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Etiology and long-term functional swallow outcomes in pediatric unilateral vocal fold immobility
International Journal of Pediatric Otorhinolaryngology 88 (2016) 179e183
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
Etiology and long-term functional swallow outcomes in pediatric unilateral vocal fold immobility* Kathleen M. Tibbetts a, *, Derek Wu a, 1, Jeffrey V. Hsu a, William B. Burton b, Michel Nassar a, Melin Tan a a Department of Otorhinolaryngology-Head and Neck Surgery, Montefiore Medical Center, Albert Einstein College of Medicine, 3400 Bainbridge Avenue, 3rd Floor, Bronx, NY 10467, USA b Albert Einstein College of Medicine, Jack and Pearl Resnick Campus, 1300 Morris Park Avenue, Belfer Building, Room 206, Bronx, NY 10461, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 April 2016 Received in revised form 7 July 2016 Accepted 8 July 2016 Available online 11 July 2016
Objective: Unilateral vocal fold immobility (UVFI) results in deficits in phonatory, respiratory, and swallow function of the pediatric patient. Little is known about long-term functional swallow outcomes. Methods: Medical records of children diagnosed with UVFI between 2005 and 2014 at a tertiary children's hospital were retrospectively reviewed. Etiology, laryngoscopy findings, and swallow status at diagnosis and follow-up were recorded. Swallow outcomes were compared by etiology using Fisher's exact test. McNemar's test was used to identify correlations between return of mobility and swallow recovery. Rates of pneumonia were compared with initial swallow evaluation results using a two-tailed ttest. Results: Eighty-eight patients with UVFI were identified and 73 patients (47% female, mean age 14.4 months, standard deviation (SD) 26.7 months) had complete medical records. Mean follow up time was 52.7 months (SD 36.8 months). Etiologies included cardiothoracic surgery (68.5%), idiopathic (12.3%), prolonged intubation (11.0%), central nervous system (CNS) abnormality (5.5%), and non-cardiac iatrogenic injury to the recurrent laryngeal nerve (2.7%). Forty-seven patients underwent a follow up laryngoscopy, and recovery of vocal fold (VF) mobility was documented in 42.6% (20/47). At diagnosis, 31.5% fed orally, compared with 79.5% at follow-up. Direct correlation between recovery of VF mobility and swallow recovery was not demonstrated. Cardiac etiologies demonstrated higher rates of swallow recovery than CNS abnormalities (p ¼ 0.0393). Twenty-five children aspirated on initial modified barium swallow (MBS) and 10 children developed pneumonias at some point during the follow up period. There was no significant difference in rates of pneumonia in patients with and without aspiration on MBS. Conclusion: Recovery of swallow in children with UVFI does not directly parallel return of VF mobility. Long-term swallow outcome is favorable in this population. Initial MBS does not indicate ultimate swallow outcome. © 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Pediatric Unilateral vocal fold immobility Dysphagia Modified barium swallow Aspiration
1. Introduction Vocal fold immobility (VFI) is the second most common cause of
* This work was presented as a poster at the ASPO 2015 Spring Meeting, Boston, MA April 2015. * Corresponding author. Present address: Department of Otolaryngology-Head and Neck Surgery, University of Texas Health Science Center-San Antonio, 8300 Floyd Curl Drive, San Antonio, TX 78229, USA. E-mail address: [email protected] (K.M. Tibbetts). 1 Present address: Department of Otolaryngology, SUNY Downstate Medical Center, 450 Clarkson Avenue, Suite 126, Brooklyn, NY 11203-2056, USA.
http://dx.doi.org/10.1016/j.ijporl.2016.07.008 0165-5876/© 2016 Elsevier Ireland Ltd. All rights reserved.
neonatal stridor after laryngomalacia [1]. Patients may present with total paralysis or partial paresis of one or both vocal folds (VF). Bilateral VFI is rare, with an estimated incidence of 0.75 cases per million births per year [2]. Unilateral VFI (UVFI) is more common, with an estimated diagnosis rate of 8e25% of pediatric patients undergoing laryngoscopy for airway evaluation [3]. Multiple etiologies of VFI in the pediatric population exist, with iatrogenic causes being most common. Cardiothoracic surgery is often causative, most often due to iatrogenic injury of the left recurrent laryngeal nerve (RLN). Injury during endotracheal intubation, birth trauma, or other post-natal intervention affecting the function of the recurrent laryngeal nerve may also result in iatrogenic VFI [4]. In
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approximately 20e41% [4e8] of cases, no cause is identified and the immobility is deemed idiopathic. There are numerous studies evaluating long-term outcomes in children with VFI of various etiologies [4e13]. Reported rates of recovery of VF mobility range from 28 to 74% and vary by etiology of VFI [7,8,13]. These studies, however, focus primarily on the return of VF mobility rather than functional outcomes such as voice and swallowing. The primary aim of this study is to evaluate long-term functional swallow outcomes of pediatric patients with UVFI. We hypothesize that UVFI in the pediatric population portends a favorable prognosis for recovery of swallow function even if VF mobility does not return. We also assess the implications of the initial swallowing evaluation in children with UVFI. We hypothesize that swallow evaluation with modified barium swallow (MBS) studies at initial diagnosis of VFI can predict which children are at risk for aspiration pneumonia. We hope that the findings of this study will guide management and expectations of clinicians and caregivers of children with UVFI by providing objective data regarding the prognosis for improvement in swallow function. 2. Materials and methods
Procedure notes detailing flexible laryngoscopy findings were reviewed to determine whether VF mobility had recovered at follow up. Laryngoscopies were performed either at the bedside during inpatient encounters or in the outpatient clinic setting. All procedure notes were authored or co-signed by an attending otolaryngologist. Video of the examinations was generally not recorded and thus was not available for review. Any return of mobility in a previously immobile VF was considered recovery. 2.3. Statistical analysis Descriptive statistics were used to summarize patient demographics, functional status at initial presentation and follow up, and etiologies of VFI. Outcomes in voice and swallowing status by etiology were compared using Fisher's exact test. McNemar's test was used to identify correlations between return of mobility and recovery of voice and swallow. A two-tailed t-test was used to determine if there was a significant difference between the rates of pneumonia in children with and without aspiration on their initial swallowing evaluation.
