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Laryngotracheal anomalies and airway fluoroscopy in infants
International Journal of Pediatric Otorhinolaryngology 97 (2017) 109e112
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
Laryngotracheal anomalies and airway fluoroscopy in infants Amal Isaiah, MD, DPhil, Kevin D. Pereira, MD, MS * Department of OtorhinolaryngologydHead and Neck Surgery, University of Maryland School of Medicine, Baltimore, MD, United States
a r t i c l e i n f o
a b s t r a c t
Article history: Received 14 November 2016 Received in revised form 17 March 2017 Accepted 28 March 2017 Available online 30 March 2017
Objectives: The role of airway fluoroscopy in the diagnosis of laryngotracheal anomalies in infants is controversial. We aimed to (i) compare airway fluoroscopic characteristics with endoscopic findings in infants presenting for evaluation of upper airway obstruction and (ii) assess the as low as is reasonably achievable (ALARA) status for airway fluoroscopy as an initial diagnostic test in suspected laryngotracheal anomalies. Materials and methods: We performed a retrospective review of children who underwent fluoroscopy and endoscopic evaluation of the airway in the operating room for suspected laryngotracheal anatomic abnormalities. Thirty-four infants who underwent both procedures at a tertiary level university-based children's hospital from January 1, 2008 to December 1, 2013 were included. Infants with suspected foreign bodies or an existing tracheostomy were excluded. Intraoperative findings from endoscopy and radiologic interpretation from fluoroscopy were compared using standard tools for validation of a diagnostic test. These metrics were compared with historic data that suggested good correlation between radiologic and endoscopic findings in older children. Results: The median age was 3.6 months (range 1e8 months). The sensitivity of airway fluoroscopy for determining laryngotracheal pathology was 18%. Specificity, positive predictive value and negative predictive value were 83%, 67% and 35%, respectively. Although each fluoroscopic exposure was optimized for pediatric patients, the median cumulative exposure to ionizing radiation was 19 mR (range 10 e34 mR). Conclusions: Airway fluoroscopy yields metrics that are overall poor to be considered a valid and accurate universal radiologic diagnostic test in infants evaluated for laryngotracheal pathology. The cumulative exposure to ionizing radiation from use of a fluoroscope cannot be justified by the sensitivity of the test and may not conform to ALARA standards for imaging in this population. © 2017 Elsevier B.V. All rights reserved.
This study was presented as an oral presentation at the American Society for Pediatric Otolaryngology Spring Meeting, Chicago, IL, May 18e22, 2016. Keywords: Airway fluoroscopy Laryngotracheal anomalies Infants
1. Introduction Visualization of the dynamic infant airway using invasive and non-invasive techniques has continued to evolve over the course of last several decades. Initial assessments were performed using the rigid metallic ventilating bronchoscope and were significantly hindered by the route and depth of anesthesia. Additional morbidity and mortality were also attributed to these early anesthetic protocols as they were predominantly gas-based, and precise monitoring of the depth of anesthesia was technically challenging based on clinical assessments alone. The first reports of using dynamic x-ray imaging to examine the
* Corresponding author. Department of OtorhinolaryngologydHead and Neck Surgery, 16 S. Eutaw St Ste 500, Baltimore, MD 21201, United States. E-mail address: [email protected] (K.D. Pereira). http://dx.doi.org/10.1016/j.ijporl.2017.03.033 0165-5876/© 2017 Elsevier B.V. All rights reserved.
