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Authors: Dr. Suraj Agarwal

Abstract:

Cone beam computed tomography (CBCT) has several applications in dentomaxillofacial diagnosis. Frequently, the imaged volume encompasses the upper airway. This article provides a systematic approach to airway analysis and the implications of the anatomic and pathologic alterations. It discusses the role of CBCT in management of obstructive sleep apnea (OSA) patients and also highlights technological advances that combine CBCT imaging with computational modeling of the airway and the potential clinical applications of such technologies.

INTRODUCTION

Sleep-related breathing disorders are characterized by abnormal respiration during sleep and include primary central sleep apneas, obstructive sleep apneas and sleep-related hypoventilation and hypoxemia. The focus of this article is on obstructive sleep apnea (OSA), where an obstruction in the upper airway results in increased breathing effort and inadequate ventilation. OSA is characterized by partial to complete obstruction of the pharyngeal airway during sleep, which results in disrupted airflow and repeated episodes of hypopnea (decrease inairflow by 25 percent to 50 percent witha decrease in oxygen saturation by ≥ 4percent) or apnea (cessation of airflowfor 10 seconds) and consequent arousalfrom sleep. The frequency of these eventsduring sleep is termed as the apnea/hypopnea index (AHI). A diagnosis ofsleepapnea is established when the AHIis > 15/hour or > 5/hour in a patientwho reports other symptoms such asdaytime sleepiness. The diagnosis ofOSA is established by polysomnography(PSG), an in-laboratory sleep test. The disordered sleep patternmanifests as excessive daytime sleepiness,impaired cognitive function and fatigue.Additionally, there is evidence thatOSA is an independent risk factor for several comorbid conditions andmortality, including cardiac arrhythmias,hypertension, coronary artery disease,type II diabetes mellitus and mood andanxiety disorders.1,2,3,4,5 Thus, untreated, OSAis a major public health concern withsubstantial societal consequences and anenormous economic burden, includingdecreased work productivity, a two tosevenfold increased risk of automobileaccidents and a two to threefold increasedrisk for occupational injuries.6,7 It isestimated that the prevalence of OSAis approximately 3 percent to 7 percent in men and 2 percent to 5 percent inwomen.4 Notably, the prevalence of OSA is as high as 41 percent to 78 percent inobese and overweight individuals and50 percent to 80 percent in individualswith severe craniofacial abnormalitiesand syndromic craniosynostosis.8,9As health care professionals, it isimportant that dentists be familiarwith the manifestations of sleep-relatedbreathing disorders so that they canidentify symptoms of these disorders and initiate referrals to appropriate specialists. Cone beam computed tomography(CBCT) has been used increasinglyin dentistry to obtain 3-D images ofthe maxillofacial structures and hasapplications in several dental andmaxillofacial diagnostic and treatmentplanningtasks.11 Often, the upperairway is encompassed in the volume ofthese CBCT scans, providing dentiststhe opportunity to evaluate upperairway morphology. Furthermore,many dentists are actively involvedin the treatment of OSA patientswith oral appliances (OA) and mayacquire CBCT scans specifically toevaluate upper airway dimensions. Thismanuscript provides the reader with anoverview of upper airway evaluationon CBCT scans. The appearances andclinical significance of pathologicalconditions that compromise the upperairway are described, with guidance onmanaging incidental findings. The roleof CBCT as an imaging modality tospecifically evaluate the upper airway inpatients with OSA is discussed. Finally,technological advances that combineCBCT imaging with computer-simulatedairflow modeling are highlighted.

Normal Upper Airway Anatomyand Function

The upper airway is a complexstructure composed of the anterior naresand nasal cavities, the pharynx, larynx andthe extrathoracic trachea. The pharynxis typically considered in four zones— the nasopharynx, the velopharynx,the oropharynx and the hypopharynx(Figure 1). The nasopharynx extendsfrom the posterior aperture of the nasalcavity to the level of the hard palate.The velopharynx extends from thehorizontal plane of the hard palatecaudally to the tip of the uvula. Theoropharynx is defined anteriorly by thetongue and posteriorly and laterally bythe pharyngeal walls. It extends fromthe uvula to the base of the epiglottis. Portions of the upper airway are boundby muscular structures such as the softpalate, the tongue and the pharyngeal wall.The muscles that control these structuresstrongly influence the patency of theairway. To appreciate airway obstructionin patients with OSA, it is important tounderstand how this muscular controlmodulates the airway size. The soft palate