2.1. Patient cohort
3. Results
A retrospective review of medical records of pediatric patients (age less than 18 years) diagnosed with vocal fold paresis or paralysis at our institution between 2005 and 2014 was performed with Institutional Review Board approval. Patients were identified through a search of an existing database of pediatric patients who had previously undergone airway evaluation by the Otolaryngology-Head and Neck Surgery (ORL-HNS) service. Additional patients were identified through a Clinical Looking Glass (CLG®) search of the ICD-9 codes for vocal fold paresis and paralysis (478.30e478.34) in patients less than 18 years old. CLG® is a data collection and management software tool that democratizes several of the electronic medical data systems used by the study institution and allows the user to collect demographic and outcome data for healthcare purposes [14].
Eighty-eight pediatric patients with UVFI were identified and 73 patients (53% male, 47% female) had complete medical records and were included in the analysis. Mean age at diagnosis was 14.4 months (standard deviation (SD) 27.6 months), and mean followup time was 52.7 months (SD 36.8 months). Patients had an average of 2.5 follow up encounters (SD 1.3) during the study period. Etiologies of UVFI were cardiothoracic surgery (68.5%), idiopathic (12.3%), prolonged intubation (11.0%), central nervous system (CNS) disorders (5.5%), and other iatrogenic injury to the RLN (2.7%). Patient demographics are displayed in Table 1. Fortyseven patients underwent a follow up laryngoscopy, and recovery of vocal fold (VF) mobility was documented in 42.6% (20/47). Twenty-six patients did not undergo a follow up laryngoscopy (Table 2). At diagnosis, 31.5% (23/73) fed orally, 8 were receiving total parenteral nutrition (TPN), and the remaining patients required a feeding tube. Patients receiving TPN were premature and at risk for or had been diagnosed with gastrointestinal complications of prematurity such as necrotizing enterocolitis, and were thus unable to receive enteral feeds. At most recent follow-up, 79.5% (58/73) were feeding orally (Table 3) and improving or
2.2. Data collected and outcomes measured Existing electronic medical records were reviewed and data pertaining to basic demographics, nature of VFI (left, right, or bilateral; total paralysis or paresis), neonatal history (prematurity, cardiac surgery, intubation, tracheotomy, other comorbidities), and etiology of VFI were collected. Data regarding patients' functional impairment (abnormalities in voice, breathing, and feeding) at the time of diagnosis and at most recent follow up were also obtained. Data pertaining to voice and swallowing status was obtained by reviewing documentation from inpatient and outpatient encounters with the pediatric ORL-HNS service, speech language pathologists, and patients' general pediatricians and other specialty physicians. Patients who were fed both via feeding tube and orally were considered to be feeding by mouth in the analysis. MBS results as well as whether aspiration pneumonia occurred and the time of diagnosis were recorded as well. All MBS studies were performed and interpreted by 1 of 5 Speech Language Pathologists (SLP) at the study institution in conjunction with the Radiology service. SLP documentation of the MBS was reviewed to determine whether aspiration occurred during the study. A binary system was employed (presence or absence of aspiration). Voice outcomes were determined through reviewing descriptions of vocal quality in documentation by either an otolaryngologist, SLP, general pediatrician, or other clinician. Objective voice measures or subjective questionnaires were not applied.
Table 1 Patient demographics. Etiology
Sex
Age at diagnosis (Months)
Cardiothoracic surgery (n ¼ 50)
29 Female 21 Male
Idiopathic (n ¼ 9)
3 Female 6 Male
Prolonged intubation (n ¼ 8)
1 Female 7 Male
CNS disorder (n ¼ 4)
1 Female 3 Male
Other RLN injury (n ¼ 2)
0 Female 2 Male
All (n ¼ 73)
34 Female 39 Male
Mean: 10.5 Range: 1e68 SD: 14.9 Mean: 10.2 Range: 0.6e25 SD: 20.3 Mean: 23.8 Range: 1e140 SD: 48.1 Mean: 56.4 Range: 1e124 SD: 63.3 Mean: 9.9 Range: 5.7e14.1 SD: 6 Mean: 14.4 Range: 0.6e140 SD: 26.7
SD ¼ Standard deviation.
K.M. Tibbetts et al. / International Journal of Pediatric Otorhinolaryngology 88 (2016) 179e183
181
Table 2 Status of vocal fold mobility at follow up. Etiology
Recovered
Immobile
No follow up Laryngoscopy
Cardiothoracic surgery (n ¼ 50) Idiopathic (n ¼ 9) Prolonged intubation (n ¼ 8) CNS disorder (n ¼ 4) Other RLN injury (n ¼ 2) All (n ¼ 73)
12/50 (24%) 4/9 (44.4%) 3/8 (37.5%) 1/4 (25%) N/A 20/73 (27.4%)
22/50 (44%) 0/9 (0%) 4/8 (50%) 1/4 (25%) N/A 27/73 (36.9%)
16/50 (32%) 5/9 (55.5%) 1/8 (12.5%) 2/4 (50%) 2/2 (100%) 26/73 (35.6%)
Table 3 Feeding status at diagnosis and follow up. Etiology Cardiothoracic surgery N ¼ 50 Idiopathic n ¼ 9 Prolonged intubation n ¼ 8 CNS disorder n ¼ 4 Other RLN injury n ¼ 2 All n ¼ 73 a
Oral Tube Oral Tube Oral Tube Oral Tube Oral Tube Oral Tube
fed fed fed fed fed fed
Feeding status at diagnosisa
Feeding status at follow-upa
15/50 (30%) 32/50 (64%) 5/9 (56.6%) 4/9 (44%) 2/8 (25%) 3/8 (37.5%) 0/4 (0%) 3/4 (75%) 2/2 (100%) 0/2 (0%) 23/73 (31.5%) 42/73 (57%)
40/50 (80%) 9/50 (18%) 8/9 (88.8%) 1/9 (11.1%) 6/8 (75%) 1/8 (12.5%) 2/4 (50%) 2/4 (50%) 2/2 (100%) 0/2 (0%) 58/73 (79.5%) 13/73 (17%)
Patients receiving total parenteral nutrition (TPN) not included in analysis.
