xRead - Swallowing Disorders in the Adult Patient (October 2024)

Dysphagia (2022) 37:1769–1776 https://doi.org/10.1007/s00455-022-10441-5

ORIGINAL ARTICLE

Does Medialization Improve Swallowing Function in Patients with Unilateral Vocal Fold Paralysis? A Systematic Review

Shumon I Dhar 1 · Marisa A. Ryan 2 · Ashley C. Davis 2 · Erin Jedlanek 3 · Kristine Pietsch 2 · Carrie Price 4 · Martin B. Brodsky 3,5 · Lee M. Akst 2

Received: 14 August 2021 / Accepted: 28 March 2022 / Published online: 12 April 2022 © The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature 2022

Abstract Glottal incompetence caused by unilateral vocal fold paralysis (UVFP) is a common cause of dysphagia and aspiration. Treat ments targeted at reducing glottal incompetence by injection augmentation or medialization thyroplasty are well established at improving voice outcomes, but improvements in swallowing function are less clear. The objective of this systematic review was to determine the impact of vocal fold medialization on dysphagia outcomes. Six electronic bibliographic databases and one clinical trial registry were searched on 3/13/2020. Our patient population were adult patients with verified UVFP that underwent vocal fold medialization. We limited review to prospective studies that had formal dysphagia assessment both before and after medialization. Nine studies met selection criteria (7 prospective case series and 2 prospective cohort studies) totaling 157 patients. The most common etiology of UVFP was iatrogenic (74/157; 47%). The majority of patients underwent injection augmentation (92/157; 59%), and the remaining underwent medialization thyroplasty. A variety of methods were used to assess changes in dysphagia including patient-reported outcome measures, flexible endoscopic evaluation of swal lowing, videofluoroscopic swallow study, and high-resolution manometry. 7/9 studies demonstrated clinically significant improvement in swallowing function following medialization; 4/9 studies demonstrated statistically significant improve ment, and three studies did not show statistically significant improvement after intervention. Study participants and outcome measures evaluating swallowing function in this review were heterogeneous. Moreover, the reviewed studies are concerning for multiple risks of bias impacting their conclusions. Taken together, this systematic review demonstrates limited evidence that injection augmentation and medialization thyroplasty improve swallowing function and/or safety. Keywords Vocal fold paralysis · Vocal fold augmentation · Dysphagia · Aspiration · Deglutition · Deglutition disorders · Systematic review

Lee M. Akst lakst1@jhmi.edu

* Shumon I Dhar

Shumon.Dhar@UTSouthwestern.edu Marisa A. Ryan

1 Department of Otolaryngology – Head & Neck Surgery, UT Southwestern Medical Center, 2001 Inwood Road, Dallas, TX 75390, USA 2 Johns Hopkins University, 601 North Caroline Street, Baltimore, MD 21287, USA 3 Department of Physical Medicine and Rehabilitation, Johns Hopkins University, 600 N. Wolfe St. ‑ Meyer 1‑160, Baltimore, MD 21287, USA 4 Towson University, 8000 York Road, Towson, MD 21252, USA 5 Department of Medicine, Division of Pulmonary and Critical Care Medicine, Johns Hopkins University, Baltimore, USA

mryan@jhmi.edu Ashley C. Davis adavi126@jhmi.edu Erin Jedlanek ejedlan1@jhmi.edu Kristine Pietsch kteets1@jhmi.edu Carrie Price carrieprice@towson.edu Martin B. Brodsky mbbrodsky@jhmi.edu

