Annals ofOfohgy. Rhinatoxy <( Ijin-nnolofty 117(5):327-334.O 2008 Annab Publishing Company. All righls reserved.

Optical Coherence Tomography of the Newborn Airway

James M. Ridgway, MD; Jianping Su, MS; Ryan Wright; Shuguang Guo, PhD;David C. Kim, MD; Roberto Barretto, MD; Gurpreet Ahuja, MD; Ali Sepehr, MD;Jorge Perez; Jack H. Sills, MD; Zhongping Chen, PhD; Brian J. R Wong, MD, PhD

Objectives: Acquired subglottic stenosis in a newborn is often associated with prolonged endotracheal intubation. Thiscondition is generally diagnosed during operative endoscopy after ainvay injury ha.s occurred. Unfortunately, endoscopyis unable lo characterize the submucosal changes observed in such airway injuries. Other modalities, such as magneticresonance imaging, computed tomography, and ultrasound, do not possess the necessary level of resolution to differen-tiate scar, neocartilage. and edema. Optical coherence tomography {OCT) is an imaging modality that produces high-resolution, cross-sectional images of living tissue (8 to 20 \xm). We examined the ability of ihis noninvasive technique tocharacterize the newborn airway in a prospective clinical trial.

Methods: Twelve newborn patients who required ventilatory support underwent OCT airway imaging. Comparativeanalysis of intubated and non-intubated states was performed.

Results: Imaging of the supraglottis. glottis, subglottis, and trachea was performed in 12 patients, revealing unique tissuecharacteristics a.s related to turbidity, signal backscattering. and architecture. Multiple structures were identified, includ-ing the vocal folds, cricoid cartilage, trachea! rings, ducts, glands, and vessels.Conclusions: Optical coherence tomography clearly identifies in vivo tissue layers and regional architecture while of-fering detailed information concerning tissue microstructures. The diagnostic potential of this technology makes OCT apromising modality in the study and surveillance of the neonatal airway.Key Terms: imaging, newborn airway, optical coherence tomography, subglottic stenosis.

INTRODUCTIONLaryngeal stenosis of the newborn is described as

a narrowing of the supraglottic. glottic, or subglot-tic regions. The most common site of this airwaynarrowing is at the level of the subglottis. In a new-born patient, this condition ttiay pass undetected orpresent as a life-threatening and, at worst, a life-end-ing event. The ability to diagnose, treat, and evenprevent subglottic stenosis has been the hallmarkof medical advances in neonatal care, as well as theharbinger of continued controversy and debate.

The architecture of the newborn subglottis isunique, as the cricoid cartilage is the only circumfer-ential ring of the upper airway. This anatomic con-figuration makes the narrowest point of the newbornairway also its most uncompromising.'- Further,the tissues of the subglottis are delicate in nature.

are easily damaged, and rapidly develop edematouschanges. These circumstances, when taken togeth-er, significantly predispose the subglottis to inflatn-mation, scar formation, and stenosis in newborn pa-tients who require endotracheal intubation.

Direct laryngoscopy and bronchoscopy has re-mained the gold standard in the evaluation of new-boms in whom subglottic stenosis is suspected.^Unfortunately, this technique is limited to the char-acterization of the surface anatomy and does notoffer detailed analysis of the subepithellal tissues.During direct laryngoscopy and bronchoscopy, air-way trauma may be incurred with the removal of theendotracheal tube, the use of surgical endoscopes,or the (re)placement of a breathing tube if respi-ratory distress or airway disease is observed. Thisclitiical circumstance is often complicated, as the