normal voice was documented in 42.5% of patients. A direct correlation between recovery of VF mobility on laryngoscopy and recovery of swallow function was not demonstrated (Table 4). There was no significant difference in age at diagnosis of UVFI between patients who recovered mobility and those who did not (p ¼ 0.56). There was also no significant difference in the age of diagnosis and recovery of swallow function (p ¼ 0.59). There were no significant differences in the rates of recovery of VF mobility among the different etiologies (p > 0.05). However, there was a statistically significant difference in rate of recovery of swallow function between patients with UVFI due to cardiac surgery and due to CNS abnormalities (80% versus 25%, p ¼ 0.0393). Of the 73 children with UVFI, 36 had a documented swallow evaluation after initial diagnosis. Twenty-five children in this cohort (69.4%) had documented aspiration during the initial swallow evaluation with MBS. Patients who passed the initial MBS (no aspiration) did not undergo follow up MBS; patients who aspirated typically underwent additional studies, with an average of 2.3 total MBS studies (SD 0.4). Ten children went on to develop pneumonias at some point during the follow up period (8 with aspiration seen on MBS) (Table 5). The average time to development of pneumonia after the initial MBS was 15.7 months (SD 13 months). There was no significant difference in rates of pneumonia in patients who did and did not aspirate on MBS (p ¼ 0.38). Of the children who developed pneumonias, 7 were fed via feeding tube at the time of the illness. 4. Discussion Pediatric VFI has been well described in the literature with varying lengths of follow up and documentation of long-term
outcomes regarding the recovery of VF function. Spontaneous recovery of VF mobility has been shown to occur, and prognosis varies with etiology. The largest study available was performed by Jabbour et al., demonstrating an overall rate of recovery of VF mobility in 28% in a cohort of 404 pediatric patients with unilateral and bilateral VFI of various etiologies (cardiac surgery, idiopathic, and neurologic) [13]. Other studies have focused on recovery rates by etiology of VFI. de Gaudemar et al. showed an overall 73% rate of spontaneous recovery of VF mobility in a study of 113 patients with congenital VFI. In this study, 70% of patients with neurologic etiologies and 74% of idiopathic cases recovered spontaneously [8]. Daya et al. also demonstrated favorable recover rates in patients with neurologic etiologies and idiopathic VFI. They identified 102 patients with both bilateral and unilateral VFI and found a 71% rate of spontaneous recovery within 2 years in children with a neurologic etiology. Sixty-four percent of children with idiopathic VFI recovered spontaneously, over a range of 6 monthse11 years [7]. The most frequent etiology of UVFI in our population was iatrogenic injury during cardiothoracic surgery. This was not surprising given our study setting, a tertiary children's hospital with an active cardiothoracic surgery service and a high volume of infants with cardiac defects requiring repair. We found an overall rate of recovery of VF mobility in 27.4% in our population, with patients with idiopathic UVFP showing the best rates of recovery of mobility (44.4%). Iatrogenic injury during cardiothoracic surgery portended the worst prognosis for return of VF function (24%), suggesting a more permanent surgical injury to the RLN. Reported rates of recovery of VF mobility after cardiothoracic surgery vary widely, however, with published rates ranging from 0 to 82% [5,6,10e12]. The discrepancies in published rates of recovery of VF mobility after
Table 4 Relationship between recovery of vocal fold mobility and swallowing status in all UVFI patients with documented follow up laryngoscopy.
Recovery in VF mobility on Laryngoscopy No recovery in VF mobility on Laryngoscopy VF ¼ vocal fold.
Recovery of swallow (oral intake)
No recovery of swallow (feeding tube)
19.1% (9/47) 46.8% (22/47)
4.3% (2/47) 32% (15/47)
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Table 5 Relationships between results of swallow evaluation with MBS and incidence of aspiration pneumonia in children with UVFI.
þPneumonia Pneumonia Total
þAspiration on MBS
Aspiration on MBS
Total
8 17 25
2 9 11
10 26 36
MBS ¼ modified barium swallow.
cardiothoracic surgery may be related to length of follow up and additional characteristics of the patient population, such as rates of prematurity and other comorbidities. It is well accepted that infants with UVFI often have concomitant compromises in ability to swallow. Infant swallow is complex, involving multiple oropharyngeal structures in addition to the larynx. The degree to which a recurrent laryngeal nerve injury can adversely affect the overall swallow function is impacted by the integrity of the other components of the swallow mechanism. In our study, we sought to go beyond determining the rates of recovery of VF mobility and evaluate the long-term functional swallowing outcomes of children with UVFI. We sought to answer the question of whether the child will ultimately be able to eat normally despite having UVFI. In our study population, all etiologies of UVFI showed improvements in swallowing status. Overall, 79.5% of patients were feeding orally at most recent follow up, compared to 31.5% at initial diagnosis. We did not find a direct correlation between recovery VF mobility and recovery of swallowing function; rates of recovery of swallow function surpassed rates of return of mobility. This suggests that normal swallowing function can be achieved even if VF mobility does not return. Presumably, other components of the swallowing mechanisms are able to compensate for an immobile vocal fold to achieve an effective swallow. This has been previously demonstrated in the literature: Nichols et al. found that 73% of patients with UVFI were feeding orally at most recent follow up compared to 45% at presentation, despite only 3% of patients recovering vocal fold mobility [12]. Additionally, in a study of 404 pediatric patients with unilateral and bilateral VFI of various etiologies (cardiac surgery, idiopathic, and neurologic), Jabbour et al. found an overall rate of recovery of VF mobility of 28%, but noted that 45.8% of patients had resolution of their presenting symptoms at most recent follow up [13]. While there were no significant differences between rates of recovery of VF mobility between the different etiologies, again we note that those with UVFI secondary to iatrogenic injury had the lowest rate of return. However, in our study, there was a statistically significant higher rate of recovery of swallow function comparing patients with iatrogenic injury due to cardiothoracic surgery and those with CNS abnormalities. This may be due to more global neurologic problems rendering those with CNS abnormalities less able to compensate than those patients with isolated RLN injury due to surgical injury. There was no significant association in the rates of pneumonia in patients with UVFI who did and did not aspirate on swallow evaluation by MBS. This suggests that even children who do not demonstrate aspiration on MBS may still be at elevated risk for episodes of aspiration. Therefore, caregivers should monitor infants and children with UVFI for signs and symptoms of aspiration and pneumonia such as coughing or choking while eating, tachypnea, shortness of breath, and fever. Additionally, several children who were fed via feeding tube developed pneumonias. This could be due to aspiration after episodes of regurgitation of feeds [15] or simply aspiration of secretions. Although we did not find MBS to be consistently predictive of pneumonia risk in our study population, it is still an essential part of the work up of children with UVFI and dysphagia in general as it can help identify strategies to manage