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Introduction Glottal incompetence as a result of unilateral vocal fold paralysis (UVFP) is a common cause of dysphagia and as many as two-thirds of patients suffering from UVFP will have dysphagia, with one-third to one-half of patients with UVFP showing evidence of aspiration [1]. UVFP can occur from a variety of etiologies including iatrogenic high vagal or recurrent laryngeal nerve (RLN) injury, stroke, neopla sia, cervical neck or intubation trauma, radiation treatment, chemotherapy side effect, or idiopathic causes [2]. The natu ral course of UVFP varies based on the etiology with iat rogenic UVFP patients having in general a great chance of recovery compared to those patients with idiopathic causes [3, 4]. The mechanism by which UVFP results in dysphagia is complex and multifactorial, and may include issues beyond glottal incompetence, such as delay of swallowing initiation, prolonged pharyngeal transit time, weakness of the phar yngeal musculature, reduced laryngopharyngeal sensation, and subsequent reduction in the laryngeal adductor reflex responsible for swallowing safety [2]. Treatment of UVFP, regardless of technique, focuses on reducing glottic insufficiency through various means such as injection augmentation, medialization thyroplasty, arytenoid adduction, and RLN reinnervation [1]. In adults, injection augmentation and medialization thyroplasty are the most commonly utilized and accepted approaches in treat ing UVFP [6]. Although the effect of these techniques on positive voice outcomes has been well studied, there is less consensus regarding their efficacy in improving swallowing parameters [7, 8]. The goal of this systematic review was to collect and ana lyze prospective evidence to determine whether vocal fold medialization procedures, such as injection augmentation or medialization thyroplasty, improve quantitative measures of swallowing function in adults with UVFP. Methods We conducted a systematic review and reported it in accord ance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [9]. Prior to initiation of the review process, we established a writ ten protocol for study inclusion, data extraction, and risk of bias assessment. The protocol was registered on 06/13/2020 with the Open Science Framework (https://d​ oi.o​ rg/1​ 0.1​ 7605/​ OSF.​IO/​567WF).

Inclusion Criteria

Included studies evaluated adult humans (18 years or older) who underwent vocal fold medialization for verified UVFP and who had a pre- and post-intervention dysphagia assess ment. Swallowing was evaluated using various instrumental assessments (e.g., flexible endoscopic evaluation of swal lowing [FEES] or videofluoroscopic swallow study [VFSS]) and patient- or clinician-reported outcomes. Swallowing evaluations had to occur within 6 months pre-intervention and 12 months post-intervention. There were no exclusions based on language. In addition, we chose to limit our identification of eligible research to prospective studies because they are better able to control for the collection of outcomes data specific to this exposure. That is, these study methods allow for greater completion of the data collected and improved control of the temporal association between vocal fold medialization (exposure) and the potential consequences of this treatment (outcomes) [10–12]. Exclusion criteria included (1) retrospective study design, editorials, viewpoints, letters to the editor, cases series with ≤ 3 patients, and reviews, (2) patients <18 years old, (3) patients with bilateral vocal fold paralysis or vocal fold paresis, (4) patients with prior treatment for UVFP such as injection augmentation, thyroplasty +/- arytenoid adduction before study enrollment, (5) patients with pre-existing dys phagia due to etiologies other than UVFP, (6) patients with esophageal disease other than reflux, and (7) patients with central nervous system disease, connective tissue disorders, head and neck tumors (other than thyroid), and history of radiation or surgery to the oral cavity or pharynx. A medical librarian with expertise in systematic review methods and searching (C.P.) developed and executed the search after consulting with the research team. The search was developed based on key articles selected by the team. Prior to running the searches in each database, the search was peer-reviewed by a second medical librarian. The search was completed in PubMed through NCBI, Embase through Elsevier, the Cochrane Library on the Wiley Platform, CINAHL Plus through EBSCO, the Web of Science Core Collection, and Scopus through Elsevier, ProQuest Dis sertations and Theses Global database, and Open Access Thesis Dissertations as part of the gray literature from data base inception to 03/13/2020. An update was completed on Exclusion Criteria Literature Search

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hyaluronic acid, calcium hydroxyapatite, fat, Silastic, Teflon, Gore-Tex, Proplast), timing of procedure, type of swallowing assessment (i.e., self-reported scale, clinician reported/symptom assessment, clinical screening tool (e.g., Yale Swallow Protocol [15]), VFSS, FEES, or high resolution manometry [16–18]), timing of pre- and post intervention dysphagia assessment, and need for speech language pathology (SLP) directed swallowing therapy post-intervention. Both statistical and clinical significance of dysphagia outcomes were extracted. Each study also underwent risk of bias assessment using the rules established by the Cochrane Collaboration [19]. Studies were judged on 7 risk parameters (study rationale, study objectives, selection criteria, study replication, sam pling, detection bias, attrition bias, avoidance, and report ing bias) to have either low, unknown, or high risk of bias.