central airways in children appeared in an early description of image intensification from the Institute of Radio Engineers (IRE) Transactions on Medical Electronics [1]. This new technique using remote delivery of the collimated x-ray beam was expected to advance imaging of the upper airway without instillation of radiographic contrast media as air itself provided dynamic contrast. These early images were utilized principally for screening for tracheobronchial foreign bodies and supplanted expiratory films to a certain degree by relying on dynamic changes within the central airways [2]. In the first complete description of using radiationoptimized fluoroscopy as a diagnostic modality in children presenting with stridor, authors reported very high sensitivity from phantoms [3]. The two important techniques described included selective filtration of a high energy x-ray beam and magnification of the area under study. In combination, the authors also mitigated the radiologic contrast between bone and soft tissue, thus
110
A. Isaiah, K.D. Pereira / International Journal of Pediatric Otorhinolaryngology 97 (2017) 109e112
improving the contrast associated with air. Realizing that dynamic imaging of the upper airway still involved combining images from multiple exposures that cumulatively increased exposure to ionizing radiation in infants and children, the focus of imaging shifted to obstructive sleep apnea (OSA). In one of the earliest studies describing fluoroscopic abnormalities in children with OSA the authors concluded that this technique should be reserved for children with mild adenotonsillar enlargement, craniofacial dysplasia, prior cleft palate repair, or neuromuscular disorders [4]. While developments in upper airway imaging have continued to streamline the technique of x-ray-based imaging in children, the gold standard for assessment of the airway remains direct endoscopic evaluation of the airway during spontaneous respiration. However, its status as the ideal tool in the diagnosis of stridor in children with suspected laryngotracheal anomalies could be questioned, when the potential risks and costs associated with general anesthesia should be taken into consideration. This may specifically be a dilemma in relatively stable infants in whom dynamic conditions such as laryngomalacia, tracheomalacia or vascular rings may be suspected as the potential etiology of obstruction. One study [5] suggested a step-wise approach including use of fluoroscopy for screening prior to definitive rigid bronchoscopy. Additionally, less invasive investigations such as flexible fiberoptic exams cannot yield adequate information about the subglottis or trachea, which is important given the significant incidence of synchronous second lesions seen in the lower airway in children who present with supraglottic pathology alone [6]. Fluoroscopy has been evaluated as a screening tool for the airway in the past. Despite its widespread use at some institutions, the results are equivocal regarding the diagnostic accuracy of airway fluoroscopy even with the best filters and spot-size optimization. Berg et al. [7] reported a retrospective cohort of infants where, the rate of disagreement between fluoroscopic and endoscopic findings approached 60%. In the same study, the reported sensitivity of airway fluoroscopy was less than 50% overall, and only 27% in infants with an endoscopic diagnosis of laryngomalacia. They concluded that the utility of the study for imaging dynamic airway obstruction was poor. These findings were in contradiction with those reported by Rudman et al. [8] who found the overall sensitivity was much higher reaching 80% for tracheal or subglottic pathology. It suggests that there may be some benefit in performing an airway fluoroscopy to help determine the need for rigid bronchoscopy in a subset of patients in whom the clinical suspicion of a definite anatomic lesion is low. Airway fluoroscopy has specifically been found to be useful for evaluation of airway foreign bodies, by supplementing the data available from chest radiographs [9], especially when clinical history is unreliable. A more recent concern has been the avoidable exposure to ionizing radiation in infants and children. While high-quality studies in this area are impractical, there is supporting evidence for increased risk in infants as a function of decreasing age and increasing radiation exposure. For example, Karlsson et al. based on surveillance of a historical cohort of 28,000 infants irradiated for hemangiomas, demonstrated a significant increase in the incidence of intracranial malignancies based on dose-response relationship [10]. Numerous advisories now enforce the as low as is reasonably achievable (ALARA) standard to shield against biologic damage resulting from ionizing radiation [11]. This has led to an interest in imaging parameters for fluoroscopy to ensure radiation safety. This study was undertaken to examine the diagnostic accuracy of using airway fluoroscopy for suspected laryngotracheal anomalies in infants. Although literature documents a few studies of its use in the pediatric population, there is sparse data from infants. In addition, we assessed the ALARA imaging standards of using airway