dysphagia and prevent aspiration, such as altering the rate of feeding and textures of feeds [16]. Ultimate swallow function in the long term may be improved despite return of vocal fold mobility because oropharyngeal and contralateral laryngeal mechanisms may compensate sufficiently and as infants grow, they transition from a supine feeding position to a more upright one which may be favorable for them. This study benefits from an extended follow up time, contrasted with some prior studies that have followed patients for less than one year [3,6,7]. We also provide data regarding the long-term functional outcomes of multiple etiologies of UVFI. This information can guide the expectations clinicians as well as counsel families of patients with UVFI with respect to prognosis for functional recovery. This study has the limitations of a retrospective review including a lack of uniformity in follow-up laryngoscopy and objective data collection for voice and swallow. The children who did not undergo repeat laryngoscopy either did not follow up with the pediatric ORL-HNS service, or the otolaryngologist opted not to perform a laryngoscopy at follow up. Those children who did not follow up with pediatric ORL-HNS were documented to be asymptomatic with respect to their previously diagnosed UVFI by other clinicians. In those cases, documentation from these other clinicians caring for the child was used to gather data regarding functional swallow and voice outcomes. The patients who did follow up with the pediatric ORL-HNS service underwent repeat laryngoscopy at the discretion of the attending otolaryngologist; laryngoscopy may have been deferred if the child was asymptomatic. While the lack of complete data regarding return of mobility on laryngoscopy limits our ability to draw definite conclusions regarding the relationship between return of mobility and recovery of swallow function, we can still infer overall prognosis of swallow function based on the available clinical documentation. Another weakness of the study is that interpretation of the MBS studies was not standardized. Given that this was a retrospective review spanning a 9 year period, the MBS studies were performed and interpreted by 5 different SLPs who worked in the department at some point during that time period. The fluoroscopy images and video were not available for review in all the patients who underwent MBS, and therefore we opted to rely on the SLP documentation to determine whether or not aspiration occurred. The authors felt that using a binary system of interpretation (aspiration versus no aspiration) of the MBS studies would reduce confounding by eliminating other variations between the reads of the 5 SLPs. With respect to voice outcomes, we are limited by a lack of objective voice measures or subjective questionnaire data. At our institution, such instruments are not routinely applied to the pediatric population. Again, we rely on subjective documentation of patients' voice quality from clinical documentation and thus are unable to draw strong conclusions regarding functional voice outcomes in children with UVFI. A prospective study of children with UVFI employing objective voice measures, quality of life questionnaires, modified barium swallow, and laryngoscopy could further elucidate the long-term functional voice and swallowing outcomes in these children. 5. Conclusion VFI, while relatively rare in the general population, is the second most common cause of neonatal stridor and can cause serious deficits in the phonatory, respiratory, and swallowing functions of the pediatric patient. Several etiologies exist, with varying prognoses for recovery of function. In this study, we focused not only on rates of recovery of VF mobility in children with UVFI, but also on patients' long-term swallowing status. Based on our data, we conclude that while VF immobility can have a deleterious impact on
K.M. Tibbetts et al. / International Journal of Pediatric Otorhinolaryngology 88 (2016) 179e183
swallowing function initially, but with time patients are able to compensate and improve their swallowing function even if VF mobility does not return. MBS is an invaluable tool for identifying children at risk for aspiration and in the development of feeding strategies in children with dysphagia, but may not reliably indicate ultimate swallowing outcome.
[9]
[10]
[11]
References [1] P.H. Holinger, Clinical aspects of congenital anomalies of the larynx, trachea, bronchi, and oesophagus, J. Laryngol. Otol. 75 (1961) 1e44. [2] G.E. Murty, C. Shinkwin, K.P. Gibbin, Bilateral vocal fold paralysis in infants: tracheostomy or not? J. Laryngol. Otol. 108 (1994) 329e331. [3] S.R. Parikh, Paediatric unilateral vocal fold immobility, Otolaryngol. Clin. North Am. 37 (2004) 203e215. [4] N. Grover, A. Bhattacharyya, Unilateral pediatric vocal cord paralysis: evolving trends, J. Laryngol. Voice 2 (2012) 5e9. [5] K.D. Pereira, B.D. Webb, M.L. Blakely, C.S. Cox Jr., K.P. Lally, Sequelae of recurrent laryngeal nerve injury after patent ductus arteriosus ligation, Int. J. Pediatr. Otorhinolaryngol. 70 (9) (2006 Sep) 1609e1612. [6] R.I. Zbar, R.J. Smith, Vocal fold paralysis in infants twelve months of age and younger, Otolaryngol. Head. Neck Surg. 114 (1996) 18e21. [7] H. Daya, A. Hosni, I. Bejar-Solar, J.N. Evans, C.M. Bailey, Pediatric vocal fold paralysis: a long-term retrospective study, Arch. Otolaryngol. Head. Neck Surg. 126 (2000) 21e25. [8] I. de Gaudemar, M. Roudaire, M. Francois, P. Narcy, Outcome of laryngeal
[12]
[13]
[14]
[15] [16]
183
paralysis in neonates: a long term retrospective study of 113 cases, Int. J. Pediatr. Otorhinolaryngol. 34 (1996) 101e110. R.C. Miyamoto, S.R. Parikh, W. Gellad, G.R. Licameli, Bilateral congenital vocal cord paralysis: a 16-year institutional review, Otolaryngol. Head. Neck Surg. 133 (2) (2005 Aug) 241e245. S.S. Khariwala, W.T. Lee, P.J. Koltai, Laryngotracheal consequences of pediatric cardiac surgery, Arch. Otolaryngol. Head. Neck Surg. 131 (4) (2005 Apr) 336e339. M.T. Truong, A.H. Messner, J.E. Kerschner, M. Scholes, J. Wong-Dominguez, H.A. Milczuk, P.J. Yoon, Pediatric vocal fold paralysis after cardiac surgery: rate of recovery and sequelae, Otolaryngol. Head. Neck Surg. 137 (5) (2007 Nov) 780e784. B.G. Nichols, J. Jabbour, D.A. Hehir, N.S. Ghanayem, D. Beste, T. Martin, R. Woods, T. Robey, Recovery of vocal fold immobility following isolated patent ductus arteriosus ligation, Int. J. Pediatr. Otorhinolaryngol. 78 (8) (2014 Aug) 1316e1319. J. Jabbour, T. Martin, D. Beste, T. Robey, Pediatric vocal fold immobility: natural history and the need for long-term follow-up, JAMA Otolaryngol. Head. Neck Surg. 140 (5) (2014 May) 428e433. E. Bellin, D.D. Fletcher, Islam S. Geberern, N. Srivastava, Democratizing information creation from health care data for quality improvement, research, and education-the Montefiore medical experience, Acad. Med. 85 (2010) 1362e1368. B. Rogers, J. Arvedson, G. Buck, P. Smart, M. Msall, Characteristics of dysphagia in children with cerebral palsy, Dysphagia 9 (1) (1994) 69e73. Winter. J. Arvedson, B. Rogers, G. Buck, P. Smart, M. Msall, Silent aspiration prominent in children with dysphagia, Int. J. Pediatr. Otorhinolaryngol. 28 (2e3) (1994 Jan) 173e181.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: http://www.ijporlonline.com/