I-nini the Deparlnieni oï Oto laryngology-Head and Neck Surgery (Ridgway, Barretlo. Ahuja. Sepehr. Wong), the Beckman Laser Insti-uilc (Ridgwiiy. Su. Wright. Guo. Sepehr. Perez. Chen. Wong), the Deparlment of Biomédical Engineering (Su. Guo. Chen, Wong), andihe Ücparimenl ol' Pediatrifs (Kim. Sills). tJniversiiy of California-Irvine. Irvine. California. This work was supported by Ihe NationaiInslitules ol' Health (DC (K)6()26. CA 91717. EB (K)29.1. RR 01192, MO 1 -RRÜ()827-28). the Flight Attendant Medical Research Institute(32456). the State of California Tobacco Related Disease Research Program ( 12RT-0113). the Air Force Office of Scientific Research(FA955(J-04-l-01til).and the Arnold and Mabel Beckman Foundation.Presented as a podium discussion at the meeting of the American Broncho-Esophagological Association, San Diego. California, April26-27, 2(K)7, Recipient of the Seymour R. Cohen Award.C'orre-spondence; Brian J. F. Wong. MD. PhD. or Zhongping Chen, PhD, Beckman Laser Institute, University of California-Irvine,1002 Health Seiences Rd, Irvine, CA 92612; e-mail, bjwong@uci.edu or z2chen@uci.edu.

327

328 Ridgway et al. Optical Coherence Tomography in Newborns

Fig 1. Photograpbs of optical coherence tomography (OCT) probe for newborns.

pulmonary, cardiac, and hypoxic thresholds in thenewborn population may postpone the evaluation ofthe airway because of limited tolerances to physi-ologic stress. In essence, the ultimate challenge inthe evaluation ofthe newborn airway is to minimizediagnostic trauma and physiologic stress while ac-curately characterizing the laryngeal tissues.

Optical coherence tomography (OCT) is an im-aging modality that utilizes non-ionizing coherentlight to produce high-resolution images of living tis-sues.-* The images are produced in a cross-sectionformat, similar to that of ultrasonography, but witha resolution of H) [im and a depth of nearly 2 mm.This high-resolution modality allows one to distin-guish the epithelium from the underlying tissue mi-crostructures on the basis of optical scattering, ab-sorption, and anisotropy with near-real-time framerates. Using OCT imaging, one can noninvasivelycharacterize living tissues beyond the current imag-ing capacities of magnetic resonance imaging, com-puted tomography, and ultrasound.^-^

The current investigation reviews OCT imagingof the newborn airway and its potential role in themanagement of intubated newborn patients. Theaims of this study were to apply OCT technologyin the characterization of tissue architecture, reviewimaging in intubated and non-intubated states, anddefine the feasibility of this modality in this givenpopulation. Briefly, we will discuss OCT image ac-quisition, interpretation, and operative instrumenta-tion, followed by a review of our series of newbornpatients. To the best of our knowledge, this is thefirst report of OCT imaging ofthe newborn airway.

METHODSPatient Population and Endoscopy. Optical co-

herence tomography imaging was performed on12 patients at the University of California-IrvineMedical Center under a protocol approved by theHuman Subjects Institutional Review Board at theUniversity of California-Irvine. The study subjects

were limited to newborn patients who required en-dotracheal intubation with mechanical re.spiratorysupport. While the patient.s were under general an-esthesia in the operating room or light sedation inthe newborn intensive care unit. OCT Imaging wasperformed with the use of a custom handheld probe.Multiple sites of the airway tract were imaged. En-doscopie photographs were only obtained in patientswho were undergoing surgical endoscopy.

OCT System and Instrumentation. The OCT sys-tem and instrumentation has been previously de-scribed and will be briefly reviewed.^-^ Near-in-frared light from a broadband light source (centralwavelength X = 1,310 nm: full width at half maxi-mum M = 80 nm; BBS 1310, AFC TechnologiesInc, Hull, Canada) enters a 2 x 2 fiberoptic coupler.In the reference arm, a rapid scanning optical delayline attains A-scan at 500 Hz without phase mod-ulation. The phase modulator generates 500-kHzphase modulation for heterodyne detection. Signalsbackscattered from the sample arm are obtainedby phase-resolved processing with the interferencefringes. The axial resolution of the system in tissueis approximately 7 ^m, and the lateral resolution ap-proaches 20 |im. The horizontal image window isset laterally from 2 to 6 mm in length, and detailedimages of tissue microstructure are tecorded up toa depth of i.6 mm. depending upon the turbidity ofthe media.