fluoroscopy as a radiation-optimized tool to compare the relative risks of imaging with those of rigid endoscopy under anesthesia. 2. Methods A retrospective review of the medical records was performed of infants who underwent both outpatient airway fluoroscopy and endoscopic evaluation of the airway in the operating room for suspected laryngotracheal pathology from January 1, 2008 to December 1, 2013 at the University of Maryland Children's Hospital. Infants with suspected foreign bodies or an existing tracheostomy were excluded. The study was approved by the Institutional Review Board (IRB) of the University of Maryland School of Medicine. Due to the retrospective nature of the study, the need to obtain consent was waived. Each fluoroscopy procedure was performed using the same imaging protocol. The fluoroscope camera was set to the cine (high frame-rate) mode. The infant's larynx, trachea and mainstem bronchi were observed during inspiration and expiration. Symmetry of lung expansion was also assessed during each respiratory cycle. Additional antero-posterior as well as lateral projections were obtained during inspiration and expiration. Pathologic narrowing, dynamic collapse and/or fixed airway lesions were interpreted by two pediatric radiologists. Endoscopic examination of the airway was performed by a single pediatric otolaryngologist and followed airway fluoroscopies. All exams were performed using a rigid telescope while obtaining exposure using an appropriatelysized Parson's laryngoscope during spontaneous respiration that followed mask inhalational induction of general anesthesia and supplemented with intravenous propofol. Both procedures were performed within 2 weeks of each other to facilitate preoperative stratification of the degree of airway obstruction, to improve outcomes with the information available from imaging. For each infant who underwent the procedure, the airway fluoroscopic findings were compared with rigid endoscopic findings as the definitive gold standard. The fluoroscopic exposure time and cumulative ionizing radiation exposure were also obtained to determine if ALARA standards of imaging could be achieved. The comparisons between radiologic and endoscopic findings were validated by standards tests including sensitivity, specificity, positive predictive value, and negative predictive value. These metrics were compared with historic data that suggest good correlation between radiologic and endoscopic findings in older children. 3. Results Thirty-four infants fulfilled the criteria for inclusion in the study. The median age was 3.6 months (range 1e8 months). All airway fluoroscopic and endoscopic examinations were uneventful. Abnormal pathology was observed in 6 fluoroscopic examinations. Endoscopic examination of the airway revealed pathology in 22/34 patients (65%). The most common fluoroscopic finding was normal anatomy. Of the 6 abnormal fluoroscopies, the most common finding was subglottic stenosis (3/6 studies). Laryngomalacia was noted in one patient and a subglottic cyst was discovered in another infant. A vascular ring was observed in one study that appeared to be causing tracheomalacia. Among the abnormal rigid endoscopic airway exams, subglottic stenosis was the most common finding (10/22). Four patients were noted to have laryngomalacia. Other uncommon lesions included a subglottic cyst, tracheomalacia, vascular ring and bronchomalacia. Results from the fluoroscopic exams were compared with endoscopic assessment as the gold standard (Table 1). Overall sensitivity was 18% (95% CI [6, 41%]) with specificity of 83% [51, 97%]. The positive predictive value of airway fluoroscopy was 67%
A. Isaiah, K.D. Pereira / International Journal of Pediatric Otorhinolaryngology 97 (2017) 109e112
111
Table 1 Confusion matrix comparing airway fluoroscopic findings with rigid endoscopic assessment. The number of patients in whom the primary fluoroscopy and endoscopy findings were available provided the data for deriving sensitivity, specificity, positive and negative predictive values as described in the Results.
Endoscopy: pathology not present Endoscopy: pathology present Total
Fluoroscopy: pathology not present
Fluoroscopy: pathology present
Total
10 18 28
2 4 6
12 22 34
[24, 94%] and the negative predictive value was 35% [19, 56%]. For any given fluoroscopic study, the probability of an abnormal result was 18% [7, 35%]. Similar value for a normal study was 82% [51, 97%]. Conventional likelihood ratio for an abnormal fluoroscopy was 1.1 [0.2, 5.1]. Normal fluoroscopic findings had a likelihood ratio of 0.98 [0.8, 1.2]. Fluoroscopic exposure times ranged from 1 to 2 min at 8e15 mR/minute. Each fluoroscopic spot film was optimized for exposure in pediatric patients, although median cumulative exposure to ionizing radiation was 19 mR (range 10e34 mR). 