Skip to main content
NCBI home page
NIHPA Author Manuscripts logoLink to NIHPA Author Manuscripts
. Author manuscript; available in PMC: 2022 Oct 17.
Published in final edited form as: Laryngoscope. 2021 Jan 5;131(6):E1971–E1979. doi: 10.1002/lary.29363

Quantitative Evaluation of Subglottic Stenosis using Ultrashort Echo Time MRI in a Rabbit Model

Deep B Gandhi 1,3, Andrew Rice 1,6, Chamindu C Gunatilaka 1,7, Nara S Higano 1,2, Robert J Fleck 1,3, Alessandro de Alarcon 4, Catherine K Hart 4, I C Kuo 4, Raouf S Amin 2,5, Jason Woods 1,2,5, Erik B Hysinger 2,5, Alister J Bates 1,2,5
PMCID: PMC9575155  NIHMSID: NIHMS1791273  PMID: 33399240

Abstract

Objectives:

To assess the ability of ultra-short echo time (UTE)-MRI to detect subglottic stenosis (SGS) and evaluate response to balloon dilation. To correlate measurements from UTE-MRI with endotracheal-tube (ETT)-sizing and to investigate whether SGS causes change in airway dynamics.

Methods:

Eight New-Zealand white rabbit airways were used as they approximate neonatal airway size. The airways were measured using ETT-sizing and 3D UTE-MRI at baseline, two weeks post-cauterization induced SGS injury, and post-balloon dilation treatment. Airway size was determined by ETT-sizing that permitted an air leak at 20 cm H2O. Static and cine UTE-MR images were acquired to determine airway anatomy and motion. Airways were segmented from MR images, and cross-sectional area (CSA), major and minor diameters (Dmajor and Dminor), and eccentricity (diameter ratio) were measured.

Results:

Post-injury CSA at the SGS was significantly reduced (mean 38%) compared to baseline (p=0.003). ETT-sizing correlated significantly with MRI-measured CSA at the SGS location at baseline and post-injury (r=0.89; p<0.001). Outer diameter from ETT-sizing correlated significantly with diameters from MRI at the SGS location (Dmajor: r=0.88; p<0.005; Dminor: r=0.79; p<0.005). There was no significant difference in the mean CSA of the trachea between end-expiration and end-inspiration at any timepoint (all p>0.05). Eccentricity of the upper trachea increased significantly post-balloon dilation (p<0.05).

Conclusion:

UTE-MRI successfully detected SGS and treatment response in the rabbit model, with good correlation to ETT-sizing. Balloon dilation increased CSA of the SGS, but not to baseline values. SGS did not alter dynamic motion for the trachea in this rabbit model; however, tracheas were significantly eccentric post-balloon dilation. UTE-MRI can detect SGS without sedation or ionizing radiation and may be a non-invasive alternative to ETT-sizing.

Keywords: Subglottic Stenosis, UTE-MRI, ETT-sizing, Balloon Dilation Treatment, Neonatal Subglottic Stenosis

INTRODUCTION:

Subglottic stenosis (SGS) is the narrowing of the subglottic lumen, typically from the inferior margin of the vocal cords to the lower border of the cricoid cartilage. SGS can be either congenital or acquired, however 95% of the neonatal SGS cases are acquired1 and iatrogenic in nature of origin. The most common cause of SGS is the injury resulting from frequent and prolonged endotracheal intubation causing edema, ulceration and necrosis of subglottic structure and ultimately leading to the development of SGS.2,3 SGS is a significant problem in neonates as it can increase resistance to the airflow and respiratory work.

