;116: 956-8.
39. Goldstein NA, Post JC, Rosenfeld RM, Campbell TF. Impact of tonsillectomy and adenoidectomy on child behavior. Arch Otolaryngol Head Neck Surg. 2000;126:494-8.
40. Gozal D. Sleep-disordered breathing and school performance in children. Pediatrics. 1998;102(3 Pt 1):616-20.
41. Bonuck K, Freeman K, Chervin RD, Xu L. Sleep-disordered breathing in a population-based cohort: behavioral outcomes at 4 and 7 years. Pediatrics. 2012 Apr;129(4):e857-65.
42. Hunter SJ, Gozal D, Smigh DL, Philby MF, Kaylegian J, and Kheirandish-Gozal L. effect of sleep-disordered breathing severity on cognitive performance measures in a large community cohort of young school-aged children. Am J Respir Crit Care Med. 2016;194(6):739–747.
43. Isaiah A, Ernst T, Cloak CC, Clark DB, Chang L. Associations btw frontal lobe structure, parent reported obstructive SDB and childhood behavior in the ABC dataset. Nature Communications. 2021,12:2205, https://doi.org/10.1038/s41467-021-22534-0.
44. Menzies B, Teng A, Burns M, Lah S. Neurocognitive outcomes of children with sleep disordered breathing: A systematic review with meta-analysis. Sleep Med Rev. 2022 Jun;63:101629. doi: 10.1016/j.smrv.2022.101629. Epub 2022 Mar 31.PMID: 35439720.
45. Kim KA, Kim SJ, Yoon A. Craniofacial anatomical determinants of pediatric sleep-disordered breathing: A comprehensive review. J Prosthodont. 2024 Nov 18. doi: 10.1111/jopr.13984. Epub ahead of print. PMID: 39557815.

Author Bio
Dr. Michael K. DeLuke Dr. Michael K. DeLuke is a board-certified orthodontist who received his specialty training at the University of Connecticut. DeLuke practiced for 18 years at DeLuke Orthodontics before retiring from private practice to teach full time. He has served as a faculty member at several hospitals and orthodontic residencies, including as the cleft-craniofacial orthodontist at Albany Medical Center in New York, and is currently an adjunct professor in the Department of Orthodontics at NSU.
DeLuke founded DeLuke Orthodontic Coaching (DOC), an ADA CERP-recognized provider. He also created “The DOC Podcast” to help his colleagues attain the highest level of personal, professional and financial success. DeLuke is a fitness enthusiast and former boxer who still actively trains. He resides in Naples, Florida, with his wife and two teenage daughters.



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