and the tongue form the anterior wall of thepharyngeal airway. The superior, middle andinferior constrictors make up the posteriorpharyngeal wall. The lateral pharyngealwalls are formed by several differentstructures, including the hyoglossus,styloglossus, stylohyoid, stylopharyngeus,palatopharyngeus, palatoglossus, thepharyngeal constrictors, adipose tissue and the palatine tonsils. In a passive state,without muscle activity, the cross-sectionaldimension of the airway is a function ofthe transmural pressure — the pressuredifferential between the intraluminalpressure and tissue pressure. A decrease inthe intraluminal pressure or an increase in the tissue pressure will narrow the airway.Mechanical influences on upper

airway dimension include static factors,such as neck and jaw position, andgravity. For example, in a slightly openjaw, there is more room in the oral cavityfor the tongue, resulting in an increasein the size of the pharynx. However, asthe mandible moves further posteriorly upon opening, it causes the tongue andthe hyoid apparatus to move posteriorly,thereby narrowing the pharyngeal airway. When the patient is in a supine position,gravitational forces on the tongue andsoft palate result in airway narrowing.Dynamic factors that influencepharyngeal airway patency includeupstream resistance in the nasal cavityand pharynx, tissue compliance andpharyngeal muscle activity. The anatomyof the nasal cavity is relatively complexand provides high resistance, yielding aturbulent airflow. This results in a morenegative nasopharyngeal intraluminalpressure. Likewise, high resistance withinthe nasopharynx/oropharynx due to anatomical constraints is associated witha more negative intraluminal pressure atsites caudal to these anatomic constraints.As a result of this upstream airwayresistance, the lumen of the pharyngealairway is narrowed during inspiration. The phasic activation of the skeletal muscles surrounding the airway helps to dilate the airway and stiffen the pharyngeal walls during inspiration. During wakefulness,

pharyngeal patency is maintained bycoordinated muscle control by thecentral nervous system. Decrease in themotor output to the pharyngeal musclesduring sleep results in decreased muscletone, narrowing of the airway lumenand an increase in airway resistance. Asa feedback mechanism, the increasingnegative pressure and rising carbon dioxidelevels stimulate the pharyngeal muscles to restore airway patency. However, inan anatomically aberrant airway, thesereflexes may not sufficiently compensatefor the reduced airway diameter andthe risk of airway collapse increases.

Normal Upper Airway Anatomyand Function

The upper airway is a complexstructure composed of the anterior naresand nasal cavities, the pharynx, larynx andthe extrathoracic trachea. The pharynxis typically considered in four zones— the nasopharynx, the velopharynx,the oropharynx and the hypopharynx(Figure 1). The nasopharynx extendsfrom the posterior aperture of the nasalcavity to the level of the hard palate.The velopharynx extends from thehorizontal plane of the hard palatecaudally to the tip of the uvula. Theoropharynx is defined anteriorly by thetongue and posteriorly and laterally bythe pharyngeal walls. It extends fromthe uvula to the base of the epiglottis. Portions of the upper airway are boundby muscular structures such as the softpalate, the tongue and the pharyngeal wall.The muscles that control these structuresstrongly influence the patency of theairway. To appreciate airway obstructionin patients with OSA, it is important tounderstand how this muscular controlmodulates the airway size. The soft palate

and the tongue form the anterior wall of thepharyngeal airway. The superior, middle andinferior constrictors make up the posteriorpharyngeal wall. The lateral pharyngealwalls are formed by several differentstructures, including the hyoglossus,styloglossus, stylohyoid, stylopharyngeus,palatopharyngeus, palatoglossus, thepharyngeal constrictors, adipose tissue and the palatine tonsils. In a passive state,without muscle activity, the cross-sectionaldimension of the airway is a function ofthe transmural pressure — the pressuredifferential between the intraluminalpressure and tissue pressure. A decrease inthe intraluminal pressure or an increase in the tissue pressure will narrow the airway.Mechanical influences on upper airway dimension include static factors,such as neck and jaw position, andgravity. For example, in a slightly openjaw, there is more room in the oral cavityfor the tongue, resulting in an increasein the size of the pharynx. However, asthe mandible moves further posteriorly upon opening, it causes the tongue andthe hyoid apparatus to move posteriorly,thereby narrowing the pharyngeal airway.