07/12/2021. Note that PubMed contains MEDLINE and that the Cochrane Library contains the Cochrane Register of Controlled Trials (CENTRAL). Additionally, a search was completed in the ClinicalTrials.gov trial registry. The searches contained three concepts: vocal fold paralysis, vocal fold medialization, and swallowing outcomes. Con trolled vocabulary, such as Medical Subject Headings and Emtree, was used where appropriate, in combination with free text keywords. No published search filters were used, and no limits were applied. The search was peer-reviewed by another medical librarian. There were 6503 total results, 3615 duplicates removed, and 2888 remaining results, which were then uploaded to the Covidence platform for title and abstract screening [13]. Zotero was used for citation manage ment [14]. The search strategies for every platform can be found in the Appendix. Five authors (A.C.D., E.J., K.M.P., M.A.R, and S.I.D) independently screened the title and abstract of identified studies using Covidence software (www.c​ovide​nce.o​ rg, Mel bourne, VIC, Australia). Two authors (S.I.D and M.A.R) then independently reviewed the full text of the remaining studies. All disagreements were resolved by a senior author (L.M.A). Study authors were directly contacted via email for missing information as needed. Prospective studies that met all criteria were then subjected to data extraction, risk of bias assessment, and outcomes analysis. The search update conducted on 7/12/2021 had a data range of 1/1/2020-7/12/2021. The same five authors per formed the title and abstract screening, and full-text review was conducted by two authors (S.I.D and L.M.A). Disagree ments were resolved by senior author (M.B.B). Data extraction and risk of bias assessment for each study meeting criteria for final review were completed indepen dently by two authors (S.I.D and M.A.R.) with data entry into a Qualtrics (2019) online form. The data were then downloaded and reviewed by a third author (M.B.B.) for completeness and disagreements. Disagreements were identified and settled with discussion and refereed by a fourth author (L.M.A). Data extracted included study date, country of first author, funding sources (government organization, association, institutional commercial, other), study type (case series, cohort, or other type), study N, study patient demographics (age, sex), cause of UVFP, method of identifying the paralysis (flexible laryngos copy with stroboscopy, flexible laryngoscopy without stroboscopy, rigid laryngoscopy, laryngoscopy not other wise specified, during FEES, laryngeal mirror, or other), type of medialization procedure (injection augmentation, transcervical medialization implant, transoral medializa tion implant) and material used (carboxymethylcellulose, Data Extraction and Risk of Bias Assessment

Statistical Methods

Descriptive statistics including proportions, means, stand ard deviations, medians, and interquartile ranges were calculated using Microsoft Excel 2019. A meta-analysis was not pursued due to substantial heterogeneity in study methods and reporting for included studies.

Results

Study Selection

We identified 2888 studies from the electronic database search and 26 additional studies from the gray literature (Fig. 1). After removing duplicates, we reviewed the titles and abstracts of 2786 studies and included 142 for full text review. On full-text review, we excluded 133 studies because of either wrong study type or study methods. The 9 remaining studies were reviewed for data extraction and risk of bias assessment; these studies contained a total of 157 patients for qualitative analysis (Table 1). The 9 studies included 7 prospective case series [20–28] and 2 prospective cohort studies [20, 23]. The studies came from 5 different countries and 1 required translation from Japa nese into English for review [26]. The 7/12/2021 search update resulted in 301 articles from which 54 duplicates were removed, leaving 247 refer ences for independent title and abstract screen. Fourteen articles met criteria for full-text review. All 14 articles were excluded due to either having an excluded article type (e.g., retrospective design) or excluded methods (e.g., no swallowing evaluation).