4. Discussion Evaluation of a child with suspected airway pathology involves an algorithm that begins with clinical assessment, which may then proceed to flexible laryngoscopy, airway imaging and direct endoscopic examination under anesthesia. Over the years, rigid endoscopy during spontaneous respiration has evolved as the gold standard for assessment of both static and dynamic airway abnormalities. Availability, cost and general anesthesia necessary for rigid endoscopy as well as the need for specialized instruments are limiting factors for wide-spread use. Given these factors, airway imaging can be a good initial tool to provide an assessment of airway patency, uncover pathology and help prepare for any eventual procedure. Airway fluoroscopy has been used historically with reasonable sensitivity especially for dynamic airway lesions [8]. It has specifically been described as a valuable adjunct in the identification and management of upper airway obstruction when hypopharyngeal collapse or multi-level obstruction are suspected [12]. Our study shows that the diagnostic value of airway fluoroscopy is particularly low in infants and reliance on this modality to make a primary diagnosis should be avoided. In addition, negative findings should be viewed carefully, and always confirmed with rigid endoscopic assessment if the index of suspicion is high on clinical grounds. Our findings that suggest fluoroscopy as a suboptimal imaging modality are in agreement with other similar studies, specifically for laryngotracheal anomalies and stridor [7], and particularly in tracheomalacia [13]. Our results also potentially raise concern for the poor sensitivity of airway fluoroscopy to impact detection of not only the primary pathology, but also the secondary lesions that are seen in association with conditions such as laryngomalacia. Factors that also merit attention include the recognition that our data was obtained from infants in whom smallersized central airways required higher resolution fluoroscopic images. With growing concern of x-ray-based studies not meeting ALARA standards, it is essential to reconsider the radiation exposure profiles of common imaging studies, including swallow studies in infants and young children. The factors that determine the suitability of fluoroscopy for imaging airway obstruction are related to (i) machine design and operation, (ii) exposure rate and cumulative exposure time, and (iii) use of filters and collimation [14]. Our exposure times, although significant longer than normal xray series, were associated with high frame rates (15 frames/second), often necessary to resolve the smaller-sized infant airways. This is the principal reason for the exposure measurements to be
approximately 25% greater than the mean exposure reported in a previous study in older children [8]. Importantly, this equals the exposure to ionizing radiation from 20 chest x-ray exposures in young children [15]. Although legal limits for pediatric fluoroscopy have not been established, a study with unacceptably low sensitivity, cannot be recommended as the primary diagnostic tool for airway pathology when rigid bronchoscopy is readily available. This is particularly important in infants in whom the airway is significantly smaller and studies require both higher frame rates as well as exposure times to reach a diagnosis. Conversely, these disadvantages need to be carefully weighed against the real-time situation where at times pediatric airway expertise may not be available and the risks of general anesthesia are substantial. We acknowledge that the small study sample size as well as the lack of blinding from the retrospective nature of this study may potentially affect conclusions. In addition, it is possible that technical aspects of airway fluoroscopy may be different in other institutions, where it is used more extensively as a screening tool. As is the case with most interpretative studies, imaging modalities are operator-dependent and higher diagnostic accuracy could be related to familiarity with the technique and resolution of the images. 5. Conclusions Our results thus do not support the universal use of airway fluoroscopy as a screening instrument for laryngotracheal anomalies in infants. In the absence of other resilient tools for dynamic airway imaging, we recommend rigid endoscopy as the gold standard for definitive diagnosis. With expanding ALARA standards, it is likely that exposures associated with fluoroscopy will continue to remain restricted for use in infants and young children. Other imaging modalities like ultrasound with more advanced resolution and without exposure to radiation may be an option in the future. Conflicts of interest The authors declare none. Acknowledgements None. References [1] J. Kirkpatrick, Medical applications of fluoroscopic image intensification - III, ME-6, IRE Trans. Med. Electron (1959) 82e83, http://dx.doi.org/10.1109/IRETME.1959.5007921. [2] I.G. Kim, W.M. Brummitt, A. Humphry, S.W. Siomra, W.B. Wallace, Foreign body in the airway: a review of 202 cases, Laryngoscope 83 (1973) 347e354, http://dx.doi.org/10.1288/00005537-197303000-00004. [3] P.M. Joseph, W.E. Berdon, D.H. Baker, T.L. Slovis, J.O. Haller, Upper airway obstruction in infants and small children. Improved radiographic diagnosis by combining filtration, high kilovoltage, and magnification, Radiology 121 (1976) 143e148, http://dx.doi.org/10.1148/121.1.143. [4] S.K. Fernbach, R.T. Brouillette, T.W. Riggs, C.E. Hunt, Radiologic evaluation of adenoids and tonsils in children with obstructive sleep apnea: plain films and fluoroscopy, Pediatr. Radiol. 13 (1983) 258e265, http://dx.doi.org/10.1007/