For imaging the newborn airway in vivo, a cus-tom flexible probe and a rigid OCT probe were de-signed to accommodate the specific anatomic con-siderations during endoscopy and the curvature ofthe endotracheal tube. The probes consist of a 900-[im single-mode fiber distally terminated hy a gradi-ent refractive index (GRIN) lens and a 0.5 mm rightangle prism (Fig 1). The GRIN lens is 0.7 mm indiameter and works to focus light. Mounting of theprism and GRIN lens is accomplished with an op-tics-grade, low-viscosity, wicking ultraviolet glue.Scanning is achieved by linearly translating the op-

Ridgway et al. Optical Coherence Tomography in Newborns 329

Fig 2. ' ;m^ L'liJoliaijlieal ÜCT inuiying with handheld|)robe in neonatal intensive care unit.

tical fiber along the long axis by means of a mo-torized piezo-driven stage (model 663.4pr. PI Line,Tustin, California). The optical fiber, the optical ele-ments, and a supportive stainless steel tube are en-closed within a transparent plastic tube (2.0()0-[¿mouter diameter. 200-[im thickness, fluorinated ethyl-enepropylene material). Two different models of thesteei tube were utilized for this project. One stain-less tube was entirely rigid lor use during surgicalendoscopy. and a flexible vertebrated steel tube wasused for imaging across the endotracheal tube (Fig2). For orienting the user, colored markings weremade along the sides of the optical fiber with lightexiting along the opposite side of the fiber tip. Thissystem design remained constant for all subjectsstudied.

OCT Imaging. Images were obtained either at thetime of surgical endoscopy. by placing the probethrough a laryngoscope with the patient in laryngealsuspension, or in the neonatal intensive care unit, byplacing the imaging probe through a circuit adap-tor into the endotracheai tube. Image productionwas directed by the orientation of light propagationas it exited the tip of the OCT fiber and was con-

BAStC NEWBORN PARAMETERS AT TIME OFOPTICAL COHERENCE TOMOGRAPHY IMAGING

ChronologicalGestational Agef at Weight at Duration of

Patient Age* Time of at Time of IntubationNo. (wk) Imaging (d) Imaging (g) (h)

123456789

101112

Average

404124273226402525253733

31.3

62761218

132

0.540.5

0.4626

0.2513.8

3.3733.2381,336t,0431.762

6573,704

586800610

3.6101.939

1.888.2*Time elapsed between first day of last mcnslmal perioddelivery.

tTime elapsed since birth.

1.50

1.46450414431224131211

6006

257.6and day of

firmed before imaging with the use of a referenceinfrared sensor card (Newport Corp. Irvine. Califor-nia). During surgical endoscopy. the tip of the ÜCTprobe was placed in near-contact to the region ofinterest with the image visualized on a bedside sat-ellite cart monitor. Trans-endotracheal imaging wasperformed with direct approximation of the flexibleOCT probe to the inner surface of the endotrachealtube with image visualization made from an OCTmonitor tower. The OCT imaging was systematical-ly performed throughout the airway along the ante-rior, right lateral, posterior, and left lateral positionswith the probe drawn from the distal to the proxi-mal airway. The OCT video files were subsequentlytransferred to a database in which still digital imageswere captured and catalogued. The image orienta-tion remained constant, with left and right sides ofthe images representing the proximal and distal re-gions of the newborn airway. The superior and infe-rior aspects of the image, respectively, illustrate the

Fij; X OCT JFTiagc of newborn trachea. E — epithelium; B — ba.seinent membrane; L — latiiina propria; T — trachea! cartilage;bar - 500 ^m.

330 Ridgway et al. Optical Coherence Tomography in Newhorns

Fig 4. Trans-endotracheal OCT image of newborn trachea. E — epithelium: B— trachea! cartilage; bar — 5Ü0 ]im.

basement membrane; L ~ lamina propria; T

surface mucosa and the inner microstructures of theregions of interest.

OCT ¡mage Analysis. Images from multiple sitesalong the aerodigestive tract were obtained. The im-ages were then sorted into 4 anatomic groups: 1)trachea. 2) subglottis, 3) glottis, and 4) supraglottis.Further comparisons were made between direct im-aging of the newborn airway and images obtainedby OCT imaging through the endotracheal tube. Areview of basic newborn parameters at the time ofOCT imaging is presented in tbe Table.