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Records iden fied through database searching (n = 2888)

Addi onal records iden fied through other sources (n = 26)

Screening Included Eligibility Iden fica on

Records a er duplicates removed (n = 128)

Records screened (n = 2786)

Records excluded (n = 2644)

Full-text ar cles assessed for eligibility (n = 142)

Full-text ar cles excluded, with reasons (n = 133): 74 (56%) - Wrong ar cle type 59 (44%) - Wrong study methods

Studies included in qualita ve synthesis (n = 9)

Fig. 1 PRISMA 2009 Flow Diagram

Clinical Presentation

Medialization Procedure

The patients’ mean age was 60 (SD = 8 years) across the 7 studies that reported age, and 50% (46/92) of patients were female across the 6 studies that reported sex (Table 1). The most common etiology of the UVFP was iatrogenic from surgery (74/157; 47%) (Table 2). The UVFP was identi fied most frequently by laryngoscopy with stroboscopy (62/157; 39%). The studies utilized a broad variety of meth ods to identify dysphagia before medialization and no single method prevailed (Table 3). Only 3 studies reported when the swallowing evaluation occurred before the procedure, each <1 month before the procedure.

Most studies (6/9; 67%) did not specify when the pro cedure was performed after the initial diagnosis of UVFP. The time intervals that were reported ranged from months to >1 year. At the level of individual stud ies, 4 studies used only injection augmentation, 3 stud ies used medialization thyroplasty, and 2 studies used both (Table 1). When analyzed by number of patients, the majority underwent injection augmentation of the paralyzed vocal fold (92/157; 59%), most commonly reported using Restylane (a form of hyaluronic acid) (20/92, 22%) or autologous fat (20/92, 22%) (Table 1,

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Table 1 Summary of all included prospective studies on dysphagia outcomes after vocal fold medialization in adults with unilateral vocal fold paralysis

Study

Country Prospective Study type Funding

Study N Sex (M/F)

Age: Mean (SD) or Median (IQR)

Injection medialization/ Medialization Implant

Abdel-Aziz, 1998 England Cohort

None None None None None None None

12 (5/7)

56 (63, 52)

Implant Implant

Atallah, 2019

France Case series

22 23 20

Bhattacharyya, 2002 U.S.

Case series

62 (13)

Injection ( n =17), Implant ( n =6) Injection ( n =10), Implant ( n =10)

Dworkin, 2006 Kammer, 2019 Ohmae, 1995 Pinna, 2019 Wang, 2012

U.S. U.S.

Cohort

Case series

Institutional 17 (11/6)

69 (54, 73) 59 (SD=NR) 72 (55, 76) 50 (IQR=NR)

Injection Injection Injection Implant Injection

Laccourreye, 1999 France Case series

20 (13/7)

Japan Case series

8 (6/2)

Brazil

Case series

15 (5/10)

Taiwan Case series

Institutional 20 (6/14)

52 (44, 62)

Totals

2/10

N = 157 7/9

Injection (n=92), Implant ( n =65)

IQR interquartile range, U.S. United States, SD standard deviation

Table 2 Characteristics of included patients’ unilateral vocal fold paralysis and its treatment types (N=157)

Table 3 Dysphagia evaluations and outcomes in adult patients with unilateral vocal fold paralysis treated with vocal fold medialization.

N (%) a

Characteristics

Methods

Number of studies a

Etiology of paralysis Intubation

Swallowing function PRE-procedure Patient-reported scale Clinician-reported/symptom assessment Videofluoroscopic Swallow Study

3 (2)

2 2 3 3 3 3 5 3 2

Idiopathic

14 (9)

Neurological

2 (1)

Surgical Trauma

74 (47)

Endoscopy Manometry

5 (3)

Tumor

15 (10) 43 (27)

Other

Unspecified/Not clear Other (aortic aneurysm) Identification of paralysis Laryngoscopy WITH strobe Laryngoscopy WITHOUT strobe

Swallowing function POST-procedure Patient-reported scale Videofluoroscopic Swallow Study

1 (1)

62 (39) 55 (35) 40 (25) 20 (22) 10 (11) 20 (22) 14 (15) 3 (3)

Endoscopy Manometry

3 Determination of changes in swallowing function POST-procedure Physiologic measurements 3 Swallowing event parameters 1 Determination of aspiration 5 Patient Reported Outcome Measures (PROMs) 5 Pharyngeal clearance of contrast 1

Other

Injection augmentation material (N= 92) Restylane

Cymetra

Teflon

Fat

Gel foam Silicone

8 (9)

a Studies may have used more than one method

Other* (Juvederm, Radiesse “most frequently”) Medialization implant approach and material (N = 65) Transcervical–silastic

17 (18)

27(42) 22 (33) 16(25)

Swallowing Outcomes

Transoral - silastic

Transcervical – material unspecified

Timing of swallowing reassessment after the procedure var ied from “immediately” to 12 months post procedure. Four of the studies re-evaluated swallowing at multiple different intervals separated by month(s) within the first year after the procedure. A variety of methods were used to identify and determine changes in swallowing after the procedure and some studies used more than one method (Table 3).

a Studies may have used more than one method

2). The remaining patients underwent medialization thy roplasty, most commonly with an transcervical-silastic (27/65; 42%) followed by transoral-silastic (22/65, 33%) (Table 1, 2).

