Unilateral Vocal Fold Paralysis After Congenital Cardiothoracic Surgery: A Meta-analysis Julie E. Strychowsky, Gavin Rukholm, Michael K. Gupta and Diane Reid Pediatrics 2014;133;e1708; originally published online May 19, 2014; DOI: 10.1542/peds.2013-3939

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/133/6/e1708.full.html

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2014 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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Unilateral Vocal Fold Paralysis After Congenital Cardiothoracic Surgery: A Meta-analysis abstract BACKGROUND AND OBJECTIVE: There is variation in the literature in regard to the occurrence of unilateral vocal fold paralysis (UVFP) after congenital cardiothoracic surgery. The objective of this study was to identify and appraise the evidence for the occurrence of UVFP after congenital cardiothoracic surgery in a meta-analysis. METHOD: A comprehensive search strategy in Medline, Embase, and the Cochrane Library was conducted, limited to English publications. Two independent reviewers screened studies for eligibility criteria. Of the 162 identified studies, 32 (20%) met the inclusion criteria. Using the Oxford Centre for Evidence-Based Medicine guidelines, 2 reviewers appraised the level of evidence, extracted data, and resolved discrepancies by consensus. Weighted pooled proportion and 95% confidence intervals (CIs) are reported. RESULTS: Thirty-two studies (n = 5625 patients) were included. Levels of evidence varied from level 3 to 4. Among all studies, the weighted pooled proportion of UVFP was 9.3% (95% CI, 6.6% to 12.5%), and among 11 studies (n = 584 patients) that postoperatively evaluated patients with flexible nasopharyngolaryngoscopy to document presence of UVFP, the weighted pooled proportion of UVFP was 29.8% (95% CI, 18.5% to 42.5%). Twenty-one studies (n = 2748 patients) evaluated patients undergoing patent ductus arteriosus ligation surgery, and the weighted pooled proportion of UVFP was 8.7% (95% CI, 5.4% to 12.6%). Six of these (n = 274 patients) assessed all patients postoperatively, and the weighted pooled proportion of UVFP was 39% (95% CI, 18% to 63%). Pooled analyses of risk factors and comorbidities are reported. Heterogeneity and publication bias were detected. CONCLUSIONS: UVFP is a demonstrated risk of congenital cardiothoracic surgery. Routine postoperative nasopharyngolaryngoscopy for vocal fold assessment by an otolaryngologist is suggested. Pediatrics 2014;133:e1708–e1723

AUTHORS: Julie E. Strychowsky, MD,a Gavin Rukholm, MD, FRCSC,a,b Michael K. Gupta, MD, MSc, FRCSC,a and Diane Reid, MD, FRCSCa aDepartment of Surgery, Division of Otolaryngology–Head and Neck Surgery, McMaster University, Hamilton, Ontario, Canada; and bPeterborough Regional Health Centre, Peterborough, Ontario, Canada

KEY WORDS unilateral vocal fold paralysis, cardiothoracic surgery, patent ductus arteriosus ABBREVIATIONS CI—confidence interval G-tube—gastrostomy tube OCEBM—Oxford Centre for Evidence-Based Medicine PDA—patent ductus arteriosus UVFP—unilateral vocal fold paralysis Dr Strychowsky conceptualized and designed the study, designed the data collection instruments, performed the literature search and data extraction, appraised the levels of evidence, carried out the initial analyses and interpretation of data, and drafted the initial manuscript; Dr Rukholm conceptualized and designed the study, performed the literature search and data extraction, appraised the levels of evidence, interpreted the data, and critically reviewed and revised the manuscript; Dr Gupta conceptualized and designed the study, carried out the statistical analysis, interpreted the data, and critically reviewed and revised the manuscript; Dr Reid conceptualized and designed the study, interpreted the data, and critically reviewed and revised the manuscript; and all authors approved the final manuscript as submitted. This article was presented as a podium presentation at the Annual Meeting of the American Society of Pediatric Otolaryngology in Arlington, Virginia, on April 26, 2013. www.pediatrics.org/cgi/doi/10.1542/peds.2013-3939 doi:10.1542/peds.2013-3939 Accepted for publication Mar 4, 2014 Address correspondence to Julie E. Strychowsky, MD, Department of Surgery, Division of Otolaryngology–Head and Neck Surgery, McMaster University, 1200 Main St West, Hamilton, Ontario, Canada, L8N 3Z5. E-mail: [email protected] PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2014 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: No external funding. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