When the patient is in a supine position,gravitational forces on the tongue andsoft palate result in airway narrowing.Dynamic factors that influencepharyngeal airway patency includeupstream resistance in the nasal cavityand pharynx, tissue compliance andpharyngeal muscle activity. The anatomyof the nasal cavity is relatively complexand provides high resistance, yielding aturbulent airflow. This results in a morenegative nasopharyngeal intraluminalpressure. Likewise, high resistance withinthe nasopharynx/oropharynx due to anatomical constraints is associated witha more negative intraluminal pressure atsites caudal to these anatomic constraints.As a result of this upstream airwayresistance, the lumen of the pharyngealairway is narrowed during inspiration. The phasic activation of the skeletal muscles surrounding the airway helps to dilate the airway and stiffen the pharyngeal walls during inspiration. During wakefulness,

pharyngeal patency is maintained bycoordinated muscle control by thecentral nervous system. Decrease in themotor output to the pharyngeal musclesduring sleep results in decreased muscletone, narrowing of the airway lumenand an increase in airway resistance. Asa feedback mechanism, the increasingnegative pressure and rising carbon dioxidelevels stimulate the pharyngeal muscles to restore airway patency. However, inan anatomically aberrant airway, thesereflexes may not sufficiently compensatefor the reduced airway diameter andthe risk of airway collapse increases.

Evaluation of the Upper Airwayon CBCT Imaging

The extent of the nasopharyngealairway that is imaged in a maxillofacialCBCT scan depends on the imagingprotocol and field of view (FOV). Typically,the pharyngeal airway is not included inthe imaged volume of a small (limited)FOV scan, such as those taken to evaluateonly a small segment of the teeth and thesupporting dentoalveolus. In a mediumFOV encompassing the maxillary andmandibular dental arches, the velopharynxand oropharynx may be only partly visualized. In contrast, a full FOV CBCTscan, such as those acquired to assess thecraniofacial skeleton for orthodontic andorthognathic treatment planning, willencompass most, if not all, of the nasalcavity and pharyngeal airway. Irrespectiveof the primary indication for the CBCTscan, it is the dentist’s responsibility to evaluate the entire imaged volume, andthis includes a systematic assessment ofthe airway. Indeed, incidental airwayabnormalities are detected on CBCT scansin 21 percent to 52 percent of patients,underscoring the need for a careful analysisof the airway on these imaging exams.12,13,14

General Imaging Considerations

The CBCT scan depicts a staticsnapshot of the upper airway. It permitsassessment of anatomic and pathologicchanges that alter upper airway morphologyand to infer increased airway resistanceand potential obstruction or collapse ofthe airway. Importantly, these radiologicalfindings alone do not establish a diagnosis ofOSA. Rather, detection of these radiologicalabnormalities should prompt a morethorough evaluation of the patient’s history and symptoms of sleep-disordered breathing.As described above, the patency ofthe airway is strongly influenced by staticand dynamic factors. For example, theposition of the patient’s tongue duringscan acquisition may cause the pharyngealairway to appear dilated or narrowed.Similarly, if the patient were to swallowduring the scan acquisition, the soft palate would appear higher and juxtaposed againstthe posterior pharyngeal wall, therebyreducing the velopharyngeal airspace. Thus,interpretation of the airway dimensionsmust consider such modifying factors.Moreover, a consistent, repeatable imagingprotocol, depending on the diagnosticpurposes of the scan, such as swallowingbefore the scan is initiated or maintaininga closed intercuspal position, is advisable. Gravity plays an important role inmodifying airway dimension when thepatient is in the supine position. Tworecent studies showed that the positionin which the CT scan is acquired (supineversus standing/sitting) considerablyimpacts the airway morphology.15,16 Forexample, Camacho et al.16 showed totalvolume of the upper airway decreasedby approximately 33 percent and cross-sectionalarea measurements decreased 32percent to 76 percent when imaged in thesupine position. This is expected, giventhe gravitational forces on the tongueand soft palate that would be operationalin the supine position. Thus, airwaymorphology imaged with the patient inthe supine position is more reflective ofthe airway morphology during sleep.