RESULTSTwelve newborn subjects ranging from 24 to 41

weeks of gestational age participated in an OCTstudy of the airway with emphasis on intubated andnon-intubated states. Cross-sectional images werecollected from multiple sites during OCT imaging.All patients underwent imaging of the supraglottic.glottic, subglottic and trachéal regions. Imaging wasperformed in 4 quadrants that were equally spacedand aligned with anterior, posterior, right lateral,and left lateral positions. Database images were re-viewed, categorized, and partitioned on the basis ofanatomic structures. Attention was also given to im-ages that demonstrated characteristics not common-ly observed in other subjects or at other sites.

The following images represent an analysis of

tissues in which epithelium, basement membrane,lamina propria, and other regional microstructureswere clearly identified in normal tissues by OCT(group 1). Each OCT image represents a specificregion of interest, as well as intubated and non-in-tubated states. Figure 3 displays a classic OCT im-age of the trachea with clear delineation between theepithelium and the underlying lamina propria alongthe basement membrane interface. Differences ingrayscale intensity are directly related to the degreeof the optical signal that is backscattered (reflected)by a given medium. Tissues with a relatively highturbidity create greater backscatter signals (eg, car-tilage) and are represented in a grayscale distribu-tion as a color closer to white. Tissues with a lowoptical scattering coefficient are represented by adarker appearance (eg, water). Such differences al-low the viewer to discern an image on the basis ofthe variable optical densities of a given tissue. Asseen in Fig 3, the optical density of the epitheliumis less than that of the lamina propria or underlyingtrachéal cartilage. In Fig 4. we see a minor decreasein overall signal intensity, but we are readily able todiscern the epithelium, lamina propria, and trachea!cartilages. This image was produced by trans-endo-tracheal OCT imaging in which the OCT fiber wasinserted into the endotracheal tube and the opticalsignal was transmitted through the tube and into thesurrounding tissues. One may note the difference

Fig 5. OCT image of newintrn LIÍCDÍII cai tikiye. E — epithelium; B — hasemeril riic-nibrane; L — lamina propria; C — cricoidcartilage; G — glandular structures; bar — 500 |j.m.

v c! al. Optical Cdhcrencc Tomographv in Newhorns 331

Fig 6. OCT image of newborn subglottis. E — epithelium; B — basement membrane; L — lamina propria; C — cricoid carti-lage; G — glandular structures; VF — vocal fold; bar — 500 (ini.

in the size of the trachea! cartilages between Figs 3and 4. These findings represent the 15-week devel-opmental difference between these two patients.

In group 2, the cricoid cartilage is well delineatedagainst the overlying tissues and glands (Fig 5). Theloss of signal beyond the cricoid cartilage denotesits optical density in comparison to the surroundingtissues. The heterogeneity ot the optical signal with-in the lamina propria represents the distribution ofseromucinous glands (darker regions). On the rightside of the image is a hysteresis artifact from theOCT translational stage. The boundaries of the re-maining subglottis are observed in Fig 6. Along theleft side of the image, the homogeneous signal ofthe vocal fold is a considerable contrast to the morecomplex signal of the distal subglottis observed onthe right. In the intubated newborn (Fig 7). the sub-glottis is once again imaged through the substanceof the endotracheal tube. Little information is lost,as the epithelium, lamina propria, glandular, and cri-coid boundaries are well visualized.

Tissues devoid of microstructural features, suchas glands or ducts, are relatively homogeneous inOCT imaging and can represent the vocal fold, gran-ulation tissue, or even scar. The last two are oftendevoid of the normal interface of the epithelium andunderlying lamina propria. This is best representedby Fig 8 from group 3, in which OCT imaging of

a normal vocal fold is resolved. As imaging is per-formed in the more proximal airway (group 4). onecan see the apposition of the glandular false vocalfold and the vocal fold with the partition of the col-lapsed ventricle in between (Fig 9).

Figure 10 represents the patient in this study whowas intubated for a period of 61 days at the time ofOCT imaging. In this image of the subglottis, onecan appreciate the two sites of clustered dark re-gions. As described in previous publications.'^'" flu-ids with similar density to that of water allow forgreater signal propagation into tissues due to limitedbackscattering. The result is greater signal penetra-tion and ultimately greater image clarity at depthsthat would not otherwise be observed in a more tur-bid medium. In contrast, blood absorbs the OCT sig-nal and creates a shadow effect in which underlyingstructures are poorly observed. Taken together, theseregions likely represent occluded glandular ducts,inflammatory changes, or recent trauma. There isalso similar optical density of the epithelium andlamina propria in these regions as well.

