Postoperative Assessment of Laryngopharyngeal Dysfunction in Neonates After Norwood Operation
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1 ORIGINAL ARTICLES: SURGERY: The Annals of Thoracic Surgery CME Program is located online at To take the CME activity related to this article, you must have either an STS member or an individual non-member subscription to the journal. Postoperative Assessment of Laryngopharyngeal Dysfunction in Neonates After Norwood Operation Konstantin Averin, MD, Karen Uzark, PhD, CPNP, Robert H. Beekman III, MD, J. Paul Willging, MD, Jesse Pratt, MS, MA, and Peter B. Manning, MD Departments of Pediatrics and Otolaryngology, and Divisions of Pediatric Cardiology, Biostatistics and Epidemiology, and Cardiothoracic Surgery, Cincinnati Children s Hospital Medical Center, Cincinnati, Ohio Background. The purpose of this study was to evaluate the incidence of vocal cord (VC) and swallowing dysfunction in infants after the Norwood operation and to examine the relationship between laryngopharyngeal dysfunction and postoperative outcomes. Methods. We conducted a retrospective review of 63 infants who underwent routine postoperative fiberoptic endoscopic evaluation of swallowing function and vocal cords after a Norwood operation at our institution during a recent 6-year period ( ). Results. The overall incidence of VC dysfunction after the Norwood operation was 58.7%. After a modification of the aortic arch dissection technique in 2007, the incidence of VC dysfunction decreased significantly from 79.5% in 2003 through 2006 to 25% in 2007 through 2009 (p < 0.001). The incidence of swallowing dysfunction also decreased from 23.1% in 2003 through 2006 to 4.2% in 2007 through 2009 (p 0.07). Swallowing dysfunction was more common in patients with VC dysfunction (21.6%) as compared with patients without VC dysfunction (7.7%; p 0.18). Patients with VC dysfunction were more often discharged home on tube-only feeding regimens compared with infants without VC dysfunction (46% versus 26.9%). In infants with both VC and swallowing dysfunction, 75% were discharged exclusively to have tube feeding. Median hospital length of stay tended to be longer in infants with swallowing dysfunction (31 days) than in infants without swallowing dysfunction (23 days; p 0.16). Conclusions. Vocal cord and swallowing dysfunction are common in infants after the Norwood operation and may increase the need for tube feeding regimens. Modification of surgical techniques for dissection and mobilization of the aorta can significantly reduce the incidence of these adverse outcomes. (Ann Thorac Surg 2012;94: ) 2012 by The Society of Thoracic Surgeons The Norwood operation is the primary surgical technique used to palliate infants with hypoplastic left heart syndrome and its variants. Since the first successful Norwood was performed in 1978, survival rates have steadily improved, but many infants still experience significant postoperative morbidity that affects hospital length of stay and quality of life. Feeding difficulties and poor weight gain are common in infants after the Norwood operation and can influence postoperative morbidity and length of hospitalization [1 3]. Potential factors contributing to feeding difficulties in these infants include gastroesophageal reflux, swallowing dysfunction, and vocal cord (VC) paralysis. The most common cause of VC paralysis in the pediatric population is iatrogenic injury of the recurrent laryngeal nerve during cardiac surgery [4, 5]. The Norwood Accepted for publication Jan 6, Address correspondence to Dr Uzark, University of Michigan Congenital Heart Center, 1500 E Medical Center Dr, SPC 5204 Ann Arbor, MI ; karenu@med.umich.edu. procedure and other operations on the aortic arch involve significant tissue dissection adjacent to the left recurrent laryngeal nerve and put it at risk for injury. Identification of VC and swallowing dysfunction after the Norwood operation may allow for early identification of neonates at risk for feeding difficulties and facilitate optimal tailoring of feeding regimens for these infants. Since January 2003, infants who survive the Norwood operation at our institution have routinely undergone a bedside flexible fiberoptic endoscopic evaluation of swallow (FEES) and VC movement before discharge to home. Through a retrospective chart review, the aims of this study were (1) to evaluate the incidence of VC and swallowing dysfunction in survivors of the Norwood operation, (2) to assess the impact of a modified aortic arch dissection technique on the incidence of VC dysfunction, and (3) to evaluate the relationship between VC or swallowing dysfunction and postoperative outcomes by The Society of Thoracic Surgeons /$36.00 Published by Elsevier Inc doi: /j.athoracsur