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BF00973342. [5] O. Cavel, M. Bergeron, L. Garel, P. Arcand, P. Froehlich, Questioning the legitimacy of rigid bronchoscopy as a tool for establishing the diagnosis of a bronchial foreign body, Int. J. Pediatr. Otorhinolaryngol. 76 (2012) 194e201, http://dx.doi.org/10.1016/j.ijporl.2011.11.002. [6] E. Adil, T. Rager, M. Carr, Location of airway obstruction in term and preterm infants with laryngomalacia, Am. J. Otolaryngol. 33 (2012) 437e440, http:// dx.doi.org/10.1016/j.amjoto.2011.10.021. [7] E. Berg, I. Naseri, S.E. Sobol, The role of airway fluoroscopy in the evaluation of children with stridor, Arch. Otolaryngol. Head. Neck Surg. 134 (2008) 415e418, http://dx.doi.org/10.1001/archotol.134.4.415. [8] D.T. Rudman, C.A. Elmaraghy, W.E. Shiels, G.J. Wiet, The role of airway fluoroscopy in the evaluation of stridor in children, Arch. Otolaryngol. Head. Neck Surg. 129 (2003) 305e309. [9] H.K. Tan, K. Brown, T. McGill, M.A. Kenna, D.P. Lund, G.B. Healy, Airway foreign bodies (FB): a 10-year review, Int. J. Pediatr. Otorhinolaryngol. 56 (2000) 91e99. [10] P. Karlsson, E. Holmberg, M. Lundell, A. Mattsson, L.E. Holm, A. Wallgren, Intracranial tumors after exposure to ionizing radiation during infancy: a
[11] [12]
[13]
[14]
[15]
pooled analysis of two Swedish cohorts of 28,008 infants with skin hemangioma, Radiat. Res. 150 (1998) 357e364. T.L. Slovis, Children, computed tomography radiation dose, and the as Low as Reasonably Achievable (ALARA) concept, Pediatrics 112 (2003) 971e972. S.E. Gibson, C.M. Myer, J.L. Strife, D.M. O'Connor, Sleep fluoroscopy for localization of upper airway obstruction in children, Ann. Otol. Rhinol. Laryngol. 105 (1996) 678e683. M. o. Sanchez, M. c. Greer, I. b. Masters, A. b. Chang, A comparison of fluoroscopic airway screening with flexible bronchoscopy for diagnosing tracheomalacia, Pediatr. Pulmonol. 47 (2012) 63e67, http://dx.doi.org/10.1002/ ppul.21517. K.J. Strauss, S.C. Kaste, The ALARA (as low as reasonably achievable) concept in pediatric interventional and fluoroscopic imaging: striving to keep radiation doses as low as possible during fluoroscopy of pediatric patientsea white paper executive summary, Radiology 240 (2006) 621e622, http://dx.doi.org/ 10.1148/radiol.2403060698. C.H. McCollough, J.T. Bushberg, J.G. Fletcher, L.J. Eckel, Answers to common questions about the use and safety of CT scans, Mayo Clin. Proc. 90 (2015) 1380e1392, http://dx.doi.org/10.1016/j.mayocp.2015.07.011.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
Laryngotracheal anomalies and airway fluoroscopy in infants Amal Isaiah, MD, DPhil, Kevin D. Pereira, MD, MS * Department of OtorhinolaryngologydHead and Neck Surgery, University of Maryland School of Medicine, Baltimore, MD, United States
a r t i c l e i n f o
a b s t r a c t
Article history: Received 14 November 2016 Received in revised form 17 March 2017 Accepted 28 March 2017 Available online 30 March 2017
Objectives: The role of airway fluoroscopy in the diagnosis of laryngotracheal anomalies in infants is controversial. We aimed to (i) compare airway fluoroscopic characteristics with endoscopic findings in infants presenting for evaluation of upper airway obstruction and (ii) assess the as low as is reasonably achievable (ALARA) status for airway fluoroscopy as an initial diagnostic test in suspected laryngotracheal anomalies. Materials and methods: We performed a retrospective review of children who underwent fluoroscopy and endoscopic evaluation of the airway in the operating room for suspected laryngotracheal anatomic abnormalities. Thirty-four infants who underwent both procedures at a tertiary level university-based children's hospital from January 1, 2008 to December 1, 2013 were included. Infants with suspected foreign bodies or an existing tracheostomy were excluded. Intraoperative findings from endoscopy and radiologic interpretation from fluoroscopy were compared using standard tools for validation of a diagnostic test. These metrics were compared with historic data that suggested good correlation between radiologic and endoscopic findings in older children. Results: The median age was 3.6 months (range 1e8 months). The sensitivity of airway fluoroscopy for determining laryngotracheal pathology was 18%. Specificity, positive predictive value and negative predictive value were 83%, 67% and 35%, respectively. Although each fluoroscopic exposure was optimized for pediatric patients, the median cumulative exposure to ionizing radiation was 19 mR (range 10 e34 mR). Conclusions: Airway fluoroscopy yields metrics that are overall poor to be considered a valid and accurate universal radiologic diagnostic test in infants evaluated for laryngotracheal pathology. The cumulative exposure to ionizing radiation from use of a fluoroscope cannot be justified by the sensitivity of the test and may not conform to ALARA standards for imaging in this population. © 2017 Elsevier B.V. All rights reserved.