The current clinical gold standard for diagnosis of SGS involves bronchoscopy with endotracheal tube (ETT)-sizing to determine the degree of narrowing based on Myer-Cotton scale.4,5 However, bronchoscopy is invasive and requires administration of general anesthesia.5,6 Neonates diagnosed with SGS are treated with tracheostomy or prolonged intubation in intensive care units due to the need for mechanical ventilatory support which makes management of neonates diagnosed with SGS very significant.2,7

Previous studies have used Computed Tomography (CT) and Optical Coherence Tomography (OCT) as non-invasive imaging methods to detect and monitor SGS.8–14 While CT has advantages in terms of high image resolution, its use in diagnosis and serial monitoring of SGS is limited due to the risks of ionizing radiation exposure and sedation in neonates. Long Range OCT (LR-OCT) has also been used to evaluate SGS. Advantages of using LR-OCT include the micron-level resolution of images, rapid scan times, airway wall thickness measurements to observe progressive pathologies, and observation of micro-anatomy.12–14 However, LR-OCT systems are not commonly found in hospitals and require expertise to set up.

A potential alternative to the conventional SGS diagnostic methods is ultrashort echo time magnetic resonance imaging (UTE-MRI), which can be performed free breathing in patients without requiring sedation or ionizing radiation15–22; as such, this technique is particularly appropriate for neonates. UTE-MRI has correlated well for dynamic airway lesions like tracheomalacia.21,23 Consequently, UTE-MRI has the potential to assess SGS abnormalities, monitor response to treatments, and provide non-invasive longitudinal follow-up for patients with SGS.

Various conservative and surgical procedures have been employed to treat SGS. Among those, balloon dilation procedure has been demonstrated to be safe and effective in treating SGS in children and reduces the need for open laryngeal surgery by 70–80%.24–28

Dynamic collapse of the trachea depends on intrinsic properties of the trachea and pressure applied across the airway wall. Previous studies have observed dynamic airway collapse in subjects with tracheal and bronchial stenoses.29 Since SGS increases resistance to airflow and pressure applied to the airway wall, SGS has the potential to alter airway dynamics of the trachea. However, none of the studies have investigated the effect of SGS to induce dynamic airway collapse.

Therefore, the goals of this study were: 1. To determine if SGS can be detected non-invasively in a rabbit model using UTE-MRI; 2. To evaluate whether UTE- MRI is sufficiently sensitive to evaluate treatment response following balloon dilation; and 3. To correlate the size of the airway lumen in SGS measured via UTE-MRI results with clinical ETT-sizing measurements; and 4. To determine if there are any changes in tracheal dynamics due to SGS during normal tidal breathing

This study uses an adult rabbit model to mimic the neonatal airway in an in-vivo setting. New Zealand white rabbits have been used as an animal model in previous studies involving surgical procedures of the larynx and the trachea.30 Since rabbit size and mass closely resemble that of three to nine-month old human infant,30 they were determined to be an optimal model for animal imaging.

MATERIALS AND METHODS:

2.1. Study Subjects

All animal care and procedures in this study were approved by the Institutional Animal Care and Use Committee at our institution. The study used eight adult New-Zealand White rabbits with a mean weight of 3.66 kg (range: 3.2 – 4.2 kg). All animals underwent ETT-sizing and UTE-MRI scan at 3 different time-points, as shown in Figure 1. Each of the procedures shown in Figure 1 are described in detail below.

Figure 1.

Figure 1.

Open in a new tab

Timeline of experimental procedures in which all the rabbits underwent ETT-sizing and UTE-MRI scan at each of the three different timepoints: baseline, two weeks post injury and post balloon dilation treatment. Time-points 2 and 3 occurred on the same day. Red arrows indicate the time taken between the procedures (30 mins to 2 hours).

2.2. Assessment of Subglottic Stenosis using ETT-sizing

2.2.1. ETT-sizing Procedure

All rabbits were administered with general anesthesia and their larynx was assessed using a laryngoscope to anesthetize the vocal folds. The airway size of subglottic region was then determined using ETT-sizing endoscopically by an ENT surgeon. ETT with the smallest diameter that permitted an air leak at 20 cm H20 was accepted as the airway size of the subglottic lumen. This procedure was performed at each of the 3 different timepoints to determine the airway cross-sectional area (CSA) from the outer diameter (OD) of the ETT as shown in Figure 1.

2.2.2. Induction of subglottic stenosis

Subglottic stenosis was artificially induced by cauterization of 75% of the circumference of the posterior subglottic region followed by 4-hour intubation carried out using a 3.5 mm ETT.31 Intubation of the rabbits after cauterization was performed to prevent acute airway collapse at sub-glottis and to exacerbate development of stenoses.