2 1258 AVERIN ET AL Ann Thorac Surg NORWOOD LARYNGOPHARYNGEAL DYSFUNCTION 2012;94: Operative Approach The Norwood operation was carried out using cardiopulmonary bypass support with deep hypothermia and regional cerebral perfusion during arch reconstruction. Aortic arch reconstruction was performed using pulmonary homograft augmentation in all cases and resection of the posterior coarctation shelf in selected cases. After initiation of cardiopulmonary bypass support, extensive dissection and mobilization of the ascending aorta, aortic arch, arch vessels, and descending aorta to about the level of the third pair of intercostal vessels was performed. Before January 2007, the entire arch dissection was carried out using the electrocautery as either a blunt dissector or to cauterize and divide tissue adherent to the aortic wall. In 2007 after observation of the Norwood procedure at another institution, the aortic arch dissection technique was modified to adopt the use of a Waterston dissecting clamp (Fig 1) for the majority of the aortic dissection. The Waterston clamp is a blunt-tipped dissector that develops the periadventitial plane around the aorta and ductus well with little need for sharp dissection and limited use of the cautery for the majority of the aortic dissection. All subsequent Norwood operations after early 2007 have used this arch dissection technique. There were no other technical modifications to the arch dissection or reconstruction during this period. Fig 1. Waterston dissecting clamp. Patients and Methods A retrospective chart review was performed of neonates who underwent Norwood procedure at our institution from 2003 to This study was approved by the Institutional Review Board of Cincinnati Children s Hospital Medical Center. Sixty-three (88%) of the 72 infant survivors had routine FEES performed, including assessment of VC mobility, during the postoperative period and are included in this study. Nine Norwood survivors were excluded related to discharge before FEES scheduled (n 2), transfer to local hospital before FEES (n 2), and genetic syndromes (n 5). Infants who died during the Norwood hospitalization before the FEES were also excluded. Medical records were reviewed to retrieve data on patient age and weight at operation, hours on a ventilator, days in the cardiac intensive care unit, days in the hospital, feeding method at hospital discharge, and the presence or absence of VC dysfunction and swallowing dysfunction on FEES. Laryngopharyngeal Evaluation Examination of laryngeal function was performed without complication at the bedside of each infant before discharge home. The FEES study was performed after the patients were extubated at least 24 to 36 hours and deemed medically fit for trials of oral feeds. Topical anesthesia (2% viscous lidocaine) was applied to a 2.2- mm-diameter flexible endoscope. The scope was inserted transnasally into the hypopharynx. All infants were undergoing routine pulse oximetry and telemetry monitoring during the evaluation. Vocal fold motion was assessed. Vocal cord dysfunction was defined as any impairment of mobility, including immobility or limited motion of the VCs resulting in inability to protect the glottis during swallowing thus raising the risk of aspiration. The child s ability to manage secretions was noted. An assessment of hypopharyngeal sensation could be made by monitoring the amount of secretions in the hypopharynx. Small tastes of breast milk or formula were given to the child, and an assessment of their ability to protect the airway from aspiration was made. (These infants had little or no experience with oral feeding.) Their ability to develop an effective swallow to clear material from the hypopharynx and their ability to avoid penetration of material into the laryngeal introitus was considered sufficient to allow progression toward oral feeding. Clear aspiration events and an inability to generate an effective swallow to clear material from the hypopharynx was reason to limit oral feeding. Infants were classified as having swallowing dysfunction if they were unable to adequately protect their airway from oropharyngeal secretions or food materials that were presented orally. Compensation strategies could be trialed during the study to determine whether and how the infant could be safely fed orally, to maximize airway protection based on FEES findings. Statistics Data were analyzed with SAS version 9.2 (SAS Institute, Inc, Cary, NC). A one-sample binomial proportion with Wald confidence interval was used in determining the overall incidence of VC dysfunction. For categorical variables (VC dysfunction, swallowing dysfunction, feeding technique) groups were compared using Fisher s exact test or a 2 test, depending on cell counts. For continuous variables (ventilator time, intensive care unit days, age at operation, and hospital days), groups were compared using the Wilcoxon rank-sum test owing to the fact that data were not normally distributed. For all tests a probability value of less than 0.05 was considered significant. Descriptive statistics are listed as mean or median (interquartile range) for continuous variables and a number percentage for categorical variables.