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Unilateral vocal fold paralysis (UVFP) secondary to left recurrent laryngeal nerve injury during cardiothoracic surgery is a known risk.1 The path of the nerve, which loops around the arch of the aorta, makes it susceptible to injury. This is especially true in patent ductus arteriosus (PDA) ligation surgery, given the nerve’s proximity to the PDA.2 Sequelae of UVFP may include stridor, absent or weak cry, aspiration, or feeding and swallowing difficulties.3 Therefore, adequate and timely diagnosis can help guide appropriate management. Although some patients are asymptomatic, this does not preclude proper assessment. Flexible nasopharyngolaryngoscopy is a short and well-tolerated procedure performed without sedation by otolaryngologists that allows direct visualization of the larynx and subsequent diagnosis of UVFP. There is variation in the literature in regard to the occurrence of UVFP after congenital cardiothoracic surgery. This may result from the lack of routine postoperative vocal fold function assessment. To date, there has been no systematic review of the evidence for the occurrence of UVFP after cardiothoracic surgery in infants and children. The primary objective of this study was to identify and appraise the evidence for the occurrence of UVFP after congenital cardiothoracic surgery (all types of surgery and PDA ligation surgery only) in infants and young children. We also sought to determine the occurrence of UVFP in patients who underwent postoperative assessment by flexible nasopharyngolaryngoscopy. Other outcomes investigated included UVFP-associated risk factors and comorbidities.

METHODS This review was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and MetaAnalyses guideline.4

Literature Search Strategy The literature was searched using Ovid Medline (1946 to October 2012), Embase (1980to2012Week 41), and the Cochrane Library (Cochrane Database of Systematic Reviews, 2012, Issue 3). The electronic database search combined intervention-specific terms (cardiothoracic surgery, cardiac surgery, heart surgery, cardiopulmonary bypass, patent ductus arteriosus, PDA ligation, ligation, closure) and outcome-specific terms (vocal fold, vocal cord, recurrent laryngeal nerve, immobility, mobility, paralysis, paresis, injury). To ensure that all relevant published articles were captured, the search was not limited by publication date or study design. Relevant articles and abstracts were selected and reviewed. Reference lists from these sources and recent review articles were searched for additional publications. Study Selection Criteria Articles were assessed for eligibility independently by 2 review authors (J.E.S. and G.R.) and were included if they were prospective or retrospective fully published studies that reported occurrence of UVFP after congenital cardiothoracic surgery in infants and young children. Secondary outcomes included type of surgery (PDA ligation or other), postoperative assessment of vocal cord function by flexible nasopharyngolaryngoscopy, patient demographics, respiratory and swallowing outcomes, and comorbidities. NonEnglish publications were excluded. Assessment of Quality Methodological quality of identified studies was appraised using the Oxford Centre for Evidence-Based Medicine (OCEBM) 2011 Levels of Evidence5:

 Level 1: Systematic review of randomized trials, systematic review of nested case–control studies, n-of-1 trials

 Level 2: Individual randomized trials or (exceptionally) observational studies with dramatic effect

 Level 3: Nonrandomized controlled cohort/follow-up studies provided there are sufficient numbers to rule out a common harm

 Level 4: Case series, case–control, or historically controlled studies

 Level 5: Mechanism-based reasoning Data Analysis Relevant data were extracted from fully published reports by 2 independent review authors (J.E.S. and G.R.) following prescribed tables developed a priori. Disagreement was resolved by consensus. Descriptive statistics were extracted or calculated for occurrence of UVFP. Cases of bilateral vocal fold paralysis were excluded. A qualitative synthesis of results was performed when applicable. Meta-analysis was performed by calculating pooled proportion of the weighted occurrence for UVFP using DerSimonian–Laird weights for the random effects model. Subgroup analyses developed a priori for postoperative assessment for UVFP and PDA ligation surgery only were conducted. Inverse variance measuring mean difference for the random effects model was used for the analysis of continuous variables. Heterogeneity between studies was tested using the Q statistic with the I2 approach. Publication bias was analyzed by visual inspection of the funnel plot and Egger’s test. StatsDirect software 1.7.8 (StatsDirect Limited, Cheshire, UK) and Review Manager 5.1.7 (The Nordic Cochrane Centre, The Cochrane Collaboration, Oxford, UK) were used.

RESULTS One hundred sixty-two studies were identified through the literature search. Titles and abstracts of these studies

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were screened for the inclusion and exclusion criteria. The search strategy did not include a limit for study design; therefore, many of the studies excluded were comments, editorials, or reviews. A resultant 50 full-text articles were further screened. Thirty-two studies that satisfied the inclusion criteria were included in the analysis (Fig 1).6–37 OCEBM levels of evidence varied from level 3 (9 studies)9–11,14–16,20,23,26 to level 4 (23 studies)6–8,12,13,17–19,21,22,24,25,27–37 (Table 1). Occurrence of UVFP, type of surgery, patient demographics, and vocal fold assessment are reported in Table 1. Analysis by Type of Surgery Thirty-two studies involving 5625 patients reported the occurrence of UVFP after any type of cardiothoracic