2.2.3. Balloon dilation to treat subglottic stenosis

Balloon dilation procedure was performed to treat SGS. This procedure involved inserting a balloon with 8 mm in diameter into the site of stenosis and inflating it for 30 seconds with a pressure of 17 atmospheres.

2.3. Non-invasive Assessment of Subglottic Stenosis using MRI

2.3.1. MRI Acquisition

MR images from the rabbits at all three timepoints were acquired on a preclinical 1.5T neonatal-sized scanner, originally an orthopedic scanner hardware (ONI Medical Systems, Wilmington, MA) modified to work on GE healthcare software.32,33 A three-dimensional radial UTE MRI sequence adapted for neonatal subjects was acquired.15,22 The scanning parameters used were: 3D resolution (x, y, z = 0.7031 mm), repetition time = ~5 ms, echo time = ~215 μs, flip angle = 5°, field of view = 180 mm, matrix size = 256 × 256 × 256, number of radial projections = ~130,000 and total scan time = ~12 minutes.

2.3.2. Retrospective respiratory gating of MRI

Multiple images were reconstructed retrospectively from the UTE MR raw data via retrospective respiratory gating. Each gated image was reconstructed from k0 data acquired at a specific phase of tidal breathing over a course of the UTE scan, as described previously.15–18,20–23,34 In this study, two sets of images were generated:- 1. Ungated rabbit images reconstructed from data acquired throughout the entirety of the breathing cycle, and 2. Gated rabbit images showing the anatomy at end-inspiration and end-expiration.

2.3.3. MRI-based geometric airway analysis

Rabbit airways were semi-automatically segmented from the 3D UTE-MR images using user-guided active contour segmentation in ITK-SNAP35 (3.8.0; Penn Image Computing and Science Laboratory; www.itksnap.org). A consistent threshold calculated from the mean of the image intensity of the surrounding soft tissues and the airway lumen was used for consistent segmentation for each rabbit at every time-point. Virtual 3D airway models were generated from these segmentations, and a series of cross-sectional disks were obtained along the length of the airway model (as shown in Figure 2A) using previously published methods.17,18,23

Figure 2.

Figure 2.

Open in a new tab

(A) 3D airway volume rendering from the UTE-MR images of a rabbit at the post-injury timepoint (left) with a virtual airway surface showing SGS, centerline through the surface and cross-sectional slices through the airway surface (right).(B) A sagittal section of the 3D UTE-MR image with the airway segmented in red (left) along with examples of major and minor airway diameters and eccentricity index calculation from airway surface slices (right).

Parameters such as airway cross-sectional area (CSA) and major and minor diameters (Dmajor and Dminor) at the site of SGS and along the length of the trachea were calculated from the luminal disks. Dmajor is the length of the largest possible line that can be drawn through the centroid of the disks, while Dminor is length of the line perpendicular to Dmajor. The ratio of minor to major diameters was also calculated to measure airway eccentricity index (EI), as shown in Figure 2B.

2.4. Statistical Analysis

Two tailed paired t-tests were used to compare measurements at the site of SGS and in the trachea between the three timepoints and between end-inspiration and end-expiration. Spearman’s correlation co-efficient (r) was used to correlate measurements of the trachea obtained using ETT-sizing and MRI. For all the boxplots in the results section, the median is indicated by a central red line, 25th and 75th percentiles are indicated by the top and bottom edges of the box, respectively. The most extreme data points not considered as outliers are indicated by whiskers, whereas the outliers (greater than 1.5 times the inter-quartile range away from the top or bottom) are indicated by the ‘+’ symbol. P-values less than 0.05 were considered statistically significant.