Evaluation of the Nasal Cavity

The nasal cavity is the entranceto the upper airway and the first ofseveral anatomic regions to evaluate ina systematic airway analysis. Althoughnasal obstruction has been considered in the etiology of sleep-disorderedbreathing, the role of nasal resistancein the pathogenesis and severe duty ofOSA has been relatively understudied.Nevertheless, there is rationale to evaluate nasal obstruction as a potentialcontributor to OSA. First, the nasalpassage is a major contributor to upperairway resistance.17Second, nasalobstruction leads to oral breathing andan open mouth position, which in turnresults in a narrow hypopharyngeal space. Thus, it is important to evaluatethe anatomy of the nasal cavity.18The nasal septum, the nasalturbinates and the floor of the nasalcavity form the boundaries of thenasal air passage. The nasal septumis an osteocartilagenous structure inthe midsagittal plane and divides thenasal cavity into the right and leftcompartments (Figure 2). The septumis made up of a bony portion formed bythe perpendicular plate of the ethmoidbone and the vomer. These two laminarbones articulate anteriorly with theseptal cartilage. Bony protrusions fromthe lateral walls of the nasal cavityform the inferior, middle and superior nasal conchae. The bony conchaeare encompassed by a spongy mucousmembrane to form the nasal turbinates(Figure 2). The space between twoadjacent turbinates is the meatus, with the size of the meatus decreasingsuccessively from inferior to superior.The physiological process of the nasalmucosa (i.e., alternating congestionand decongestion of the large veinsin the nasal mucosa and subsequentenlargement or reduction of the mucosa,termed “nasal cycling”) contributes tofluctuations in nasal airflow betweenthe right and left nasal passages. Deviation of the nasal septum is arelatively common anatomic variation.However, depending on the extent of thedeviation, it may obstruct nasal airflowand increase nasal airway resistance(Figure 3). Similarly, hypertrophy ofthe nasal turbinates, distinct from thealternating fullness found in normal “nasalcycling,” is a common cause for nasalairway obstruction (Figure 4). The PhaseI of the Powell-Riley surgical protocolfor sleep-disordered breathing19 includessurgical correction of nasal septumdeviation and turbinate hypertrophy.Increased nasal resistance is known tonegatively impact treatment outcome withoral appliances for OSA management,underscoring the importance ofevaluating nasal anatomy in patientswho are candidates for this therapy.20

Evaluation of the Pharyngeal Airway

The entire length of the pharyngealairway encompassed in the imagedvolume, including the nasopharynx,velopharynx, oropharynx and laryngopharynx, should be evaluatedsystematically for patency and symmetry.This will enable detection of anatomicalvariations and pathological changesthat compromise the airway.Several studies have demonstrated that the cross-sectional area of the pharyngealairway is smaller in OSA patientscompared with normal subjects.21,22,23,24,25 Avisual assessment of the airspace is oftenadequate to provide an assessment of itsnormalcy. However, when the dimensionsappear narrow (Figures 5 and 6), linearand cross-sectional area measurementsmust be made. Many CBCT softwareprograms allow the user to segment theairway and determine the cross-sectionalarea, anteroposterior (AP) and lateraldimensions, at the narrowest site in theairway. Ogawa et al.24 showed that theminimum cross-sectional area in normalsubjects was significantly higher than thatin OSA patients (146.9, 111.7 mm2versus 45.8 ) 17.5 mm2, respectively).Additionally, the minimal AP and lateraldimensions from normal subjects werealso higher (7.8) 3.3 mm versus 4.6) 1.2 mm for the AP dimensions and16.2) 6.8 mm versus 11.6) 4.5 mmfor lateral dimensions). Thus, there isstrong evidence that airway dimensionsare reduced in OSA patients. However,the extent of narrowing does not seemto correlate with the OSA severity. It is important to note that there is anoverlap in the ranges of airway dimensionsbetween normal and OSA patients.Thus, airway dimensions alone do notserve as a diagnostic characteristic tocategorize patients as normal or OSA.