surgery.6–37 The weighted pooled proportion for UVFP was 9.3% (95% CI, 6.6% to 12.5%) (Fig 2). Heterogeneity analysis measured an I2 (inconsistency) of 91.4% (95% CI, 89.3% to 92.9%). This is the percentage of variation across studies that is due to heterogeneity rather than chance. Funnel plot analysis revealed a possible publication bias; Egger’s test showed the presence of bias (bias = 2.5; 95% CI, 1.8 to 3.2; P , .0001). Twenty-onestudiesinvolving 2748patients reported the occurrence of UVFP after PDA ligation only.7,8,10–15,17,20,21,24,27–31,34–37 The weighted pooled proportion was 8.7% (95% CI, 5.4% to 12.6%) (Fig 3). Heterogeneity analysis measured an I2 of 81.6% (95% CI, 65.0% to 88.4%). Funnel plot analysis and Egger’s test showed the presence of publication

bias (bias = 3.3; 95% CI, 2.2 to 4.4; P , .0001). Analysis for Postoperative Assessment of Vocal Fold Function Only 10% of patients underwent postoperative vocal fold function assessment. Among patients undergoing any type of cardiothoracic surgery procedure, 11 studies involving 584 patients postoperatively evaluated every patient with flexible nasopharyngolaryngoscopy.6,9–11,14–17,20,22,23 The weighted pooled proportion for UVFP was 29.8% (95% CI, 18.5% to 42.5%) (Fig 4). Heterogeneity analysis measured an I2 of 90.4% (95% CI, 85.2% to 93.1%). Both funnel plot and Egger’s test analyses showed publication bias among the studies (bias = 7.0; 95% CI, 2.3 to 11.7; P = .0079).

FIGURE 1 Flow diagram of study selection.

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PDA ligation

PDA ligation

All cardiothoracic surgery

PDA ligation

PDA ligation

Rukholm et al, 20128 (Canada), Jul 2003–Jul 2010

Carpes et al, 20119 (Canada), Nov 2008–Aug 2009

Benjamin, 201010 (USA), Jan 2004–Dec 2006

Roksund, 201011 (Norway), 1982–1985 (surgery), 2008–2009 (study)

All cardiothoracic surgery

Type of Surgery

Heuchan et al, 20127 (UK), 2001–2007

Dewan et al, 20126 (USA), May 2007–May 2008

Author, YearRef (Country), Years of Study

TABLE 1 Outcomes

+VCP: SA 8.86 6 5.99 d SW 2.99 6 0.54 kg 2VCP: SA 10.36 6 6.73 d SW 3.11 6 0.50 kg GA 26 wk (25–27) BW 840 g (730–1035) SA 31 d (25–41) +VCP: GA 25.4 wk (24.8–26.0) BW 743.8 g (665.4–822.1) SA 28.9 wk (28.0–30.0) SW 845.8 g (766.5–925.2) 2VCP: GA 26.7 wk (26.0–27.5) BW 990.0 g (858.4–1121.5) SA 34.0 wk (29.5–38.5) SW 1404 g (966.3–1843.3) +VCP: SA 0.7 m (0.1–14.2) SW 3.7 kg (3.2–9.2) 2VCP: SA 7.8 m (4.1–36.7) SW 7.5 kg (4.9–15.7) Extremely low BW +VCP: GA 24.5 6 1.1 wk BW 722 6 122 g SA 17 68.7 d SW 722 6 140 g 2VCP: GA 24.8 6 1.3 wk BW 728 6 132 g SA 22 6 14.5 d SW 798 6 219 g GA ,28 wk or BW ,1000 g SA 12 d (4–29) +VCP: GA 27.1 6 1.5 wk BW 874 6 138 g 2VCP: GA 27.0 6 2.9 wk BW 928 6 283 g

Patient Demographics

7/11 (64%)

22/55 (40%) 22/25 (88%) scoped

8/100 (8%)

19/111 (17.1%)

6/125 (4.8%)

15/76 (19.7%)

Occurrence of UVFP (Cases/Total) (%)

Flexible NPL and continuous laryngoscopy during maximal treadmill exercise

Flexible NPL if suspected VCP

Flexible NPL immediately preoperatively and within 72 h of extubation

27.9% NPL postoperative 0.9% NPL preoperative

NR

Flexible NPL after extubation, swallowing evaluation

Assessment for Vocal Cord Function

3

3

3

4

4

4

Level of Evidence

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PDA ligation

Type of Surgery

Norwood procedure

Srinivasan, 200916 (USA)

Davis, 200818 (USA)

Clement, 200817 (Canada), Oct 2003–May 2004

GA ,37 wk GA 26 6 6.5 wk (23 6 3 to 34) BW 943.5 g (535–1793) SA 29 6 4.7 wk (25 6 6 to 40 6 4) SW 1104 g (525–2520) GA 25.5 6 2.3 wk BW 837.7 6 277.2 g SA 14.1 6 1.8 d SW 881.3 6 338.1 g Premature infants: GA 26.6 6 2.5 wk BW 1000 6 394 g SA 17 6 12 d SW ,1 kg Suture ligature: GA 25 6 2.0 wk BW 740 6 288 g SW 1054 6 626 g Clip: GA 24.7 6 1.3 wk BW 651 6 169 g SW 762 6 210 g Group 1: SA 10 d (3–218) SW 3.2 kg (2.0–5.7) Group 2:

Patient Demographics

SA 6 d (2–64) SW 3.3 kg (2.3–4.3) PDA ligation +VCP: GA 24.8 wk (24–26) BW 725 g (580–887) SA 14.5 d (6–31) 2VCP: GA 27.0 wk (25–31) BW 1040 g (700–1540) SA 13.8 d (4–53) Hypoplastic left heart syndrome; BW 3.19 6 0.69 kg TGA SA 6.1 6 3.8 d BW 3.35 6 0.65 kg SA 9.2 6 10.0 d

PDA ligation (suture ligature or clip)

Spanos, 200915 (USA), 1995–2005

Group 1, 2001–2004 Group 2, 2005–2007 (standardized management)

PDA ligation

Smith, 200914 (USA), Apr 2004–Oct 2007

Mandhan, 200913 (New Zealand), Jan 1987–Dec PDA ligation 2005

Sørensen, 201012 (Denmark), 1998–2007

Author, YearRef (Country), Years of Study

TABLE 1 Continued

0/26 (0%)

5/27 (18.5%)

12/23 (52%)

4/40 (10%) 18/40 (45%) (all scoped)

13/68 (19%)

14/86 (16%)

1/145 (0.7%)

3/46 (7%)

Occurrence of UVFP (Cases/Total) (%)

NR

Flexible NPL, 20 pts Video fluoroscopic swallow study

Flexible NPL all patients in Group 2

4

4

3

3

3

Postextubation flexible NPL

Flexible NPL after extubation

4

4

Level of Evidence

NR

NR

Assessment for Vocal Cord Function

PDA ligation

PDA ligation

All cardiothoracic surgery Norwood procedure Aortic arch reconstruction

PDA ligation

Pereira, 200620 (USA), Mar 2001–Feb 2004

Villa, 200621 (France), Sep 1991–Feb 2004

Khariwala, 200522 (USA), 4-y period

Skinner, 200523 (USA), Apr 2003–Dec 2004

Vida, 200424 (Italy), Jun 1994–Dec 2002

All cardiothoracic surgery

PDA ligation

PDA ligation

PDA ligation PDA ligation

Kohr, 200326 (USA), Mar 1999–Sep 1999

Liang, 200327 (Taiwan), Mar 1998–May 2001

Niinikoski, 200128 (Finland), 1988–1998

LeBlanc, 200029 (Canada), Jan 1985–Dec 1998 Russell, 199830 (Canada), Jan 1985–Dec 1997

Einarson, 200325 (Canada), Jan 1998–Dec 1999 All cardiothoracic surgery

All cardiothoracic surgery

Type of Surgery

Sachdeva, 200719 (USA), Jan 2000–Jan 2006

Author, YearRef (Country), Years of Study

TABLE 1 Continued

Neonates ,28 d: SA 7.8 6 5.6 d (1–25) SW 3.22 6 0.62 kg (1.5–4.8) SA 4.8 6 5.2 y (1 d–16.7 y) SW 19.6 6 17.8 kg (3.1–72.6) Premature infants excluded Subgroup ,1 y +VCP: SW 9.0 kg (8.9–9.1) 2VCP: SW 10.3 kg (6.2–11.5) Very low BW infants ,1500 g: GA 27.2 wk BW 963 6 239 g SA 12 6 8 d SW 969 6 231 g Nonpremature infants Premature infants: GA 26 wk (23–36) BW 847.5 g (400–2300) SA 21 d (4–60) SW 982.5 (475–2740)

SA 6 d (2–19) SW 3.1 kg (1.9–4.2) SA 9 d (4–33) SW 3.1 (2.0–3.7) SA 45 m (3–161) SW 18 kg (4.2–73)

Pediatric

GA 25 wk BW 740 g SA 23 d SW 914 g Low BW infants, 24 pts Low BW infants: 2.1 6 0.4 kg

SA 13.5 d (1–1604) SW 3.45 kg (0.9–14.5)

Patient Demographics

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1/101 (1%)

3/18 (16.7%)

4/50 (8%)

8/101 (8%)

1/150 (0.7%)

Low BW infants: 2/24 (8.3%) transient 1/24 (4.2%) persistent Children: 15/676 (2.2%) transient 2/676 (0.3%) persistent 11/48 (23%) UVFP 3/48 (6%) Bilateral VCP 3/33 (9%) 4/16 (25%)

7/61 (11.5%)

38/2255 (1.7%)

Occurrence of UVFP (Cases/Total) (%)

NR NR

NR

Bronchoscopy if hoarseness, inspiratory stridor, or weak cry

ORL if recommended by speech–language pathologist

ORL assessment not specified

NR

Flexible NPL (median 10 d postoperative) Modified barium swallow

Inpatient ORL consultation

NR

Flexible NPL postextubation

NR if all scoped

Assessment for Vocal Cord Function

4 4

4

4

3

4

4

3

4

4

3

4

Level of Evidence

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Postoperative laryngoscopy

ORL assessment only if symptomatic

NR

NR

NR

Assessment for Vocal Cord Function

4 4

4

4

4

4

4

Level of Evidence

BW, birth weight; GA, gestational age; NPL, nasopharyngolaryngoscopy; NR, not reported; ORL, otorhinolaryngology; pts, patients; SA, age at surgery; SW, weight at surgery; TGA, transposition of the great arteries; VATS, video-assisted thoracoscopic surgery; VCP, vocal cord paralysis.