3 Ann Thorac Surg AVERIN ET AL 2012;94: NORWOOD LARYNGOPHARYNGEAL DYSFUNCTION 1259 Table 1. Comparison of Patient Characteristics Before (Group A) and After (Group B) Modification of Aortic Dissection Procedure Results (Group A) (n 39) (Group B) (n 24) p Value Median age at Norwood (days) Mean weight at Norwood (kg) Norwood with Blalock- 69.2% 79.2% 0.39 Taussig shunt Norwood with Sano 30.8% 20.8% 0.39 Incidence of vocal cord 79.5% 25.0% dysfunction Incidence of swallowing dysfunction 23.1% 4.2% 0.07 A total of 63 patients were included in this analysis. Median age at stage I Norwood operation was 6 days, and the mean weight was kg. Primary diagnosis was hypoplastic left heart syndrome in 71%. Postoperative source of pulmonary blood flow was a modified Blalock- Taussig shunt in 46 (73%) and a right ventricle to pulmonary artery conduit (Sano) in 17 (27%). Thirty-nine patients (group A, ) had the Norwood operation using electrocautery for arch dissection, and 24 patients (group B, ) had modification of the arch dissection procedure using the Waterston dissecting clamp. As shown in Table 1, there were no significant differences between the two groups related to weight at operation or shunt type. Patients median age at time of repair was higher in group B (5 days) than group A (3 days; p 0.03). The overall incidence of VC dysfunction was 58.7% (37 of 63). Of the 37 patients with VC dysfunction, 35 had exclusively left-sided VC dysfunction. Of the remaining 2, 1 had bilateral VC paralysis and 1 infant who had a right-sided aortic arch had right VC dysfunction. The incidence of VC dysfunction decreased from 79.5% in group A ( ) to 25% in group B ( ) after modification of the aortic arch dissection technique used during the Norwood (p 0.001; Table 1). The incidence of swallowing dysfunction also trended down, decreasing from 23.1% in group A to 4.2% in group B (p 0.07). Overall, the incidence of swallowing dysfunction tended to be higher in patients with VC dysfunction (21.6%) as compared with patients without VC dysfunction (7.7%; p 0.18). Comparing children with and without VC dysfunction (Table 2), there was no significant difference in the median number of hours on a ventilator, median intensive care unit length of stay, and median hospital length of stay. Discharge feeding regimen was oral with tube supplementation in 36 (57.1%), exclusively by tube in 24 (38.1%) including 7 by gastrostomy tube and 17 by nasogastric tube, and exclusively oral in 3 patients (4.8%). In infants with VC dysfunction, 46% were discharged from the hospital on tube-only feeding regimens, in comparison to 26.9% of infants without VC dysfunction (p 0.13). As shown in Table 3, when comparing patients with and without swallowing dysfunction, there was no statistically significant difference in the median number of hours on a ventilator, median cardiac intensive care unit length of stay, and median hospital length of stay. However median hospital length of stay tended to be longer in infants with swallowing dysfunction (p 0.16). In infants with swallowing dysfunction, 60.0% were discharged with tube-only feeding regimens, versus 34.0% of patients without swallowing dysfunction (p 0.16). In patients with both VC and swallowing dysfunction, 75.0% were discharged with tube-only feeding regimens, whereas 32.7% of those with neither problem were discharged with tube-only feeding (p 0.05). Comment Vocal cord dysfunction is a common complication in neonates after the Norwood operation, with an overall incidence of 59% in our study. There is wide variation in the previously reported incidence of VC dysfunction in this patient population, ranging from 9% to 45% [6 8]. Srinivasan and colleagues [8] found that identification of VC dysfunction significantly increased from 10% to 45% when routine VC assessment, as used in our institution, was performed in all infants in contrast to evaluation only when clinically indicated. We agree that VC dysfunction may often be unrecognized by caregivers in the postoperative period after a Norwood operation. Fiberoptic endoscopic evaluation of swallow was an excellent testing modality for this medically compromised patient population, as we were able not only to assess VC dysfunction but also to assess the Table 2. Comparison of Outcomes in Infants With and Without Vocal Cord Dysfunction VC Dysfunction Present (n 37) VC Dysfunction Absent (n 26) p Value Median ventilator time (h) a 163 ( ) ( ) 0.64 Median CICU length of stay (days) a 14 (10 21) 14.5 (8 24) 0.90 Median hospital length of stay (days) a 23.5 ( ) 24 (17 38) 0.92 Feeding method (% feeding by tube only) 46.0% 26.9% 0.13 Swallowing dysfunction 21.6% 7.7% 0.18 a Values are median and interquartile range in parentheses. CICU cardiac intensive care unit; VC vocal cord.