This study was presented as an oral presentation at the American Society for Pediatric Otolaryngology Spring Meeting, Chicago, IL, May 18e22, 2016. Keywords: Airway fluoroscopy Laryngotracheal anomalies Infants
1. Introduction Visualization of the dynamic infant airway using invasive and non-invasive techniques has continued to evolve over the course of last several decades. Initial assessments were performed using the rigid metallic ventilating bronchoscope and were significantly hindered by the route and depth of anesthesia. Additional morbidity and mortality were also attributed to these early anesthetic protocols as they were predominantly gas-based, and precise monitoring of the depth of anesthesia was technically challenging based on clinical assessments alone. The first reports of using dynamic x-ray imaging to examine the
* Corresponding author. Department of OtorhinolaryngologydHead and Neck Surgery, 16 S. Eutaw St Ste 500, Baltimore, MD 21201, United States. E-mail address: [email protected] (K.D. Pereira). http://dx.doi.org/10.1016/j.ijporl.2017.03.033 0165-5876/© 2017 Elsevier B.V. All rights reserved.
central airways in children appeared in an early description of image intensification from the Institute of Radio Engineers (IRE) Transactions on Medical Electronics [1]. This new technique using remote delivery of the collimated x-ray beam was expected to advance imaging of the upper airway without instillation of radiographic contrast media as air itself provided dynamic contrast. These early images were utilized principally for screening for tracheobronchial foreign bodies and supplanted expiratory films to a certain degree by relying on dynamic changes within the central airways [2]. In the first complete description of using radiationoptimized fluoroscopy as a diagnostic modality in children presenting with stridor, authors reported very high sensitivity from phantoms [3]. The two important techniques described included selective filtration of a high energy x-ray beam and magnification of the area under study. In combination, the authors also mitigated the radiologic contrast between bone and soft tissue, thus
110
A. Isaiah, K.D. Pereira / International Journal of Pediatric Otorhinolaryngology 97 (2017) 109e112
improving the contrast associated with air. Realizing that dynamic imaging of the upper airway still involved combining images from multiple exposures that cumulatively increased exposure to ionizing radiation in infants and children, the focus of imaging shifted to obstructive sleep apnea (OSA). In one of the earliest studies describing fluoroscopic abnormalities in children with OSA the authors concluded that this technique should be reserved for children with mild adenotonsillar enlargement, craniofacial dysplasia, prior cleft palate repair, or neuromuscular disorders [4]. While developments in upper airway imaging have continued to streamline the technique of x-ray-based imaging in children, the gold standard for assessment of the airway remains direct endoscopic evaluation of the airway during spontaneous respiration. However, its status as the ideal tool in the diagnosis of stridor in children with suspected laryngotracheal anomalies could be questioned, when the potential risks and costs associated with general anesthesia should be taken into consideration. This may specifically be a dilemma in relatively stable infants in whom dynamic conditions such as laryngomalacia, tracheomalacia or vascular rings may be suspected as the potential etiology of obstruction. One study [5] suggested a step-wise approach including use of fluoroscopy for screening prior to definitive rigid bronchoscopy. Additionally, less invasive investigations such as flexible fiberoptic exams cannot yield adequate information about the subglottis or trachea, which is important given the significant incidence of synchronous second lesions seen in the lower airway in children who present with supraglottic pathology alone [6]. Fluoroscopy has been evaluated as a screening tool for the airway in the past. Despite its widespread use at some institutions, the results are equivocal regarding the diagnostic accuracy of airway fluoroscopy even with the best filters and spot-size optimization. Berg et al. [7] reported a retrospective cohort of infants where, the rate of disagreement between fluoroscopic and endoscopic findings approached 60%. In the same study, the reported sensitivity of airway fluoroscopy was less than 50% overall, and only 27% in infants with an endoscopic diagnosis of laryngomalacia. They concluded that the utility of the study for imaging dynamic airway obstruction was poor. These findings were in contradiction with those reported by Rudman et al. [8] who found the overall sensitivity was much higher reaching 80% for tracheal or subglottic pathology. It suggests that there may be some benefit in performing an airway fluoroscopy to help determine the need for rigid bronchoscopy in a subset of patients in whom the clinical suspicion of a definite anatomic lesion is low. Airway fluoroscopy has specifically been found to be useful for evaluation of airway foreign bodies, by supplementing the data available from chest radiographs [9], especially when clinical history is unreliable. A more recent concern has been the avoidable exposure to ionizing radiation in infants and children. While high-quality studies in this area are impractical, there is supporting evidence for increased risk in infants as a function of decreasing age and increasing radiation exposure. For example, Karlsson et al. based on surveillance of a historical cohort of 28,000 infants irradiated for hemangiomas, demonstrated a significant increase in the incidence of intracranial malignancies based on dose-response relationship [10]. Numerous advisories now enforce the as low as is reasonably achievable (ALARA) standard to shield against biologic damage resulting from ionizing radiation [11]. This has led to an interest in imaging parameters for fluoroscopy to ensure radiation safety. This study was undertaken to examine the diagnostic accuracy of using airway fluoroscopy for suspected laryngotracheal anomalies in infants. Although literature documents a few studies of its use in the pediatric population, there is sparse data from infants. In addition, we assessed the ALARA imaging standards of using airway
fluoroscopy as a radiation-optimized tool to compare the relative risks of imaging with those of rigid endoscopy under anesthesia. 2. Methods A retrospective review of the medical records was performed of infants who underwent both outpatient airway fluoroscopy and endoscopic evaluation of the airway in the operating room for suspected laryngotracheal pathology from January 1, 2008 to December 1, 2013 at the University of Maryland Children's Hospital. Infants with suspected foreign bodies or an existing tracheostomy were excluded. The study was approved by the Institutional Review Board (IRB) of the University of Maryland School of Medicine. Due to the retrospective nature of the study, the need to obtain consent was waived. Each fluoroscopy procedure was performed using the same imaging protocol. The fluoroscope camera was set to the cine (high frame-rate) mode. The infant's larynx, trachea and mainstem bronchi were observed during inspiration and expiration. Symmetry of lung expansion was also assessed during each respiratory cycle. Additional antero-posterior as well as lateral projections were obtained during inspiration and expiration. Pathologic narrowing, dynamic collapse and/or fixed airway lesions were interpreted by two pediatric radiologists. Endoscopic examination of the airway was performed by a single pediatric otolaryngologist and followed airway fluoroscopies. All exams were performed using a rigid telescope while obtaining exposure using an appropriatelysized Parson's laryngoscope during spontaneous respiration that followed mask inhalational induction of general anesthesia and supplemented with intravenous propofol. Both procedures were performed within 2 weeks of each other to facilitate preoperative stratification of the degree of airway obstruction, to improve outcomes with the information available from imaging. For each infant who underwent the procedure, the airway fluoroscopic findings were compared with rigid endoscopic findings as the definitive gold standard. The fluoroscopic exposure time and cumulative ionizing radiation exposure were also obtained to determine if ALARA standards of imaging could be achieved. The comparisons between radiologic and endoscopic findings were validated by standards tests including sensitivity, specificity, positive predictive value, and negative predictive value. These metrics were compared with historic data that suggest good correlation between radiologic and endoscopic findings in older children. 3. Results Thirty-four infants fulfilled the criteria for inclusion in the study. The median age was 3.6 months (range 1e8 months). All airway fluoroscopic and endoscopic examinations were uneventful. Abnormal pathology was observed in 6 fluoroscopic examinations. Endoscopic examination of the airway revealed pathology in 22/34 patients (65%). The most common fluoroscopic finding was normal anatomy. Of the 6 abnormal fluoroscopies, the most common finding was subglottic stenosis (3/6 studies). Laryngomalacia was noted in one patient and a subglottic cyst was discovered in another infant. A vascular ring was observed in one study that appeared to be causing tracheomalacia. Among the abnormal rigid endoscopic airway exams, subglottic stenosis was the most common finding (10/22). Four patients were noted to have laryngomalacia. Other uncommon lesions included a subglottic cyst, tracheomalacia, vascular ring and bronchomalacia. Results from the fluoroscopic exams were compared with endoscopic assessment as the gold standard (Table 1). Overall sensitivity was 18% (95% CI [6, 41%]) with specificity of 83% [51, 97%]. The positive predictive value of airway fluoroscopy was 67%
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111
Table 1 Confusion matrix comparing airway fluoroscopic findings with rigid endoscopic assessment. The number of patients in whom the primary fluoroscopy and endoscopy findings were available provided the data for deriving sensitivity, specificity, positive and negative predictive values as described in the Results.