Fan, 198936 (USA), Dates NR Davis, 198837 (USA), Jun 1980–Jul 1987

Laborde, 199535 (USA), Sep 1991–Mar 1995

Zbar, 199634 (USA), Jan 1991–Jan 1994

Aortic coarctation SA 13 d (3–34) and 69 d (61–78) 1/23 (4.3%) and tubular hypoplasia repair SW 2.9 kg (1.3–5) PDA ligation ,12 m 6/68 (8.8%) +VCP: 22.7% for extremely low BW (,1 kg) GA 26.3 wk BW 0.9 kg SA 31.9 d SW 1.1 kg 2VCP: GA 33.8 wk BW 2.3 kg SA 88.4 d SW 3.4 kg PDA ligation ,6 m, 70 pts (30%) 6/230 (2.6%) 6–48 m, 123 pts (54%) 5 transient .48 m, 37 pts (16%) 1 persistent SW 12.6 kg (1.2–65) PDA ligation ,1500 g 7/167 (4.2%) PDA ligation Premature infants 3/106 (2.8%)

1/45 (2.2%)

0/20 (0%) 1/20 (5%)

Occurrence of UVFP (Cases/Total) (%)

Rajasinghe, 199633 (USA), Jul 1992–Jan 1995

Coil occlusion: SA 4.1 6 4.9 y (6 m–15 y) SW 18 6 16 kg Surgical closure: SA 3 6 3.9 y (4 m–10 y) SW 12 6 7 kg SA 2.65 y (1 d–14.1 y) SW 11.78 kg (580 g–45.9 kg)

Patient Demographics

VATS for various procedures

PDA ligation (coil occlusion or surgical closure)

Type of Surgery

Lavoie, 199632 (USA), Dates NR

Hawkins, 199631 (USA), Jul 1994–Mar 1996

Author, YearRef (Country), Years of Study

TABLE 1 Continued

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FIGURE 2 UVFP after all types of cardiothoracic surgery (32 studies). Weighted pooled proportion for UVFP was 9.3% (95% CI, 6.6% to 12.5%).

Six studies involving 274 patients postoperatively evaluated every patient with flexible nasopharyngolaryngo-

scopy after PDA ligation.10,11,14,15,17,20 The weighted pooled proportion for UVFP was 39% (95% CI, 18% to 63%) (Fig 5).

Heterogeneity analysis measured an I2 of 93.2% (95% CI, 88.5% to 95.4%). Analysis of the funnel plot by visual

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FIGURE 3 UVFP after PDA ligation only (21 studies). Weighted pooled proportion of UVFP was 8.7% (95% CI, 5.4% to 12.6%).

inspection did not suggest publication bias; Egger’s test confirmed its absence (bias = 7.6; 95% CI, 23.4 to 18.5; P = .13). Analysis for Demographics Five studies involving 354 patients reported birth weights for patients with and without UVFP after surgery.8,10,11,14,17,34 For patients with and without UVFP, birth weights ranged from 725 to 900 g and 728 to 2300 g, respectively. The weighted pooled mean difference between patients with and without UVFP was 2201 g (95% CI, 2372 g to 230 g) (P = .02) (Fig 6); patients with UVFP were 201 g smaller e1716

than those without. Heterogeneity analysis measured an I2 of 79%. Weight at the time of surgery was reported among 6 studies (373 patients) as a comparison for patients with and without UVFP.6,8,9,27,34 Surgical weight ranged from 846 g to 9000 g among patients with UVFP and 1404 g to 10 300 g for those without. The weighted pooled mean difference was 2820 g (95% CI, 21564 g to 276 g) (P = .03), showing patients with UVFP to have significantly smaller weights at the time of surgery (Fig 7). Heterogeneity analysis measured an I2 of 71%.

Gestational age of patients with and without UVFP was reported among 6 studiesinvolving 399patients.8,10,11,14,17,34 Among patients with and without UVFP, gestational ages ranged from 24.5 to 27.1 weeks and 24.8 to 33.8 weeks, respectively. The weighted pooled mean difference was 21.1 weeks (95% CI, 21.7 to 20.46 weeks, P = .0007), statistically significantly correlating younger gestational ages with a higher incidence of UVFP (Fig 8). There was low heterogeneity among the studies (I2 = 28%). Five studies involving 378 patients reported age at the time of surgery for

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FIGURE 4 UVFP after all cardiothoracic surgery in patients who underwent postoperative vocal fold assessment (11 studies). Weighted pooled proportion for UVFP was 29.8% (95% CI, 18.5% to 42.5%).