4 1260 AVERIN ET AL Ann Thorac Surg NORWOOD LARYNGOPHARYNGEAL DYSFUNCTION 2012;94: Table 3. Comparison of Outcomes in Infants With and Without Swallowing Dysfunction Swallowing Dysfunction Present (n 10) Swallowing Dysfunction Absent (n 53) p Value Median ventilator time (h) a ( ) 138 ( ) 0.14 Median ICU length of stay (days) a 15 (12 25) 14 (8 21) 0.51 Median hospital length of stay (days) a 31 (26 35) 23 (17 35) 0.16 Feeding method (% feeding by tube only) 60.0% 34.0% 0.16 Vocal cord dysfunction 80.0% 54.7% 0.18 a Values are median and interquartile range in parentheses. ICU intensive care unit. variables that correlated with the ability to feed orally, assess the ability to protect the airway, and evaluate gross sensory awareness of the hypopharynx that correlates well with airway protection abilities. The FEES was done without complication. In contrast to videographic swallow studies, the FEES provided the ability to assess patients who do not orally feed, as the patient s ability to handle secretions can still be assessed; pooling of secretions in the hypopharynx has been shown to correlate with aspiration risk [9, 10]. Importantly, our data also suggest that the occurrence of VC dysfunction is affected by surgical techniques, as modification of our aortic arch dissection procedure in 2007 was associated with a threefold decrease in VC dysfunction, presumably by avoiding injury to the recurrent laryngeal nerve. Dissection of the aortic arch and ductus is an integral part of the Norwood operation. This places the left recurrent laryngeal nerve at risk for damage as a result of traction and stretching as well as because of the heat of an electrocautery unit. Our data suggest that cautery may be a significant source of injury, as modification in technique that avoided or minimized use of the cautery was associated with a marked decrease in the incidence of this complication. The clinical relevance of this complication relates to the ability of the vocal folds to assist with protection of the airway. Operative injury to the recurrent laryngeal nerve may also contribute to swallowing dysfunction related to loss of pharyngeal innervation or glottic incompetence. If a child has poor oral motor control of material in the mouth, these materials may prematurely spill into the hypopharynx. If there is diminished sensation, a swallow may not be triggered in a timely fashion. If the vocal cords are not functioning normally, there is an increased risk of aspiration of this material pooling in the hypopharynx if it accumulates to the point where it overflows the aryepiglottic folds or spills through a deep interarytenoid notch. Skinner and colleagues [6] reported swallowing dysfunction in 48% of infants after Norwood operation. Although swallowing dysfunction in our cohort was less common at 16% overall, the incidence of swallowing dysfunction was approximately three times higher in patients with VC dysfunction. Truong and colleagues [11] reported that 45% of pediatric patients with vocal fold paralysis after cardiac surgery demonstrated aspiration or laryngeal penetration on modified barium swallow. In a recent report describing noncardiac risk factors for failure of infants with single ventricle to survive to stage II palliation, the strongest predictor of failure was VC paralysis with evidence of aspiration [12]. Given the serious risk of aspiration associated with swallowing dysfunction, recognition of this postoperative complication may be critical to avoiding an important cause of morbidity and potential interstage mortality in this patient population. Finally, although VC and swallowing dysfunction were not significantly associated with longer duration of ventilator time, intensive care unit time, or hospital length of stay in our cohort, the median hospital length of stay was 8 days longer in infants with swallowing dysfunction, consistent with the findings of Skinner and colleagues [6]. Longer length of hospital stay is frequently related to feeding difficulties, which are common in infants with hypoplastic left heart syndrome [2, 7]. Sachdeva and colleagues [1] identified that VC dysfunction after pediatric cardiovascular surgery was commonly associated with feeding problems and frequent need for gastrostomy. Likewise, Kohr and colleagues [13] found that dysphagia or swallowing dysfunction was associated with significant morbidity including longer length of hospital stay and need for home nasogastric tube feedings. All of their patients with dysphagia were discharged home on alternative feeding regimens. In our study, infants with VC or swallowing dysfunction were almost twice as likely to be discharged home feeding by nasogastric or gastrostomy tube only, and in infants with both VC and swallowing dysfunction, a full 75% were discharged home exclusively on tube feeding. An FEES examination provided early information to allow a treatment program to be developed for safer feeding during hospitalization and after discharge. Feeding therapists (speech or occupational therapists) had objective information and recommendations to guide their therapy strategies. Without oral stimulation and the introduction of small volumes of materials orally, the oral motor skills needed for the development of a safe swallow will not develop. Basic therapy strategies of positioning, pacing, controlling the rate of fluid flow, and controlling the viscosity of the liquid were used based on FEES findings to maximize airway protection. Therapists were then often able to advance volumes based on clinical observation and provided guidance to staff and families regarding optimal feeding strategies.