In the circumstance of poor image quality alto-gether, one must consider the possibility that oth-er components in the newborn airway may absorbor backscatter the OCT signal. The image in Fig ! Irepresents a fluid that was lining the outside of theendotracheal tube that nearly absorbed the entire

Fig 7. Trans-endotracheal OCT image of newborn subglottis. E — epithelium; B — basement membrane; L — lamina propria;C — cricoid cartilage; G — glandular structures; bar — 5(M) |xm.

332 Ridgway er ut, Optical Coherence Tomography in Newhonis

Fig 8. OCT image of newborn glottis. E — epithelium; B — basement membrane; L — lamina propria; VF — vocal fold; bar- 500 Mm.

Optical signal. On further evaluation ofthe patient'shistory, the infant was noted to have frank reflux ob-served in the morning and was started on antirefluxtherapy before OCT imaging.

DISCUSSIONNarrowing ofthe subglottic airway can represent

a congenital, acquired, or combined process. Con-genital stenosis implies that the narrowing ofthe la-ryngeal apparatus is a preexisting condition not cre-ated by acts of medical intervention or therapy. Of-ten this form of narrowing is associated with othermalformations or syndromes involving the head andneck. However, congenital narrowing ofthe airwaymay predispose a newborn to the development ofsubglottic stenosis if airway instrumentation or in-tubation is required. In the circumstance of acquiredsubglottic stenosis, Iaryngeal injury is often relat-ed to intubation and/or other medical interventionsthat can lead to soft tissue trauma and inflammation.This form of stenosis is suspected to represent themajority (95%) of clinical cases observed and hasdefined our focus of investigation. "- ^

In this study we present our experience with 12newborn patients who underwent OCT imaging ofthe airway. With each patient studied, OCT imagingwas able to resolve surface epithelium, tbe underly-ing lamina propria, and the interface ofthe ba.sementmembrane in all tissues of the laryngeal airway. In

the majority of patients imaged, we were able to vi-sualize the interface ofthe supraglottic, glottic, sub-glottic, and trachea! regions. The characterization ofthe newborn airway is of exceptional value in theneonatal setting, as operative endoscopy does notpossess the ability to view into tissues and magneticresonance imaging, computed tomography, and ul-trasonography do not possess the spatial resolutionnecessary to evaluate processes at the microscopiclevel. Additionally, operative endoscopy may needto be delayed in those patients whose conditions aretoo unstable and pose too much of an operative riskfor them to be brought from the neonatal intensivecare unit to the operating room for evaluation. Theability to noninvasively image the newborn airwaywith a high-resolution imaging modality would sig-niflcantly aid the pédiatrie otolaryngologist and peri-natologist in the care of a newborn who requireslong-term intubation.

Optical coherence tomography is a noninvasivetechnology that does not 1) produce ionizing radia-tion, 2) require patient extubation, 3) add physio-logic stress in a mechanically ventilated patient, or4) signiflcantly contribute to the risk of subglotticstenosis. In this current application, OCT was con-ducted with near-real-time image and video produc-tion with associated live-feed audio. This technoi-ogy has been well established in multiple fields oflaboratory and medicine research and provides the

Fig 9. Trans-endotrachcal OCT image of newborn false vocal fold (FF) and true vocal fold (VF). E — epithcliuin; B — base-ment membrane; L — lamina propria; G — glandular structures; V — ventricle; bar — 5(K) ^m.

Ridgway et al. Optical Coherence Tomography in Newborns 333

Fig 10. TraiLs-eiidotiuchcal ÜCT image of .subglotlis in prolonged intLibiition. E — epithelium; B — basemcnl niembriine; L— lamina propria; F — fluid; bar — 500 (im.

ability to microscopically view tissues without thelimitations, complications, and artifacts inherent incurrent operative techniques. It is important to reit-erate that all trans-endotracheal imaging performedin this study was conducted from within the con-fines of the endolracheal tube. The imaging fiber,with its associated housing, did not exceed 2 mm indiamcler. As a comparison, the diameter of the OCTprobe is less than that ofthe standard newborn endo-tracheal suction catheter used in daily maintenanceand hygiene of the inlubated airway.