FIGURE 5 UVFP after PDA ligation only and postoperative vocal fold assessment (6 studies). Weighted pooled proportion for UVFP was 39% (95% CI, 18% to 63%).

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patients with and without UVFP.6,8,9,17,34 Surgical ages ranged from 8.9 to 31.9 days and 10.4 to 237 days, respectively. The weighted pooled mean difference between patients with and without UVFP was 217.8 days (95% CI, 241.8 to 6.3 days, P = .15) and not statistically significant (Fig 9). Heterogeneity analysis measured an I2 of 62%. Analysis for Duration of Ventilation Five studies, comprising 226 patients, reported a comparison of duration of ventilation for patients with and without UVFP.6,10,11,17,20 The weighted pooled mean difference was not statistically

significant (6.88 days; 95% CI, 22.1 to 15.9 days; P = .13) (Fig 10). I2 was 51%.

Other Analyses

reporting of data among studies included or too few studies that reported the same outcome. Length of stay in hospital was reported in 2 studies.6,17 Mean length of stay was statistically significantly longer among patients with UVFP in both studies. Dewan et al6 reported on patients who underwent median sternotomy for cardiac surgery (34.9 6 29.5 days vs 22.9 6 14.6 days, P = .02), and Clement et al17 investigated extremely low birth weight infants undergoing PDA ligation (148.2 vs 96.8 days, P , .001).

Additional pooling of data were not possible because of the nonuniform

Two studies did not report any recovery of vocal fold function at follow-up points

Analysis for Gastrostomy Tube Use A comparison of gastrostomy tube (G-tube) use in patients with and without UVFP was reported among 283 patients in 5 studies.8,10,17,20,23 The pooled odds ratio was 7.3 (95% CI, 1.6 to 32.8, P = .010), suggesting a correlation of G-tube use among patients without UVFP (Fig 11). I2 was 49%.

FIGURE 6

Birth weight (6 studies). Weighted pooled mean difference between patients with and without UVFP was 2201 g (95% CI, 2372 g to 230 g) (P = .02).

FIGURE 7

Weight at time of surgery (5 studies). Weighted pooled mean difference was 2820 g (95% CI, 21564 g to 276g) (P = .03).

FIGURE 8

Gestational age (6 studies). Weighted pooled mean difference was 21.1 weeks (95% CI, 21.7 to 20.46 weeks) (P = .0007).

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FIGURE 9

Age at time of surgery (5 studies). Weighted pooled mean difference between patients with and without UVFP was 217.8 days (95% CI, 241.8 to 6.3 days) (P = .15).

FIGURE 10

Duration of ventilation (5 studies). Weighted pooled mean difference was 6.88 days (95% CI, 22.1 to 15.9 days), P = .13.

FIGURE 11 G-tube use (5 studies). Pooled odds ratio was 7.3 (95% CI, 1.6 to 32.8) (P = .010).

of 6 and 5 to 19 months, respectively.34,36 Khariwala et al22 reported a recovery 9 of 11 patients (82%). Carpes et al9 reported recovery of vocal fold movement in 3 of 7 patients at 3 months’ follow-up. Furthermore, Spanos et al15 reported longterm follow-up (range 1–18 months) for 6 patients with UVFP. Only 2 patients were found to have full recovery. Sachdeva et al19 reported follow-up in 9 patients with UVFP and found full recovery of function in 3 patients, partial recovery in 4 patients, and no signs of recovery in 2 patients; however, no time frame for follow-up was reported.

DISCUSSION To our knowledge, this is the first systematic review and meta-analysis to report the pooled occurrence of UVFP after cardiothoracic surgery in infants and children. Among 32 studies, involving 5625 patients, the weighted pooled proportion of UVFP was 9.3%. For those undergoing only PDA ligation, the pooled proportion was 8.7%. However, it is important to consider the occurrence of UVFP in the population of patients who underwent routine postoperative vocal cord function assessment by flexible

nasopharyngolaryngoscopy. Only 10% of patients after any type of cardiothoracic surgeryorPDAligationsurgeryunderwent postoperative vocal fold function assessment. The weighted pooled proportion of patients with UVFP in this population was 30% for patients undergoing all types of cardiothoracic surgery and 39% for those undergoing PDA ligation. These data suggest that the occurrence of UVFP among patients who were postoperatively assessed for vocal fold function is significant. Ninety percent of patients included in our analysis of 32