3. RESULTS:

3.1. MRI assessment of SGS

Figure 3 shows the airway CSA at the location of SGS calculated from the ungated MRI at the three timepoints. There was a significant decrease between the baseline and post-injury timepoints (p=0.003) with an average CSA decrease of 38%. There was an average CSA increase of 18% between the post injury and post balloon dilation treatment timepoints; however, this increase was not statistically significant (p=0.08). There was a significant difference in the CSA at the location of SGS between baseline and post balloon dilation treatment (p=0.015), with the average CSA at post balloon dilation being 22% lower than at baseline.

Figure 3.

Figure 3.

Open in a new tab

Cross-sectional areas of the rabbits at the site of SGS calculated using UTE MRI at the three timepoints. CSA of the rabbit airways at the site of stenosis significantly decreased during post-injury timepoint from the baseline timepoint. Balloon dilation treatment resulted in an increase in the CSA at the site of stenosis; however, it was still significantly lower than the baseline CSA values.

3.2. Correlation between MRI and ETT sizing measurements of SGS

All rabbits at the baseline timepoint were sized with a 4.0 mm ETT prior to inducing stenosis. Two rabbits had a free-leak at 4.0 mm ETT size and hence their baseline subglottic diameter could not be assessed by ETT-sizing.

Figure 4A shows a significant correlation between CSA at the site of SGS calculated from ETT and ungated MRI at the post-injury timepoint (r=0.93; p<0.005) and for the baseline and post-injury timepoints (r=0.89; p<0.005) at the site of SGS. However, results from post balloon dilation were not included as the airways at that timepoint were more eccentric compared to the other two time-points (See sections 3.3 and Discussion).

Figure 4.

Figure 4.

Open in a new tab

(A) Correlation between CSA at the site of SGS obtained through ETT sizing and through assessment using ungated UTE MRI. (B) Correlation between OD obtained through ETT sizing and the major and minor diameters obtained through assessment using ungated UTE MRI at the site of SGS for the baseline and post-injury timepoints.

CSA and major and minor diameters at the site of stenosis obtained through UTE MRI assessment show significant correlation with CSA and OD, respectively obtained through ETT sizing.

There was a significant correlation between the outer diameter (OD) calculated from ETT-sizing and Dmajor obtained from MRI assessment of the airway at the site of SGS for the baseline and post-injury timepoints (r=0.88; p<0.0001) as shown in Figure 4B. Similarly, there was a significant correlation between OD calculated from ETT and Dminor obtained from MRI assessment of the airway at the site of SGS (r=0.79; p<0.0001).

3.3. Investigation of tracheal dynamics due to SGS

To investigate whether the presence of SGS results in dynamic changes in the distal trachea, either from softening of the trachea or increased amplitude of positive and negative pressure swing, the average CSA of the trachea was calculated from respiratory-gated UTE MR images at end-expiration and end-inspiration for all three timepoints. No significant difference in the average CSA of the airway was observed between end-expiration and end-inspiration for all the three imaging timepoints (all p>0.05), indicating no airway dynamics during tidal breathing as shown in Figure 5.

Figure 5.

Figure 5.

Open in a new tab

Average CSA of the rabbits’ airways at end-expiration and end-inspiration assessed from gated UTE MRI images at the three imaging timepoints. There was no significant difference between the average CSA of the rabbits’ airways between end-expiration and end-inspiration at any of the three timepoints, indicating no dynamic airway collapse.

3.4. Incidental Finding: Increased eccentricity of trachea following balloon dilation treatment

Although there was no dynamic airway collapse due to SGS, a change in the shape of the upper trachea was observed. The tracheal shape was quantified using the parameter EI from glottis to the midpoint of the trachea. The airways at the post balloon dilation timepoint during end-inspiration were more eccentric (lower EI) than at the other timepoints as shown in Figure 6. The EI of the airways did not change significantly between end-inspiration and end-expiration.

Figure 6.

Figure 6.

Open in a new tab

Figure showing the minimum ratio of minor and major diameters (EI) for all three timepoints at end-inspiration for each timepoint from glottis to midpoint of the trachea (A). Posterior view of the airway surface of a rabbit at each of the three timepoints (B). There is a significant increase in eccentricity in the rabbits’ airways post the balloon dilation treatment timepoint.