Several common pathologicalconditions compromise airwaydimension. A common cause isenlargement of the pharyngeal andpalatine tonsils. The pharyngeal tonsil(adenoids) is a region of lymphatic tissuelocated at the posterior nasopharyngealboundary. The palatine tonsils arelymphoid masses located on the lateralaspect of the oropharynx. Enlargementof the adenoids and/or palatine tonsilsis the most common cause of OSAin children (Figures 7 and 8). For these patients, surgical treatment withtonsillectomy and/or adenoidectomy isthe recommended first-line of treatmentand resolves OSA in 82 percent of thispatient population. 26, 27 In addition,neoplasms in the nasopharynx andoropharynx can also grow into the airwayand cause obstruction (Figure 9).28

Evaluation of Craniofacial Morphology

Certain craniofacial morphologicalcharacteristics have been shown tobe associated with an increased riskfor OSA, especially in children. In arecent meta-analysis, Flores-Mir et al.29 evaluated nine studies and identified themost commonly reported findings acrossthe studies. These included a narrowmaxillary dental arch with a high palatalvault, an obtuse gonial angle, posterior-inferiorrotation of the mandible, aretruded chin, tendency toward anterioropen bite and lip incompetence as wellas smaller nasopharyngeal airway spaces.While many of these features wereinitially described using cephalometricradiography, their recognition onCBCT images is pertinent. Likely, the3-D nature of CBCT will enhance therecognition of these various craniofacialfeatures. Children with dental andskeletal abnormalities are often imagedwith CBCT for orthodontic andorthognathic treatment planning. Inparticular, patients with craniofacialsyndromes are often imaged with CBCTfor treatment planning. The incidenceof OSA in this latter population ismarkedly high8 and thus, particularattention must be directed to the airwaywhen analyzing scans of these patients.Equally important, the potentialbeneficial or negative impacts ofsurgical and orthodontic interventionson the airway must be assessed.

Managing Incidental Findings

As described above, all CBCT scansacquired, irrespective of the primarydiagnostic task,must be analysed systematically for other abnormalities,including those in the airway. Asrequired, dentists should seek theexpertise of an oral and maxillofacialradiologist to provide a thoroughinterpretation of the entire scan volume.This is particularly important given that incidental abnormalities of the airwayhave been detected in 21 percent to52 percent of CBCT scans.12,13,14 Equallyimportant is the dentist’s role in managingpatients with incidental findings that areassociated with an increased risk for OSA.As an initial step, the dentist shouldquery the patient for a history of snoringand daytime sleepiness. The medical

history should be evaluated, risk factors including congestive heart failure, refractoryhypertension, type II diabetes, stroke andatrial fibrillation. Following this initialassessment, a more comprehensive historyand physical examination for sleep-relateddisordered breathing may be required. Asappropriate, dentists who do not have theexpertise in OSA management shouldrefer the patient to a specialist in sleepmedicine or dental sleep medicine forfurther evaluation and possible therapy.The American Academy ofSleep Medicine has developedclinical guidelines for evaluation and management of OSA.30 This includes acomprehensive sleep history, evaluationof risk factors and co-morbidities anda thorough physical examination toassess the respiratory, cardiovascularand neurological systems.30

CBCT Evaluation of the OSA Patient

Dentists who treat obstructive sleepapnea with oral appliances may prescribea CBCT scan to specifically evaluate theupper airway. The general principles ofairway analysis described above would alsoapply to evaluation of the CBCT scansin these patients. Specifically, the CBCTexamination may provide clues to thepotential cause for airway narrowing, suchas adenotonsillar hypertrophy, mandibularretrognathia, etc. Indeed, anatomicalvariations and pathological aberrations,such as conchae bullosa, hypertrophicnasal turbinates, enlarged tonsils,elongated or posteriorly placed soft palate,reduced airway dimensions and enlarged

tongue, have been detected as incidentalfindings in patients with OSA.31 Inaddition, CBCT provides additionalinformation that may contribute totreatment planning and prognosis.