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studies did not undergo routine postoperative assessment. Among these patients, stridor, absent or weak cry, aspiration, or feeding or swallowing difficulties most often prompt additional investigation of vocal fold function. Children who are asymptomatic initially may not be diagnosed until early childhood, when they present with an inability to sing or a weak voice. Smith et al14 reported a rate of delayed diagnosis of 14%. Timely diagnosis would ensure that appropriate treatment options such as use of thickened foods, voice therapy, or surgical intervention be made available to them.38 Methods of Vocal Fold Assessment Methods of vocal fold assessment generally included assessment with flexible nasopharyngolaryngoscopy, a welltolerated bedside examination that does not require sedation. Ten studies performed the assessment after extubation.6,9–11,14–17,20,23 One study did not specify whether patients underwent flexible nasopharyngolaryngoscopy; however, an otorhinolaryngologist assessed all the patients, and therefore we assumed that those needing additional assessment would have undergone the diagnostic laryngoscopy.22 Carpes et al9 also performed the assessment immediately preoperatively. Roksund et al11 assessed patients approximately 25 years after PDA ligation by performing flexible nasopharyngolaryngoscopy and continuous laryngoscopy during maximal treadmill exercise. Three studies also included swallowing assessments.6,7,23 Preoperative assessment of vocal fold function merits discussion. The inherent benefit is the avoidance of attributing the occurrence of UVFP to iatrogenic injury if it is noted preoperatively. However, patients may have associated heart failure, pulmonary failure, and poor respiratory reserve secondary to their cardiac anomaly, which may preclude adequate preoperative evaluation. Pree1720

operative assessment of vocal fold function was reported only in the study from BC Children’s Hospital.9 The authors performed flexible laryngoscopy immediately before surgery in the operating room and within 72 hours after extubation. Twenty-four (15%) patients could not undergo preoperative assessment because of endotracheal intubation, and 4 (2.5%) were found to have UVFP preoperatively and were excluded from their study. Additional techniques for vocal fold function assessment may include extubation followed by direct laryngoscopy and rigid bronchoscopy, laryngeal electromyography, or laryngeal ultrasound. Maturo et al39 prospectively showed that laryngeal electromyography could predict recurrent laryngeal nerve function return when compared with diagnosis by flexible fiberoptic laryngeal examination. The authors reported this technique to be a safe, operator-friendly method for determining the likelihood of function return in a variety of patients, including those who had undergone PDA ligation. The mean patient age was 21.4 months. Wang et al40 reported the usefulness of laryngeal ultrasound for vocal fold assessment. They showed maximum glottic angle and vocal fold–arytenoid angle to be quantitative ultrasonographic indicators of vocal fold immobility among 45 children of median age 4 years and 6 months (range 9 months–13 years). However, the efficacy of laryngeal electromyography or ultrasound has not been described in neonates or infants, nor has it been used in the intubated patient. Risk Factors UVFP was shown to be statistically significantly associated with younger gestational age, lower birth weight, and lower surgical weight among the limited number of studies that reported these outcomes. Age at time of surgery was not a significant risk factor for UVFP. Length of mechanical ventilation was not signifi-

cantly different between groups. G-tube use was statistically significantly higher among patients without UVFP. These analyses are based on limited patient numbers because of the small number of studies that reported these outcomes by presence or absence of UVFP. Patients who need congenital cardiac surgery often havemultiple comorbidities. Two studies8,11 reported associations between bronchopulmonary dysplasia and UVFP after PDA ligation. Roksund et al11 reported outcomes for 11 patients; bronchopulmonary dysplasia was present in 86% of patients with UVFP and 50% of those without UVFP (P , .001). Among 111 patients, Rukholm et al8 reported 74% of patients with UVFP to have bronchopulmonary dysplasia, compared with 47% of those without UVFP (P = .043); however, given the Bonferroni method of statistical analysis for multiple comparisons, only P , .006 was considered significant. This retrospective study from our center at McMaster University showed only gastroesophageal reflux disease to be statistically significantly associated with UVFP after PDA ligation, and not G-tube feeding, sepsis, pneumonia, retinopathy of prematurity, or anemia of prematurity.8 Benjamin et al10 compared neurodevelopmental outcomes between patients with and without UVFP after PDA ligation and found no significant difference between groups. Surgical technique for PDA ligation and its correlation with occurrence of UVFP has also been investigated. Spanos et al15 compared rates of paralysis between vascular clip and suture ligation procedures in a prospective study and found similar incidence of UVFP in both groups (19% vs 20%). All cases of UVFP were in infants who weighed ,1 kg at birth. Zbar et al34 showed iatrogenic UVFP to be associated only with the use of surgical clips and not suture; however, the authors determined that it was not possible to establish a plausible correlation because clips were