4. DISCUSSION:

Subglottic stenosis is a serious respiratory condition in neonates. The current gold-standard to detect SGS and monitor the effectiveness of treatments to alleviate SGS in neonates is ETT-sizing during bronchoscopy. This study investigated the use of 3D UTE-MRI, a non-invasive, high-resolution imaging technique, to detect SGS and evaluate the effectiveness of balloon dilation to treat SGS in a rabbit model. UTE-MRI correlated exceptionally well for evaluating airway size and the development of SGS.

SGS was detected using UTE-MRI as there was a significant decrease in the CSA at the site of SGS between the baseline and the post-injury timepoints as shown in Figure 3. The CSA at the site of SGS increased after balloon dilation, but it did not return to baseline values. These results suggest that clinically, balloon dilation can help to improve conditions of neonates diagnosed with SGS by increasing the airway size at the stenosis site; further work may be warranted to investigate whether variations in balloon dilation procedural parameters, including number of dilations performed, affect the degree of to which SGS can be clinically resolved.

Comparison of airway geometric parameters at the site of SGS obtained from ETT-sizing and UTE-MRI demonstrated significant correlation between the two approaches for the baseline and post-injury timepoints as well as for the post-injury timepoint alone. The correlation at baseline timepoint alone could not be determined as all the rabbits were sized with a 4.0 mm ETT at baseline. These results demonstrate that MRI can accurately determine airway geometric parameters comparable to ETT-sizing. The use of non-invasive MRI could be particularly useful with patients for whom invasive procedures such as ETT-sizing and bronchoscopy cannot be performed due to the risk of clinical complications.

To investigate whether SGS causes dynamic airway collapse, the average CSA of the tracheas were calculated at end-inspiration and end-expiration. The rationale for choosing the end-inspiration and end-expiration timepoints was that the largest decrease in CSA from end-inspiration is expected at end-expiration due to positive pleural pressure acting on the airway surface causing it to collapse.23 There was no significant difference in the average CSA of the trachea between end-inspiration and end-expiration at the three timepoints. This suggests that there was no significant increase in airway dynamics observed after the induced SGS or after the treatment procedure as initially hypothesized.

Furthermore, although there was no dynamic airway collapse, there was a significant increase in eccentricity of the airway from glottis to the mid-point of the trachea post balloon dilation at end-inspiration and end-expiration. In this study, balloon dilation treatment appears to cause invagination of the posterior trachea. This increase in airway eccentricity could be attributed to tracheal edema following balloon dilation. A delay of approximately 30 minutes to 2 hours between the two procedures could have been enough for the tracheal edema to develop and be imaged during the MRI scan. Due to these differences in time and airway conditions between ETT-sizing and MRI scan, the data at the post balloon dilation timepoint was discarded from the correlation between airway measurements made with the two modalities. The rabbits were only imaged at a single timepoint post balloon dilation; hence it is unknown whether the increased eccentricity of the trachea was acute and then resolved over time or if it was persistent.

UTE-MRI images have a high isotropic resolution of 0.7 mm; however, images obtained from CT and LR-OCT have better resolution (0.2–0.5 mm for CT and ~10 μm for LR-OCT). This resolution limit results in partial volume effects at the boundary of the airway and the adjacent tissue, resulting in small airway segmentation inaccuracies that could affect geometric airway evaluations. However, deploying a consistent threshold for segmentation can mitigate any bias in segmentation and make the process consistent. Another limitation of our study was that post balloon dilation UTE-MRI scan was performed after some delay following the ETT-sizing. The airway eccentricity observed following the treatment procedure could have possibly been due to airway edema resulting from the procedure. Longitudinal scanning of the airway at additional timepoints following the treatment procedure would have allowed quantification of the improvement in the airway size following reduction of edema. Additionally, while T2-weighted MR sequences could confirm the presences of edema, such scans were not acquired since edema-induced tracheal eccentricity was an unexpected finding.