Cunentty. multiple clinical inve.stigations are un-der way in which OCT imaging technology is beingapplied to characterize various tissue and diseasestates. In the field of ophthalmology. OCT imaginghas become an invaluable tool with current clinicalapplications in the imaging of macular edema, cho-roidal neovascularization. and glaucomatous chang-es. Other medical fields currently investigating OCTimaging include cardiology, gastroenterology, hepa-tology. pulmonology. and urology.''-'^ ' ' Investiga-tive studies of OCT technology in the field of otolar-yngology have also led to various potential applica-tions of this imaging modality.'^'''"'^"-"

This study represents the first efforts to charac-terize the newborn airway by use of OCT imagingtechnology. Correlation of OCT images in intubatedand non-intubated patients revealed only minor re-duction in the optical signal while continuing to re-

solve the various tissue layers and microstructuresofthe laryngotracheal apparatus. Studies of variousintubation timelines further revealed tissue changesthat may not be otherwise appreciated or revealedwith current techniques that require the removal ofthe endotracheal tube.

There are a number of limitations and challengesin the study presented. Ofthe 12 patients imaged,only I patient was free of prior intubation trauma orairway assistance. The limited numberof patients inthis study also prevented us from drawing any diag-nostic conclusions beyond the imaging capabilitiesof OCT technology. However, such difficulties areinherent in a pilot study and create a mandate forfurther investigation and discussion of this topic. Wehave also discovered a number of challenges whenapplying this technology, each of which can com-promise image quality. T"here is a learning curve, aswith many operative techniques, in which an indi-vidual and a team are to become accustomed to atechnique or procedure. The surgeon must coordi-nate the positioning ofthe OCT probe on the basis ofknown anatomy and image reference, much like thecardiologist who performs ultrasound in the evalua-tion ofthe heart. It is important lo note that the probeposition must be adjusted to create the optima! im-age for future analysis and that such actions requirea working knowledge of image interpretation.

Although the incidence of subglottic stenosis has

Fig II. frans-endoiracheal ÜCT image ot" fluid lining ouLside of endotracheal lube. ET — outer rim (black) of endoiraeheiiltube; F — fluid; SG — subglottic tissue; bar — 500 \in\.

334 Ridgway et al. Optical Coherence Tomography in Newborns

declined considerably over the past three decades,the ability to perform in vivo tissue imaging with anoninvasive. high-resolution modality could signifi-cantly alter the management of the newborn airway.With the capability to perform studies at or near vid-eo rates, one could easily complete initial and week-ly evaluations of high-risk newborns who requirelong-term ventilator assistance. Of important note isthe relatively recent application of this modality inthe head and neck with rapid improvements in im-age resolution, speed of image production, and evo-lution of clinical instrumentation.

Optical coherence tomography is a novel imag-ing modality that allows for noninvasive imaging ofthe newborn airway in intubated and non-intubatedstates. With its high-resolution capabilities, OCT isable to resolve the tissues of the ititubated newbornairway without creating physiologic stress or induc-ing soft tissue injury. These findings, although pre-liminary, have reaffirmed our clinical investigationof this promising modality. To this end. we will con-tinue to develop our experience in the newborn pop-ulation, as well as advance our understanding of thepotential clinical applications of OCT.

Acknowledgments: The authors thank master machinists Rudolph Limburg and Steve Knislcy for assistance with coiistruclion of Iheinstrumentation. We thank the nurses and respiratory therapist of the UC Irvine Neonatal Intensive Care Unil for their et'torts. as wellas Aya Yamamoto. RN. for her help and patience in the operating room. The US Governmenl is authorized to reproduce and distributereprints for Governmental purposes notwithstanding any copyright notation. The views and conclusions contained herein are those ofthe authors and should not be interpreted as necessarily representing the official policies or endorsements, either expressed or implied.of the Air Force Research Laboratory or the tJS Government.

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