Evaluation of Prognostic Factors

Oral appliances (OA), prescribed anddelivered by dentists, are often used inthe treatment of mild-to-moderate OSA.Although oral appliances may result inoutstanding quality of life improvementin the individual patient, the overallsuccess rate for controlling OSA with the use of OA is approximately 52 percent.32Such an outcome statistic underscoresthe need to better plan the appropriateOSA therapy approach for the specificpatient. Currently, we do not have afull understanding of the various factorsthat contribute to OA success/failure.However, some studies have demonstratedthat specific features are associated withOA treatment outcome. For example,increased nasal airway resistancenegatively impacts treatment outcome.20Thus, the CBCT scan should be evaluatedfor anatomical aberrations such as adeviated nasal septum and pathologicalalterations such as turbinate hypertrophy.Shenet al.33 evaluated predictors of OAoutcomes and found that patients witha minimal retroglossal area, mandibularretrognathia and a shorter anterior facialheight responded better to OA therapy.A shorter soft palate and an increasedcranial base angulation were predictive oforal appliance treatment success.34 CBCTimaging often reflects changes in airwaymorphology with oral appliance therapy(Figure 9). However, no quantitativerecommendations for the use of specificprognostic factors in appropriate treatmentplanning of OSA therapy exist to date.

It is also important to note thatalthough a radiographic abnormalitymay be associated with OSA patients,due to the complex and dynamic natureof the upper airway, treatment of this finding may not directly improve OSAsymptomatology. Previous studies haveshown that the hyoid bone in patientswith OSA is displaced in a posterior andcaudal direction. It has been speculatedthat inferior displacement of the hyoidbone will angulate and mechanically disadvantage the geniohyoid muscle. Chiet al.35 showed that inferior displacementof the hyoid bone is a function of a larger tongue volume. Surgical procedureshave been developed to normalize thehyoid position. However, the surgicalprocedures will not address the primarycause of a larger tongue, and thus, may notbe adequate to effectively manage OSA.CBCT scans can also be taken toevaluate treatment-induced changes,for example with an OA (Figure 10)or by surgical correction. However,clinicians must be aware that an increase in airway size is not a reliable indicatorof treatment success. This should beevaluated by symptom resolution and animprovement in the AHI and oxygensaturation as determined by PSG.

Dynamic Modeling of the UpperAirway

Although CBCT imaging providesexcellent visualization of the staticairway morphology, it does not provideany direct information on airflowand airway resistance. However, theairway geometry imaged on CBCTimaging can be used to computationallymodel these dynamic aspects and thusprovide functional information. Suchdynamic modeling has importantclinical applications — purelygeometric factors such as changes inthe airway cross-sectional area do notpredict response to OA therapy andthere is a need to develop patientspecificdynamic assays of airflow.Computational fluid dynamics (CFD) flow parameters in a specified geometryand provides a quantitative andqualitative description of regional flowand pressure in a particular structure.Computational modeling to studybiological phenomena should be anadequate representation of the biologicalsituation. Only a few studies have appliedCFD to characterize flow behaviors of theupper airway and to analyze changes inthis flow with therapeutic intervention forOSA management.36,37,38,39 Some studies have attemptedto model such dynamic interactions in apatient-specific approach using fluidstructureinteractions (FSI).40,41,42 Althoughprocesses for CFD and FSI have separatelybeen established, their combination andapplication to airway analysis is notstraightforward.

Conclusions

CBCT imaging is being usedincreasingly for several differentdentomaxillofacial diagnostic andtreatment-planning tasks. Often, suchCBCT scans partially or fully encompassthe upper airway. Dentists must be familiarwith the normal anatomy of the airwayso that any incidental abnormalitiescan be recognized. A systematicevaluation of the various compartmentsof the upper airway is important torecognize anatomic and pathologicalterations. As appropriate, dentistsmust seek consultation with appropriatespecialists to confirm and, if needed,manage such findings. Technologicaladvances that combine CBCT imagingwith computational modeling of theairway have potential applications formanagement of patients with OSA.

REFRENCES
 
  1. Carlson JT, Hedner JA, Ejnell H, Peterson LE.High prevalence ofhypertension in sleepapnea patients independent of obesity.Am JRespirCrit Care Med 1994;150(1):72-7.
  2. Gami AS, Hodge DO, Herges RM, et al. Obstructive sleepapnea, obesity and the risk of incident atrial fibrillation. J Am CollCardiol2007;49(5):565-71.

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