This study represents the first application of UTE-MRI in measuring SGS and response to treatment in a rabbit model. UTE-MRI can overcome the limitations faced by other imaging methods, as it can be performed during tidal breathing and without the need for sedation or ionizing radiation, which is extremely important in neonates. UTE-MRI can also quantify geometric properties of the airway without any distortion to the airway as is the case in ETT-sizing and some LR-OCT procedures, which can result in incorrect measurement of the airway size and CSA. Another major advantage of using UTE-MRI is the ability to retrospectively gate the MRI data to obtain images at specific timepoints during tidal breathing, allowing for evaluation of airway dynamics. MRI systems are available at most hospitals and do not require additional expertise in set up and scanning, and major MRI vendors are making UTE sequences available commercially. These advantages suggest UTE-MRI can be a very useful tool to detect SGS and longitudinally monitor efficacy of treatment methods in neonatal population.

Future studies will include computational fluid dynamics (CFD) simulations based on these imaging techniques to evaluate airflow and the work of breathing due to SGS. Application of the present techniques to neonatal patients diagnosed with SGS may have clinical relevance.

5. CONCLUSION:

UTE-MRI successfully detected SGS post injury due to significant decrease in the CSA from baseline measurements. Significant positive correlations were observed between geometric parameters obtained from ETT-sizing and UTE-MRI for the baseline and post injury timepoints. Furthermore, no significant changes in tracheal dynamics was observed in the rabbits due to SGS; however, an incidental finding demonstrated that the tracheal eccentricity significantly increased following the balloon dilation treatment as observed from gated UTE-MRI. Overall, this study successfully demonstrated the use of UTE-MRI as a non-invasive alternative to objectively quantify airway geometric parameters and detect SGS in a rabbit model with significant correlation to the current clinical gold standard. The results of this study indicate the potential to use UTE-MRI for non-invasively detecting and monitoring SGS in neonates in a clinical setting and potentially for evaluating SGS-related airway dynamics with retrospective gating.

Acknowledgements:

The authors would like to acknowledge the grant support from Research Innovation and Pilot Funding Program at Cincinnati Children’s Hospital and NIH T32 HL007752.