Etiology and long-term functional swallow outcomes in pediatric unilateral vocal fold immobility* Kathleen M. Tibbetts a, *, Derek Wu a, 1, Jeffrey V. Hsu a, William B. Burton b, Michel Nassar a, Melin Tan a a Department of Otorhinolaryngology-Head and Neck Surgery, Montefiore Medical Center, Albert Einstein College of Medicine, 3400 Bainbridge Avenue, 3rd Floor, Bronx, NY 10467, USA b Albert Einstein College of Medicine, Jack and Pearl Resnick Campus, 1300 Morris Park Avenue, Belfer Building, Room 206, Bronx, NY 10461, USA
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 April 2016 Received in revised form 7 July 2016 Accepted 8 July 2016 Available online 11 July 2016
Objective: Unilateral vocal fold immobility (UVFI) results in deficits in phonatory, respiratory, and swallow function of the pediatric patient. Little is known about long-term functional swallow outcomes. Methods: Medical records of children diagnosed with UVFI between 2005 and 2014 at a tertiary children's hospital were retrospectively reviewed. Etiology, laryngoscopy findings, and swallow status at diagnosis and follow-up were recorded. Swallow outcomes were compared by etiology using Fisher's exact test. McNemar's test was used to identify correlations between return of mobility and swallow recovery. Rates of pneumonia were compared with initial swallow evaluation results using a two-tailed ttest. Results: Eighty-eight patients with UVFI were identified and 73 patients (47% female, mean age 14.4 months, standard deviation (SD) 26.7 months) had complete medical records. Mean follow up time was 52.7 months (SD 36.8 months). Etiologies included cardiothoracic surgery (68.5%), idiopathic (12.3%), prolonged intubation (11.0%), central nervous system (CNS) abnormality (5.5%), and non-cardiac iatrogenic injury to the recurrent laryngeal nerve (2.7%). Forty-seven patients underwent a follow up laryngoscopy, and recovery of vocal fold (VF) mobility was documented in 42.6% (20/47). At diagnosis, 31.5% fed orally, compared with 79.5% at follow-up. Direct correlation between recovery of VF mobility and swallow recovery was not demonstrated. Cardiac etiologies demonstrated higher rates of swallow recovery than CNS abnormalities (p ¼ 0.0393). Twenty-five children aspirated on initial modified barium swallow (MBS) and 10 children developed pneumonias at some point during the follow up period. There was no significant difference in rates of pneumonia in patients with and without aspiration on MBS. Conclusion: Recovery of swallow in children with UVFI does not directly parallel return of VF mobility. Long-term swallow outcome is favorable in this population. Initial MBS does not indicate ultimate swallow outcome. © 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Pediatric Unilateral vocal fold immobility Dysphagia Modified barium swallow Aspiration
1. Introduction Vocal fold immobility (VFI) is the second most common cause of
* This work was presented as a poster at the ASPO 2015 Spring Meeting, Boston, MA April 2015. * Corresponding author. Present address: Department of Otolaryngology-Head and Neck Surgery, University of Texas Health Science Center-San Antonio, 8300 Floyd Curl Drive, San Antonio, TX 78229, USA. E-mail address: [email protected] (K.M. Tibbetts). 1 Present address: Department of Otolaryngology, SUNY Downstate Medical Center, 450 Clarkson Avenue, Suite 126, Brooklyn, NY 11203-2056, USA.
http://dx.doi.org/10.1016/j.ijporl.2016.07.008 0165-5876/© 2016 Elsevier Ireland Ltd. All rights reserved.
neonatal stridor after laryngomalacia [1]. Patients may present with total paralysis or partial paresis of one or both vocal folds (VF). Bilateral VFI is rare, with an estimated incidence of 0.75 cases per million births per year [2]. Unilateral VFI (UVFI) is more common, with an estimated diagnosis rate of 8e25% of pediatric patients undergoing laryngoscopy for airway evaluation [3]. Multiple etiologies of VFI in the pediatric population exist, with iatrogenic causes being most common. Cardiothoracic surgery is often causative, most often due to iatrogenic injury of the left recurrent laryngeal nerve (RLN). Injury during endotracheal intubation, birth trauma, or other post-natal intervention affecting the function of the recurrent laryngeal nerve may also result in iatrogenic VFI [4]. In
180
K.M. Tibbetts et al. / International Journal of Pediatric Otorhinolaryngology 88 (2016) 179e183
approximately 20e41% [4e8] of cases, no cause is identified and the immobility is deemed idiopathic. There are numerous studies evaluating long-term outcomes in children with VFI of various etiologies [4e13]. Reported rates of recovery of VF mobility range from 28 to 74% and vary by etiology of VFI [7,8,13]. These studies, however, focus primarily on the return of VF mobility rather than functional outcomes such as voice and swallowing. The primary aim of this study is to evaluate long-term functional swallow outcomes of pediatric patients with UVFI. We hypothesize that UVFI in the pediatric population portends a favorable prognosis for recovery of swallow function even if VF mobility does not return. We also assess the implications of the initial swallowing evaluation in children with UVFI. We hypothesize that swallow evaluation with modified barium swallow (MBS) studies at initial diagnosis of VFI can predict which children are at risk for aspiration pneumonia. We hope that the findings of this study will guide management and expectations of clinicians and caregivers of children with UVFI by providing objective data regarding the prognosis for improvement in swallow function. 2. Materials and methods
Procedure notes detailing flexible laryngoscopy findings were reviewed to determine whether VF mobility had recovered at follow up. Laryngoscopies were performed either at the bedside during inpatient encounters or in the outpatient clinic setting. All procedure notes were authored or co-signed by an attending otolaryngologist. Video of the examinations was generally not recorded and thus was not available for review. Any return of mobility in a previously immobile VF was considered recovery. 2.3. Statistical analysis Descriptive statistics were used to summarize patient demographics, functional status at initial presentation and follow up, and etiologies of VFI. Outcomes in voice and swallowing status by etiology were compared using Fisher's exact test. McNemar's test was used to identify correlations between return of mobility and recovery of voice and swallow. A two-tailed t-test was used to determine if there was a significant difference between the rates of pneumonia in children with and without aspiration on their initial swallowing evaluation.