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criteria (5/9; 56%), patient sampling (6/9; 67%), detection bias (7/9; 78%), and avoidance bias (4/9; 44%).= 92)

Patient-reported outcome measures (PROMs) such as a patient-reported scale and a determination of the presence of aspiration on an instrumental assessment (i.e., FEES or VFSS) were employed most frequently, each in 5 studies. Patients underwent some form of therapy with SLP for dysphagia in addition to the medialization procedure in 8/9 (89%) studies, but the timing and extent of therapy were unspecified in all cases. In 4 studies, a statistically significant improvement in swallowing function after the procedure was reported, [21, 26–28] although 3 studies demonstrated no statistically significant improvement [22–24]. The two remaining studies only reported descriptive statistics without statistical testing for swallowing outcomes [20, 25]. Authors concluded clinically significant improvement in swallowing function in 7/9 (78%) studies [20, 21, 23, 25–28], includ ing one study where the improvement was not statistically significant [23]. Risk of bias assessments is summarized in Table 4. All studies provided adequate rationale, stated clear objectives, and were free of commercial support. Most studies mini mized attrition (7/9; 78%) and reporting bias (7/9; 78%) and provided sufficient information for study replication (6/9; 67%). Areas of methodological weakness included selection Risk of Bias

Discussion This systematic review suggests that treatment of UVFP in adults with vocal fold medialization procedures of injec tion augmentation or medialization thyroplasty can improve swallowing outcomes. However, statistically significant improvement in swallowing outcome measures was not consistently identified. In part, this may be due to the het erogeneity of patient selection criteria, operative technique/ type of augmentation material, and method of swallowing assessment. Post-procedure swallowing assessment varied among PROMs, VFSS, FEES, or high-resolution manome try. The outcome measures varied even among studies using VFSS. For instance, in studies assessed via VFSS, binary presence or absence of aspiration, Penetration–Aspiration Scale (PAS) score, an alternative scoring system, or another type of descriptive analysis of swallowing pathology were all utilized [20, 22, 25]. A recent systematic review reported the effects of injec tion laryngoplasty on aspiration in patients with acute iatro genic vocal fold paralysis [29]. This review included a wide

Table 4 Risk of bias assessment

Reference

Study Type

Avoidance Bias

Reporting Bias

Government/

Rationale ̵̵ ̵̵ ̵̵ ̵̵ ̵ ̵̵ ̵̵ ̵̵ ̵ Clear Objective(s) Selection Criteria Replication Sampling Detection Bias Attrition Bias

Institutional/

Commercial Support

Abdel-Aziz 1998 x

Cohort

Atallah 2019 x

Case Series

Bhattacharyya 2002 x Case Series

Dworkin 2006 x Kammer 2019 x

Cohort

Case Series Case Series Case Series Case Series Case Series

Laccourreye 1999 x

Ohmae 1995 x Pinna 2019 x Wang 2012 x

Key: = low risk of bias; = unknown risk of bias; = high risk of bias. - absent, ✓ present