Footnotes

Level of Evidence: Not Applicable

Conflicts of Interest: None

7. REFERENCES:

  • 1.Walner DL, Loewen MS, Kimura RE. Neonatal subglottic stenosis - Incidence and trends. Laryngoscope. 2001. doi: 10.1097/00005537-200101000-00009 [DOI] [PubMed] [Google Scholar]
  • 2.Schweiger C, Marostica PJC, Smith MM, Manica D, Carvalho PRA, Kuhl G. Incidence of post-intubation subglottic stenosis in children: Prospective study. J Laryngol Otol. 2013;127(4):399–403. doi: 10.1017/S002221511300025X [DOI] [PubMed] [Google Scholar]
  • 3.Joshi VV, Mandavia SG, Stern L, Wiglesworth FW. Acute Lesions Induced by Endotracheal Intubation: Occurrence in the Upper Respiratory Tract of Newborn Infants With Respiratory Distress Syndrome. Am J Dis Child. 1972;124(5):646–649. doi: 10.1001/archpedi.1972.02110170024003 [DOI] [PubMed] [Google Scholar]
  • 4.Myer CM, O’connor DM, Cotton RT. Proposed grading system for subglottic stenosis based on endotracheal tube sizes. Ann Otol Rhinol Laryngol. 1994. doi: 10.1177/000348949410300410 [DOI] [PubMed] [Google Scholar]
  • 5.Eid E. Anesthesia for subglottic stenosis in pediatrics. Saudi J Anaesth. 2009. doi: 10.4103/1658-354x.57882 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Leventhal DD, Krebs E, Rosen MR. Flexible laser bronchoscopy for subglottic stenosis in the awake patient. Arch Otolaryngol - Head Neck Surg. 2009. doi: 10.1001/archoto.2009.28 [DOI] [PubMed] [Google Scholar]
  • 7.Ho AMH, Mizubuti GB, Dion JM, Beyea JA. Paediatric postintubation subglottic stenosis. Arch Dis Child. 2019;0(0):2019. doi: 10.1136/archdischild-2018-316517 [DOI] [PubMed] [Google Scholar]
  • 8.Zdanski C, Davis S, Hong Y, et al. Quantitative assessment of the upper airway in infants and children with subglottic stenosis. Laryngoscope. 2016. doi: 10.1002/lary.25482 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Hernandez RJ, Tucker GF. Congenital tracheal stenosis: Role of CT and high kV films. Pediatr Radiol. 1987. doi: 10.1007/BF02388158 [DOI] [PubMed] [Google Scholar]
  • 10.Jewett BS, Cook RD, Johnson KL, et al. Subglottic stenosis: correlation between computed tomography and bronchoscopy. Ann Otol Rhinol Laryngol. 1999;108(9):837–841. doi: 10.1177/000348949910800904 [DOI] [PubMed] [Google Scholar]
  • 11.Lam WWM, Tam PKH, Chan FL, Chan KL, Cheng W. Esophageal atresia and tracheal stenosis: Use of three-dimensional CT and virtual bronchoscopy-in neonates, infants, and children. Am J Roentgenol. 2000. doi: 10.2214/ajr.174.4.1741009 [DOI] [PubMed] [Google Scholar]
  • 12.Sharma GK, Ahuja GS, Wiedmann M, et al. Long-range optical coherence tomography of the neonatal upper airway for early diagnosis of intubation-related subglottic injury. Am J Respir Crit Care Med. 2015. doi: 10.1164/rccm.201501-0053OC [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Ajose-Popoola O, Su E, Hamamoto A, et al. Diagnosis of subglottic stenosis in a rabbit model using long-range optical coherence tomography. Laryngoscope. 2017. doi: 10.1002/lary.26241 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Kozlowski KM, Sharma GK, Chen JJ, et al. Dynamic programming and automated segmentation of optical coherence tomography images of the neonatal subglottis: enabling efficient diagnostics to manage subglottic stenosis. J Biomed Opt. 2019. doi: 10.1117/1.jbo.24.9.096001 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Higano NS, Hahn AD, Tkach JA, et al. Retrospective respiratory self-gating and removal of bulk motion in pulmonary UTE MRI of neonates and adults. Magn Reson Med. 2017. doi: 10.1002/mrm.26212 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Hahn AD, Cao X, Higano NS, et al. Self-Gating of Respiratory Motion for Pulmonary Ultra Short Echo Time MRI of Infants in the NICU. Magn Reson Med AJR Am J Roentgenol AJR Am J Roentgenol J Am Stat Assoc Magn Reson Med. 2013. [Google Scholar]
  • 17.Bates AJ, Higano NS, Hysinger EB, Fleck RJ, Hahn AD, Fain SB, Kingma PS, Amin RS, Woods JW. Quantitative assessment of airway dynamics and abnormalities during restful breathing in infants using MRI. Am J Respir Crit Care Med. 2018. [Google Scholar]
  • 18.Higano NS, Bates AJ, Hysinger EB, et al. Quantitative geometric assessment of regional airway collapse in neonates via retrospectively respiratory-gated 1H {UTE} {MRI}. In: Proc. Joint Annual Meeting ISMRM-ESMRMB, Paris, France.; 2018. [Google Scholar]