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used in 91% of premature infants who needed PDA ligation. Carpes et al9 reported the use of cautery in 8 (100%) patients with UVFP, compared with 60 (65%) patients without UVFP. Additional inquiry in regard to surgical technique and perhaps operator learning curve may be warranted. Study Weaknesses The inherentweakness of our study isdue to the heterogeneity that is introduced when data are pooled from studies with nonuniform patient populations and methods. Variability in the type of surgery (PDA ligation versus other cardiothoracic surgery), vocal fold assessment, and patient demographics contributes to this weakness. The random effects model for statistical analysis and a priori subgroup analyses were undertaken to account for some of these limitations. Caseserieswerethemostcommontypeof study. This study type satisfied the criteria for level 4 evidence according to the OCEBM; future studies should be aimed toward higher levels of evidence. Significant publication bias was detected for all analyses (type of surgery and postoperative vocal fold assessment) except for the subgroup of 6 studies that included patients who underwent PDA ligation only and routine postoperative assessment. Recovery of Vocal Fold Function Recovery of vocal fold function warrants discussion. From the studies included in this analysis, 2 studies reported no recovery at follow-up points of 6 and 5 to 19 months, respectively.34,36 The population of patients with vocal fold paralysis in these studies was 6 and 7 patients, respectively.34,36 Zbar et al34 hypothesized that their high rate of nonrecovery resulted from the surgical clipping technique. Conversely, Khariwala et al22 reported a recovery rate of 82% (9 of 11 patients) among their single-center retrospective review of patients undergoing surgical repair of congenital cardiac

defects, attributing the rate of recovery to stretching of the recurrent laryngeal nerve and subsequent return of full function. The time frame for this recovery ranged from 8 weeks to 10 months.22 Carpes et al9 also reported recovery of vocal fold movement in 3 of 7 patients at 3 months’ follow-up. Spanos et al15 reported long-term follow-up of 6 patients with UVFP. Follow-up ranged from 1 to 18 months, and of the 6 patients, only 2 were found to have full recovery. Sachdeva et al19 reported follow-up in 9 patients with UVFP and found recovery of function in 3 patients, partial recovery in 4 patients, and no signs of recovery in 2 patients. Although excluded from our current analysis because their study population included only patients with UVFP, Truong et al41 reported a retrospective case series to determine the rate of recovery of pediatric vocal fold paralysis after cardiac surgery. They reported that 28 (35%) patients recovered function, with a median time from diagnosis to recovery of 6.6 months, and that 52 (65%) of patients had persistent paralysis, with a median follow-up time of 16.4 months. Furthermore, the authors reported that premature patients were significantly less likely to recover vocal fold function. Given the wide variation of results, additional investigation is needed to adequately determine recovery of vocal fold function after cardiac surgery. However, it should be noted that recovery of UVFP has been reported as late as 11 years after the initial surgery; therefore, the results showing poor recovery may simply reflect follow-up time that is too short.17

Radiesse Voice Gel). Cohen et al42 demonstrated the procedure to be a safe and effective treatment for carefully selected patients. Subjective or objective symptom improvement was experienced in 24 of 27 injections (89%). Zur43 reported her recent success with recurrent laryngeal nerve reinnervation using the ansa cervicalis for unilateral vocal fold immobility in children. Among 10 children (9 of whom had previous PDA ligation), 7 demonstrated physiologic frequency range improvement at 6 months’ follow-up. Median time from injury to repair was 64.5 months. Paniello et al44 reported the results of a multicenter randomized controlled trial comparing medialization laryngoplasty with laryngeal reinnervation and showed older patients to be better suited for laryngoplasty, whereas reinnervation was better suited for younger patients. Given these possible surgical interventions, adequate postoperative assessment of vocal fold function is warranted to identify patients who may benefit from these procedures. However, conservative management including voice therapy should always be considered before surgical intervention.

Surgical Management of UVFP

UVFP is a demonstrated risk of cardiothoracic surgery among infants and children. Pooled analysis suggests that it may be associated with a younger gestational age and lower birth weight and weight at time of surgery. Routine postoperativenasopharyngolaryngoscopyfor vocal cord assessment by an otolaryngologist is suggested.

Early identification of UVFP would allow subsequent surgical interventions such as medialization laryngoplasty (injection or surgical) or laryngeal reinnervation if appropriate. Injection medialization laryngoplasty was reviewed in 13 patients (27 injections) with a variety of injectable materials (Gelfoam, Radiesse Voice, or

Future Studies Future studies should focus on prospectivelyenrollingandfollowingpatients undergoing congenital cardiothoracic surgery, assessing vocal fold function routinelypostoperatively,anddetermining risk factors, comorbidities, and long-term respiratory function, swallowing, voice outcomes, and recovery rates.

CONCLUSIONS

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Unilateral Vocal Fold Paralysis After Congenital Cardiothoracic Surgery: A Meta-analysis Julie E. Strychowsky, Gavin Rukholm, Michael K. Gupta and Diane Reid Pediatrics 2014;133;e1708; originally published online May 19, 2014; DOI: 10.1542/peds.2013-3939 Updated Information & Services

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Unilateral vocal fold paralysis after congenital cardiothoracic surgery: a meta-analysis.

There is variation in the literature in regard to the occurrence of unilateral vocal fold paralysis (UVFP) after congenital cardiothoracic surgery. Th...
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