2.1. Patient cohort
3. Results
A retrospective review of medical records of pediatric patients (age less than 18 years) diagnosed with vocal fold paresis or paralysis at our institution between 2005 and 2014 was performed with Institutional Review Board approval. Patients were identified through a search of an existing database of pediatric patients who had previously undergone airway evaluation by the Otolaryngology-Head and Neck Surgery (ORL-HNS) service. Additional patients were identified through a Clinical Looking Glass (CLG®) search of the ICD-9 codes for vocal fold paresis and paralysis (478.30e478.34) in patients less than 18 years old. CLG® is a data collection and management software tool that democratizes several of the electronic medical data systems used by the study institution and allows the user to collect demographic and outcome data for healthcare purposes [14].
Eighty-eight pediatric patients with UVFI were identified and 73 patients (53% male, 47% female) had complete medical records and were included in the analysis. Mean age at diagnosis was 14.4 months (standard deviation (SD) 27.6 months), and mean followup time was 52.7 months (SD 36.8 months). Patients had an average of 2.5 follow up encounters (SD 1.3) during the study period. Etiologies of UVFI were cardiothoracic surgery (68.5%), idiopathic (12.3%), prolonged intubation (11.0%), central nervous system (CNS) disorders (5.5%), and other iatrogenic injury to the RLN (2.7%). Patient demographics are displayed in Table 1. Fortyseven patients underwent a follow up laryngoscopy, and recovery of vocal fold (VF) mobility was documented in 42.6% (20/47). Twenty-six patients did not undergo a follow up laryngoscopy (Table 2). At diagnosis, 31.5% (23/73) fed orally, 8 were receiving total parenteral nutrition (TPN), and the remaining patients required a feeding tube. Patients receiving TPN were premature and at risk for or had been diagnosed with gastrointestinal complications of prematurity such as necrotizing enterocolitis, and were thus unable to receive enteral feeds. At most recent follow-up, 79.5% (58/73) were feeding orally (Table 3) and improving or
2.2. Data collected and outcomes measured Existing electronic medical records were reviewed and data pertaining to basic demographics, nature of VFI (left, right, or bilateral; total paralysis or paresis), neonatal history (prematurity, cardiac surgery, intubation, tracheotomy, other comorbidities), and etiology of VFI were collected. Data regarding patients' functional impairment (abnormalities in voice, breathing, and feeding) at the time of diagnosis and at most recent follow up were also obtained. Data pertaining to voice and swallowing status was obtained by reviewing documentation from inpatient and outpatient encounters with the pediatric ORL-HNS service, speech language pathologists, and patients' general pediatricians and other specialty physicians. Patients who were fed both via feeding tube and orally were considered to be feeding by mouth in the analysis. MBS results as well as whether aspiration pneumonia occurred and the time of diagnosis were recorded as well. All MBS studies were performed and interpreted by 1 of 5 Speech Language Pathologists (SLP) at the study institution in conjunction with the Radiology service. SLP documentation of the MBS was reviewed to determine whether aspiration occurred during the study. A binary system was employed (presence or absence of aspiration). Voice outcomes were determined through reviewing descriptions of vocal quality in documentation by either an otolaryngologist, SLP, general pediatrician, or other clinician. Objective voice measures or subjective questionnaires were not applied.
Table 1 Patient demographics. Etiology
Sex
Age at diagnosis (Months)
Cardiothoracic surgery (n ¼ 50)
29 Female 21 Male
Idiopathic (n ¼ 9)
3 Female 6 Male
Prolonged intubation (n ¼ 8)
1 Female 7 Male
CNS disorder (n ¼ 4)
1 Female 3 Male
Other RLN injury (n ¼ 2)
0 Female 2 Male
All (n ¼ 73)
34 Female 39 Male
Mean: 10.5 Range: 1e68 SD: 14.9 Mean: 10.2 Range: 0.6e25 SD: 20.3 Mean: 23.8 Range: 1e140 SD: 48.1 Mean: 56.4 Range: 1e124 SD: 63.3 Mean: 9.9 Range: 5.7e14.1 SD: 6 Mean: 14.4 Range: 0.6e140 SD: 26.7
SD ¼ Standard deviation.
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Table 2 Status of vocal fold mobility at follow up. Etiology
Recovered
Immobile
No follow up Laryngoscopy
Cardiothoracic surgery (n ¼ 50) Idiopathic (n ¼ 9) Prolonged intubation (n ¼ 8) CNS disorder (n ¼ 4) Other RLN injury (n ¼ 2) All (n ¼ 73)
12/50 (24%) 4/9 (44.4%) 3/8 (37.5%) 1/4 (25%) N/A 20/73 (27.4%)
22/50 (44%) 0/9 (0%) 4/8 (50%) 1/4 (25%) N/A 27/73 (36.9%)
16/50 (32%) 5/9 (55.5%) 1/8 (12.5%) 2/4 (50%) 2/2 (100%) 26/73 (35.6%)
Table 3 Feeding status at diagnosis and follow up. Etiology Cardiothoracic surgery N ¼ 50 Idiopathic n ¼ 9 Prolonged intubation n ¼ 8 CNS disorder n ¼ 4 Other RLN injury n ¼ 2 All n ¼ 73 a
Oral Tube Oral Tube Oral Tube Oral Tube Oral Tube Oral Tube
fed fed fed fed fed fed
Feeding status at diagnosisa
Feeding status at follow-upa
15/50 (30%) 32/50 (64%) 5/9 (56.6%) 4/9 (44%) 2/8 (25%) 3/8 (37.5%) 0/4 (0%) 3/4 (75%) 2/2 (100%) 0/2 (0%) 23/73 (31.5%) 42/73 (57%)
40/50 (80%) 9/50 (18%) 8/9 (88.8%) 1/9 (11.1%) 6/8 (75%) 1/8 (12.5%) 2/4 (50%) 2/4 (50%) 2/2 (100%) 0/2 (0%) 58/73 (79.5%) 13/73 (17%)
Patients receiving total parenteral nutrition (TPN) not included in analysis.