Endoscopy: pathology not present Endoscopy: pathology present Total
Fluoroscopy: pathology not present
Fluoroscopy: pathology present
Total
10 18 28
2 4 6
12 22 34
[24, 94%] and the negative predictive value was 35% [19, 56%]. For any given fluoroscopic study, the probability of an abnormal result was 18% [7, 35%]. Similar value for a normal study was 82% [51, 97%]. Conventional likelihood ratio for an abnormal fluoroscopy was 1.1 [0.2, 5.1]. Normal fluoroscopic findings had a likelihood ratio of 0.98 [0.8, 1.2]. Fluoroscopic exposure times ranged from 1 to 2 min at 8e15 mR/minute. Each fluoroscopic spot film was optimized for exposure in pediatric patients, although median cumulative exposure to ionizing radiation was 19 mR (range 10e34 mR). 4. Discussion Evaluation of a child with suspected airway pathology involves an algorithm that begins with clinical assessment, which may then proceed to flexible laryngoscopy, airway imaging and direct endoscopic examination under anesthesia. Over the years, rigid endoscopy during spontaneous respiration has evolved as the gold standard for assessment of both static and dynamic airway abnormalities. Availability, cost and general anesthesia necessary for rigid endoscopy as well as the need for specialized instruments are limiting factors for wide-spread use. Given these factors, airway imaging can be a good initial tool to provide an assessment of airway patency, uncover pathology and help prepare for any eventual procedure. Airway fluoroscopy has been used historically with reasonable sensitivity especially for dynamic airway lesions [8]. It has specifically been described as a valuable adjunct in the identification and management of upper airway obstruction when hypopharyngeal collapse or multi-level obstruction are suspected [12]. Our study shows that the diagnostic value of airway fluoroscopy is particularly low in infants and reliance on this modality to make a primary diagnosis should be avoided. In addition, negative findings should be viewed carefully, and always confirmed with rigid endoscopic assessment if the index of suspicion is high on clinical grounds. Our findings that suggest fluoroscopy as a suboptimal imaging modality are in agreement with other similar studies, specifically for laryngotracheal anomalies and stridor [7], and particularly in tracheomalacia [13]. Our results also potentially raise concern for the poor sensitivity of airway fluoroscopy to impact detection of not only the primary pathology, but also the secondary lesions that are seen in association with conditions such as laryngomalacia. Factors that also merit attention include the recognition that our data was obtained from infants in whom smallersized central airways required higher resolution fluoroscopic images. With growing concern of x-ray-based studies not meeting ALARA standards, it is essential to reconsider the radiation exposure profiles of common imaging studies, including swallow studies in infants and young children. The factors that determine the suitability of fluoroscopy for imaging airway obstruction are related to (i) machine design and operation, (ii) exposure rate and cumulative exposure time, and (iii) use of filters and collimation [14]. Our exposure times, although significant longer than normal xray series, were associated with high frame rates (15 frames/second), often necessary to resolve the smaller-sized infant airways. This is the principal reason for the exposure measurements to be
approximately 25% greater than the mean exposure reported in a previous study in older children [8]. Importantly, this equals the exposure to ionizing radiation from 20 chest x-ray exposures in young children [15]. Although legal limits for pediatric fluoroscopy have not been established, a study with unacceptably low sensitivity, cannot be recommended as the primary diagnostic tool for airway pathology when rigid bronchoscopy is readily available. This is particularly important in infants in whom the airway is significantly smaller and studies require both higher frame rates as well as exposure times to reach a diagnosis. Conversely, these disadvantages need to be carefully weighed against the real-time situation where at times pediatric airway expertise may not be available and the risks of general anesthesia are substantial. We acknowledge that the small study sample size as well as the lack of blinding from the retrospective nature of this study may potentially affect conclusions. In addition, it is possible that technical aspects of airway fluoroscopy may be different in other institutions, where it is used more extensively as a screening tool. As is the case with most interpretative studies, imaging modalities are operator-dependent and higher diagnostic accuracy could be related to familiarity with the technique and resolution of the images. 5. Conclusions Our results thus do not support the universal use of airway fluoroscopy as a screening instrument for laryngotracheal anomalies in infants. In the absence of other resilient tools for dynamic airway imaging, we recommend rigid endoscopy as the gold standard for definitive diagnosis. With expanding ALARA standards, it is likely that exposures associated with fluoroscopy will continue to remain restricted for use in infants and young children. Other imaging modalities like ultrasound with more advanced resolution and without exposure to radiation may be an option in the future. Conflicts of interest The authors declare none. Acknowledgements None. References [1] J. Kirkpatrick, Medical applications of fluoroscopic image intensification - III, ME-6, IRE Trans. Med. Electron (1959) 82e83, http://dx.doi.org/10.1109/IRETME.1959.5007921. [2] I.G. Kim, W.M. Brummitt, A. Humphry, S.W. Siomra, W.B. Wallace, Foreign body in the airway: a review of 202 cases, Laryngoscope 83 (1973) 347e354, http://dx.doi.org/10.1288/00005537-197303000-00004. [3] P.M. Joseph, W.E. Berdon, D.H. Baker, T.L. Slovis, J.O. Haller, Upper airway obstruction in infants and small children. Improved radiographic diagnosis by combining filtration, high kilovoltage, and magnification, Radiology 121 (1976) 143e148, http://dx.doi.org/10.1148/121.1.143. [4] S.K. Fernbach, R.T. Brouillette, T.W. Riggs, C.E. Hunt, Radiologic evaluation of adenoids and tonsils in children with obstructive sleep apnea: plain films and fluoroscopy, Pediatr. Radiol. 13 (1983) 258e265, http://dx.doi.org/10.1007/
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