  • 19.Hahn AD, Higano NS, Walkup LW, Thomen RP, Cao X, Merhar SL, Tkach JA, Woods JW, Fain SW. Pulmonary MRI of neonates in the intensive care unit using 3D ultrashort echo time and a small footprint MRI system. J Magn Reson Imaging. 2017. DOI: 10.1002/jmri.25394 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Higano NS, Bates AJ, Hysinger EB, et al. Dynamic Tracheal Collapse and Correlation to Later Tracheostomy in Neonates with Bronchopulmonary Dysplasia Via Quantitative Ultrashort Echo-Time MRI. In:; 2019. doi: 10.1164/ajrccm-conference.2019.199.1_meetingabstracts.a4264 [DOI] [Google Scholar]
  • 21.Hysinger EB, Bates AJ, Higano NS, et al. Ultrashort Echo-Time MRI for the Assessment of Tracheomalacia in Neonates. In: Chest. ; 2020. doi: 10.1016/j.chest.2019.11.034 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Higano NS, Spielberg DR, Fleck RJ, et al. Neonatal pulmonary magnetic resonance imaging of bronchopulmonary dysplasia predicts short-term clinical outcomes. Am J Respir Crit Care Med. 2018. doi: 10.1164/rccm.201711-2287OC [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Bates AJ, Higano NS, Hysinger EB, et al. Quantitative Assessment of Regional Dynamic Airway Collapse in Neonates via Retrospectively Respiratory-Gated 1 H Ultrashort Echo Time MRI. J Magn Reson Imaging. 2019;49(3):659–667. doi: 10.1002/jmri.26296 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Hautefort C, Teissier N, Viala P, Van Den Abbeele T. Balloon dilation laryngoplasty for subglottic stenosis in children: Eight years’ experience. Arch Otolaryngol - Head Neck Surg. 2012. doi: 10.1001/archoto.2011.1439 [DOI] [PubMed] [Google Scholar]
  • 25.Elkerbout SC, Van Lingen RA, Gerritsen J, Roorda RJ. Endoscopic balloon dilatation of acquired airway stenosis in newborn infants: A promising treatment. Arch Dis Child. 1993;68(1 SPEC NO):37–40. doi: 10.1136/adc.68.1_Spec_No.37 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Axon PR, Hartley C, Rothera MP. Endoscopic balloon dilatation of subglottic stenosis. J Laryngol Otol. 1995. doi: 10.1017/s0022215100131561 [DOI] [PubMed] [Google Scholar]
  • 27.Maresh A, Preciado DA, O’Connell AP, Zalzal GH. A comparative analysis of open surgery vs endoscopic balloon dilation for pediatric subglottic stenosis. In: JAMA Otolaryngology - Head and Neck Surgery. ; 2014. doi: 10.1001/jamaoto.2014.1742 [DOI] [PubMed] [Google Scholar]
  • 28.Durden F, Sobol SE. Balloon laryngoplasty as a primary treatment for subglottic stenosis. Arch Otolaryngol - Head Neck Surg. 2007. doi: 10.1001/archotol.133.8.772 [DOI] [PubMed] [Google Scholar]
  • 29.Kampmann C, Wiethoff CM, Huth RG, et al. Management of life-threatening tracheal stenosis and tracheomalacia in patients with mucopolysaccharidoses. In: JIMD Reports. ; 2017. doi: 10.1007/8904_2016_578 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Visaya JM, Ward RF, Modi VK. Feasibility and mortality of airway balloon dilation in a live rabbit model. JAMA Otolaryngol - Head Neck Surg. 2014;140(3):215–219. doi: 10.1001/jamaoto.2013.6541 [DOI] [PubMed] [Google Scholar]
  • 31.Schweiger C, Hart CK, Tabangin ME, Cohen AP, Roetting NJ, de Alarcón A. Impact of Balloon Diameter on Dilation Outcomes in a Model of Rabbit Subglottic Stenosis. Laryngoscope. 2019. doi: 10.1002/lary.27574 [DOI] [PubMed] [Google Scholar]
  • 32.Tkach JA, Hillman NH, Jobe AH, et al. An MRI system for imaging neonates in the NICU: Initial feasibility study. Pediatr Radiol. 2012. doi: 10.1007/s00247-012-2444-9 [DOI] [PubMed] [Google Scholar]
  • 33.Tkach JA, Li Y, Pratt RG, et al. Characterization of acoustic noise in a neonatal intensive care unit MRI system. Pediatr Radiol. 2014. doi: 10.1007/s00247-014-2909-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Hahn AD, Higano NS, Walkup LL, et al. Pulmonary MRI of neonates in the intensive care unit using 3D ultrashort echo time and a small footprint MRI system. J Magn Reson Imaging. 2017. doi: 10.1002/jmri.25394 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 35.Yushkevich PA, Piven J, Hazlett HC, et al. User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. Neuroimage. 2006. doi: 10.1016/j.neuroimage.2006.01.015 [DOI] [PubMed] [Google Scholar]

RESOURCES