normal voice was documented in 42.5% of patients. A direct correlation between recovery of VF mobility on laryngoscopy and recovery of swallow function was not demonstrated (Table 4). There was no significant difference in age at diagnosis of UVFI between patients who recovered mobility and those who did not (p ¼ 0.56). There was also no significant difference in the age of diagnosis and recovery of swallow function (p ¼ 0.59). There were no significant differences in the rates of recovery of VF mobility among the different etiologies (p > 0.05). However, there was a statistically significant difference in rate of recovery of swallow function between patients with UVFI due to cardiac surgery and due to CNS abnormalities (80% versus 25%, p ¼ 0.0393). Of the 73 children with UVFI, 36 had a documented swallow evaluation after initial diagnosis. Twenty-five children in this cohort (69.4%) had documented aspiration during the initial swallow evaluation with MBS. Patients who passed the initial MBS (no aspiration) did not undergo follow up MBS; patients who aspirated typically underwent additional studies, with an average of 2.3 total MBS studies (SD 0.4). Ten children went on to develop pneumonias at some point during the follow up period (8 with aspiration seen on MBS) (Table 5). The average time to development of pneumonia after the initial MBS was 15.7 months (SD 13 months). There was no significant difference in rates of pneumonia in patients who did and did not aspirate on MBS (p ¼ 0.38). Of the children who developed pneumonias, 7 were fed via feeding tube at the time of the illness. 4. Discussion Pediatric VFI has been well described in the literature with varying lengths of follow up and documentation of long-term
outcomes regarding the recovery of VF function. Spontaneous recovery of VF mobility has been shown to occur, and prognosis varies with etiology. The largest study available was performed by Jabbour et al., demonstrating an overall rate of recovery of VF mobility in 28% in a cohort of 404 pediatric patients with unilateral and bilateral VFI of various etiologies (cardiac surgery, idiopathic, and neurologic) [13]. Other studies have focused on recovery rates by etiology of VFI. de Gaudemar et al. showed an overall 73% rate of spontaneous recovery of VF mobility in a study of 113 patients with congenital VFI. In this study, 70% of patients with neurologic etiologies and 74% of idiopathic cases recovered spontaneously [8]. Daya et al. also demonstrated favorable recover rates in patients with neurologic etiologies and idiopathic VFI. They identified 102 patients with both bilateral and unilateral VFI and found a 71% rate of spontaneous recovery within 2 years in children with a neurologic etiology. Sixty-four percent of children with idiopathic VFI recovered spontaneously, over a range of 6 monthse11 years [7]. The most frequent etiology of UVFI in our population was iatrogenic injury during cardiothoracic surgery. This was not surprising given our study setting, a tertiary children's hospital with an active cardiothoracic surgery service and a high volume of infants with cardiac defects requiring repair. We found an overall rate of recovery of VF mobility in 27.4% in our population, with patients with idiopathic UVFP showing the best rates of recovery of mobility (44.4%). Iatrogenic injury during cardiothoracic surgery portended the worst prognosis for return of VF function (24%), suggesting a more permanent surgical injury to the RLN. Reported rates of recovery of VF mobility after cardiothoracic surgery vary widely, however, with published rates ranging from 0 to 82% [5,6,10e12]. The discrepancies in published rates of recovery of VF mobility after
Table 4 Relationship between recovery of vocal fold mobility and swallowing status in all UVFI patients with documented follow up laryngoscopy.
Recovery in VF mobility on Laryngoscopy No recovery in VF mobility on Laryngoscopy VF ¼ vocal fold.
Recovery of swallow (oral intake)
No recovery of swallow (feeding tube)
19.1% (9/47) 46.8% (22/47)
4.3% (2/47) 32% (15/47)
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Table 5 Relationships between results of swallow evaluation with MBS and incidence of aspiration pneumonia in children with UVFI.
þPneumonia Pneumonia Total
þAspiration on MBS
Aspiration on MBS
Total
8 17 25
2 9 11
10 26 36
MBS ¼ modified barium swallow.
cardiothoracic surgery may be related to length of follow up and additional characteristics of the patient population, such as rates of prematurity and other comorbidities. It is well accepted that infants with UVFI often have concomitant compromises in ability to swallow. Infant swallow is complex, involving multiple oropharyngeal structures in addition to the larynx. The degree to which a recurrent laryngeal nerve injury can adversely affect the overall swallow function is impacted by the integrity of the other components of the swallow mechanism. In our study, we sought to go beyond determining the rates of recovery of VF mobility and evaluate the long-term functional swallowing outcomes of children with UVFI. We sought to answer the question of whether the child will ultimately be able to eat normally despite having UVFI. In our study population, all etiologies of UVFI showed improvements in swallowing status. Overall, 79.5% of patients were feeding orally at most recent follow up, compared to 31.5% at initial diagnosis. We did not find a direct correlation between recovery VF mobility and recovery of swallowing function; rates of recovery of swallow function surpassed rates of return of mobility. This suggests that normal swallowing function can be achieved even if VF mobility does not return. Presumably, other components of the swallowing mechanisms are able to compensate for an immobile vocal fold to achieve an effective swallow. This has been previously demonstrated in the literature: Nichols et al. found that 73% of patients with UVFI were feeding orally at most recent follow up compared to 45% at presentation, despite only 3% of patients recovering vocal fold mobility [12]. Additionally, in a study of 404 pediatric patients with unilateral and bilateral VFI of various etiologies (cardiac surgery, idiopathic, and neurologic), Jabbour et al. found an overall rate of recovery of VF mobility of 28%, but noted that 45.8% of patients had resolution of their presenting symptoms at most recent follow up [13]. While there were no significant differences between rates of recovery of VF mobility between the different etiologies, again we note that those with UVFI secondary to iatrogenic injury had the lowest rate of return. However, in our study, there was a statistically significant higher rate of recovery of swallow function comparing patients with iatrogenic injury due to cardiothoracic surgery and those with CNS abnormalities. This may be due to more global neurologic problems rendering those with CNS abnormalities less able to compensate than those patients with isolated RLN injury due to surgical injury. There was no significant association in the rates of pneumonia in patients with UVFI who did and did not aspirate on swallow evaluation by MBS. This suggests that even children who do not demonstrate aspiration on MBS may still be at elevated risk for episodes of aspiration. Therefore, caregivers should monitor infants and children with UVFI for signs and symptoms of aspiration and pneumonia such as coughing or choking while eating, tachypnea, shortness of breath, and fever. Additionally, several children who were fed via feeding tube developed pneumonias. This could be due to aspiration after episodes of regurgitation of feeds [15] or simply aspiration of secretions. Although we did not find MBS to be consistently predictive of pneumonia risk in our study population, it is still an essential part of the work up of children with UVFI and dysphagia in general as it can help identify strategies to manage