5 Ann Thorac Surg AVERIN ET AL 2012;94: NORWOOD LARYNGOPHARYNGEAL DYSFUNCTION 1261 This study has several limitations. A few patients did not have an FEES study performed. No patient in our study underwent a preoperative FEES study because of the critically ill nature of many neonates with singleventricle physiology preoperatively. In addition, it would have been beneficial to have follow-up evaluation to know the long-term implications of laryngopharyngeal dysfunction. Although follow-up studies were recommended in infants with significant swallowing dysfunction, many patients received outpatient follow-up at other institutions and it was beyond the scope of this retrospective review. Reported rates of recovery of VC paralysis range from 25% to 82% [6, 11, 14], but most studies include only patients who were initially referred for symptomatic VC dysfunction and follow-up times varied. Although the relationship between persistent feeding difficulty and laryngopharyngeal dysfunction in these patients is unknown, approximately one third of the patients (37.5%) in our study with significant swallowing dysfunction who survived to stage 2, generally performed at 5 to 6 months of age, were feeding orally at that time, with the remainder continuing to require tube feeding. Although there were no major differences in the surgical or postoperative management of these infants other than the aortic dissection technique noted, some practice variation is inherent in patient management by multiple providers. Most changes such as modifications to some details of our perfusion strategy would not be expected to influence recurrent laryngeal nerve paralysis. It is possible that the increasing experience of the surgeons with time may have affected the outcome in some ways, but we did not analyze differences among surgeons. Larger, multicenter studies are needed to clarify the causes and consequences of laryngopharyngeal dysfunction in this patient population. In summary, routine screening for laryngopharyngeal dysfunction demonstrated that VC and swallowing dysfunction are common in infants after the Norwood operation. Modification of surgical techniques for dissection and mobilization of the aorta, avoiding extensive electrocautery, may significantly reduce the incidence of this complication. Avoidance of laryngopharyngeal dysfunction may contribute to improved oral feeding and better clinical outcomes in these high-risk infants. Use of FEES may provide meaningful information to help guide feeding strategies in this vulnerable infant population. References 1. Sachdeva R, Hussain E, Moss MM, et al. Vocal cord dysfunction and feeding difficulties after pediatric cardiovascular surgery. J Pediatr 2007;15: Kelleher DK, Laussen P, Teixeira-Pinto A, Duggan C. Growth and correlates of nutritional status among infants with hypoplastic left heart syndrome (HLHS) after stage 1 Norwood procedure. Nutrition 2006;22: Cameron JW, Rosenthal A, Olson AD. Malnutrition in hospitalized children with congenital heart disease. Arch Pediatr Adolesc Med 1995;149: de Jong AL, Kuppersmith RB, Sulek M, Friedman EM. Vocal cord paralysis in infants and children. Otolaryngol Clin North Am 2000;33: Zbar RI, Smith RJ. Vocal fold paralysis in infants twelve months of age and younger. Otolaryngol Head Neck Surg 1996;114: Skinner ML, Halstead LA, Rubinstein CS, Atz AM, Andrews D, Bradley SM. Laryngopharyngeal dysfunction after the Norwood procedure. J Thorac Cardiovasc Surg 2005;130: Davis D, Davis S, Cotman K, et al. Feeding difficulties and growth delay in children with hypoplastic left heart syndrome versus d-transposition of the great arteries. Pediatr Cardiol 2008;29: Srinivasan C, Sachdeva R, Morrow WR, et al. Standardized management improves outcomes after the Norwood procedure. Congenit Heart Dis 2009;4: Hartnick CJ, Hartley BE, Miller C, Willging JP. Pediatric fiberoptic endoscopic evaluation of swallowing. Ann Otol Rhinol Laryngol 2000;109: Link DT, Willging JP, Miller CK, Cotton RT, Rudolph CD. Pediatric laryngopharyngeal sensory testing during flexible endoscopic evaluation of swallowing: feasible and correlative. Ann Otol Rhinol Laryngol 2000;109: Truong MT, Messner AH, Kerschner JE, et al. Pediatric vocal fold paralysis after cardiac surgery: rate of recovery and sequelae. Otolaryngol Head Neck Surg 2007;137: Pierce JR, Sharma SS, Castle SL, et al. Noncardiac risk factors for failure to survive to stage II palliation [Abstract]. Congenit Heart Dis 2010;5: Kohr LM, Dargan M, Hague A, et al. The incidence of dysphagia in pediatric patients after open heart procedures with transesophageal echocardiography. Ann Thorac Surg 2003;76: Khariwala SS, Lee WT, Koltai PJ. Laryngotracheal consequences of pediatric cardiac surgery. Arch Otolaryngol Head Neck Surg 2005;131:336 9.
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