dysphagia and prevent aspiration, such as altering the rate of feeding and textures of feeds [16]. Ultimate swallow function in the long term may be improved despite return of vocal fold mobility because oropharyngeal and contralateral laryngeal mechanisms may compensate sufficiently and as infants grow, they transition from a supine feeding position to a more upright one which may be favorable for them. This study benefits from an extended follow up time, contrasted with some prior studies that have followed patients for less than one year [3,6,7]. We also provide data regarding the long-term functional outcomes of multiple etiologies of UVFI. This information can guide the expectations clinicians as well as counsel families of patients with UVFI with respect to prognosis for functional recovery. This study has the limitations of a retrospective review including a lack of uniformity in follow-up laryngoscopy and objective data collection for voice and swallow. The children who did not undergo repeat laryngoscopy either did not follow up with the pediatric ORL-HNS service, or the otolaryngologist opted not to perform a laryngoscopy at follow up. Those children who did not follow up with pediatric ORL-HNS were documented to be asymptomatic with respect to their previously diagnosed UVFI by other clinicians. In those cases, documentation from these other clinicians caring for the child was used to gather data regarding functional swallow and voice outcomes. The patients who did follow up with the pediatric ORL-HNS service underwent repeat laryngoscopy at the discretion of the attending otolaryngologist; laryngoscopy may have been deferred if the child was asymptomatic. While the lack of complete data regarding return of mobility on laryngoscopy limits our ability to draw definite conclusions regarding the relationship between return of mobility and recovery of swallow function, we can still infer overall prognosis of swallow function based on the available clinical documentation. Another weakness of the study is that interpretation of the MBS studies was not standardized. Given that this was a retrospective review spanning a 9 year period, the MBS studies were performed and interpreted by 5 different SLPs who worked in the department at some point during that time period. The fluoroscopy images and video were not available for review in all the patients who underwent MBS, and therefore we opted to rely on the SLP documentation to determine whether or not aspiration occurred. The authors felt that using a binary system of interpretation (aspiration versus no aspiration) of the MBS studies would reduce confounding by eliminating other variations between the reads of the 5 SLPs. With respect to voice outcomes, we are limited by a lack of objective voice measures or subjective questionnaire data. At our institution, such instruments are not routinely applied to the pediatric population. Again, we rely on subjective documentation of patients' voice quality from clinical documentation and thus are unable to draw strong conclusions regarding functional voice outcomes in children with UVFI. A prospective study of children with UVFI employing objective voice measures, quality of life questionnaires, modified barium swallow, and laryngoscopy could further elucidate the long-term functional voice and swallowing outcomes in these children. 5. Conclusion VFI, while relatively rare in the general population, is the second most common cause of neonatal stridor and can cause serious deficits in the phonatory, respiratory, and swallowing functions of the pediatric patient. Several etiologies exist, with varying prognoses for recovery of function. In this study, we focused not only on rates of recovery of VF mobility in children with UVFI, but also on patients' long-term swallowing status. Based on our data, we conclude that while VF immobility can have a deleterious impact on
K.M. Tibbetts et al. / International Journal of Pediatric Otorhinolaryngology 88 (2016) 179e183
swallowing function initially, but with time patients are able to compensate and improve their swallowing function even if VF mobility does not return. MBS is an invaluable tool for identifying children at risk for aspiration and in the development of feeding strategies in children with dysphagia, but may not reliably indicate ultimate swallowing outcome.
[9]
[10]
[11]
References [1] P.H. Holinger, Clinical aspects of congenital anomalies of the larynx, trachea, bronchi, and oesophagus, J. Laryngol. Otol. 75 (1961) 1e44. [2] G.E. Murty, C. Shinkwin, K.P. Gibbin, Bilateral vocal fold paralysis in infants: tracheostomy or not? J. Laryngol. Otol. 108 (1994) 329e331. [3] S.R. Parikh, Paediatric unilateral vocal fold immobility, Otolaryngol. Clin. North Am. 37 (2004) 203e215. [4] N. Grover, A. Bhattacharyya, Unilateral pediatric vocal cord paralysis: evolving trends, J. Laryngol. Voice 2 (2012) 5e9. [5] K.D. Pereira, B.D. Webb, M.L. Blakely, C.S. Cox Jr., K.P. Lally, Sequelae of recurrent laryngeal nerve injury after patent ductus arteriosus ligation, Int. J. Pediatr. Otorhinolaryngol. 70 (9) (2006 Sep) 1609e1612. [6] R.I. Zbar, R.J. Smith, Vocal fold paralysis in infants twelve months of age and younger, Otolaryngol. Head. Neck Surg. 114 (1996) 18e21. [7] H. Daya, A. Hosni, I. Bejar-Solar, J.N. Evans, C.M. Bailey, Pediatric vocal fold paralysis: a long-term retrospective study, Arch. Otolaryngol. Head. Neck Surg. 126 (2000) 21e25. [8] I. de Gaudemar, M. Roudaire, M. Francois, P. Narcy, Outcome of laryngeal
[12]
[13]
[14]
[15] [16]
183
paralysis in neonates: a long term retrospective study of 113 cases, Int. J. Pediatr. Otorhinolaryngol. 34 (1996) 101e110. R.C. Miyamoto, S.R. Parikh, W. Gellad, G.R. Licameli, Bilateral congenital vocal cord paralysis: a 16-year institutional review, Otolaryngol. Head. Neck Surg. 133 (2) (2005 Aug) 241e245. S.S. Khariwala, W.T. Lee, P.J. Koltai, Laryngotracheal consequences of pediatric cardiac surgery, Arch. Otolaryngol. Head. Neck Surg. 131 (4) (2005 Apr) 336e339. M.T. Truong, A.H. Messner, J.E. Kerschner, M. Scholes, J. Wong-Dominguez, H.A. Milczuk, P.J. Yoon, Pediatric vocal fold paralysis after cardiac surgery: rate of recovery and sequelae, Otolaryngol. Head. Neck Surg. 137 (5) (2007 Nov) 780e784. B.G. Nichols, J. Jabbour, D.A. Hehir, N.S. Ghanayem, D. Beste, T. Martin, R. Woods, T. Robey, Recovery of vocal fold immobility following isolated patent ductus arteriosus ligation, Int. J. Pediatr. Otorhinolaryngol. 78 (8) (2014 Aug) 1316e1319. J. Jabbour, T. Martin, D. Beste, T. Robey, Pediatric vocal fold immobility: natural history and the need for long-term follow-up, JAMA Otolaryngol. Head. Neck Surg. 140 (5) (2014 May) 428e433. E. Bellin, D.D. Fletcher, Islam S. Geberern, N. Srivastava, Democratizing information creation from health care data for quality improvement, research, and education-the Montefiore medical experience, Acad. Med. 85 (2010) 1362e1368. B. Rogers, J. Arvedson, G. Buck, P. Smart, M. Msall, Characteristics of dysphagia in children with cerebral palsy, Dysphagia 9 (1) (1994) 69e73. Winter. J. Arvedson, B. Rogers, G. Buck, P. Smart, M. Msall, Silent aspiration prominent in children with dysphagia, Int. J. Pediatr. Otorhinolaryngol. 28 (2e3) (1994 Jan) 173e181.