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Conclusion We conclude there is moderate evidence to support the use of vocal fold medialization to improve swallowing function in patients with UVFP. However, the heterogeneity of study populations, variations in intervention technique, variations in outcome measures, and other confounding variables limit our ability to determine the clinical impact and strength of vocal fold medialization as an intervention. Further prospec tive clinical studies with control groups and validated out come measures (e.g., Eating Assessment Tool, SWAL-QOL, penetration–aspiration scale, pharyngeal contractile integral [30–33]) will be necessary to better isolate the effect of vocal fold medialization on swallowing function in UVFP patients. Supplementary Information The online version contains supplemen tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​00455-0​ 22-1​ 0441-5. Author Contributions SID: co-first author writer, title and abstract reviewer, full-text reviewer; MAR: co-first author, writer, title and abstract reviewer, full-text reviewer; ACD: title and abstract reviewer; EJ: title and abstract reviewer; KP: title and abstract reviewer; CP: manuscript editing, medical librarian; MBB: co-senior author, manu script editing, study design; LMA: co-senior author, manuscript edit ing, study design References 1. Misono S, Merati AL. Evidence-based practice: evaluation and management of unilateral vocal fold paralysis. Otolaryngol Clin North Am. 2012;45:1083–108. 2. Cates DJ, Kuhn MA. Management of dysphagia in unilateral vocal fold paralysis. In: Amin MR, Johns MM, editors. Decision mak ing in vocal fold paralysis: a guide to clinical management [Inter net]. Cham: Springer International Publishing; 2019 [cited 2021 Mar 6]. pp. 41–55. https://d​ oi.o​ rg/1​ 0.1​ 007/9​ 78-3-0​ 30-2​ 3475-1_4. 3. Husain S, Sadoughi B, Mor N, Sulica L. Time Course of Recovery of Iatrogenic Vocal Fold Paralysis. Laryngoscope. 2019;129:1159–63. 4. Husain S, Sadoughi B, Mor N, Levin AM, Sulica L. Time course of recovery of idiopathic vocal fold paralysis. Laryngoscope. 2018;128:148–52. 5. Sridharan SS, Rosen CA. Diagnostic studies in workup for vocal fold paralysis: when and why. In: Amin MR, Johns MM, edi tors. Decision making in vocal fold paralysis: a guide to clini cal management. Cham: Springer International Publishing; 2019 [cited 2021 Mar 6]. pp. 3–12. https://​doi.​org/​10.​1007/​ 978-3-​030-​23475-1_1. 6. Tam S, Sun H, Sarma S, Siu J, Fung K, Sowerby L. Medialization thyroplasty versus injection laryngoplasty: a cost minimization analysis. J Otolaryngol Head Neck Surg. 2017;46:14. Declarations Conflict of interest Martin B Brodsky PhD ScM discloses a relation ship with MedBridge, Inc. No other conflicts of interest to disclose by other authors.

range of study designs, including lower quality retrospec tive cohort and case studies. Outcomes measures included “clinical assessment,” FEES or VFSS interpretation, PAS, or advancement of diet. Of the 14 studies they included, only 3 overlapped with studies included in our review [22, 24, 25]. The authors concluded that evidence to support injec tion laryngoplasty in treating aspiration in patient with acute iatrogenic UVFP was inconclusive and called for prospective studies with quantitative measures being needed [29]. This differed from our review’s objectives and method ology in several categories. Our patient population had a wider scope and included patients with dysphagia and all cause UVFP including not only iatrogenic, but also idio pathic, neurological, traumatic, and others. In our review, interventions were not limited to injection augmentation, and included other types of medialization procedures (e.g., thyroplasty). In addition, swallowing function—not solely the presence of aspiration—was assessed both pre- and post intervention as a criterion for study inclusion. Despite the rigorous methodology employed in an effort to clarify impact of medialization on swallowing function in patients with UVFP, we still encountered several limita tions in the present study. There was substantial missing data from the studies reviewed, especially for patient demograph ics, how vocal fold paralysis was verified, material used for injection, timing of the pre-procedure swallowing assess ment, timing of the procedure after the diagnosis of UVFP, and details about therapy with SLP. For some of the studies, dysphagia was the secondary outcome and voice was pri mary outcome. Therefore, not all patients included necessar ily had dysphagia despite their UVFP, possibly limiting the potential study outcomes. For instance, one study reported 8 of 12 patients had pre-procedure aspiration, whereas another study included all patients with a PAS >3, suggesting greater compromise to airway protection [20, 24]. We also limited studies to only those with prospective study designs, perhaps influencing prevalence estimates. With regard to our selection criteria, by excluding patients with CNS disorders, neoplasms of the head and neck, and connective tissue disorders, this study is limited in its generalizability—by design, the results presented here are applicable only to patients with isolated TVCP as it relates to their dysphagia. The authors recognize this limita tion and feel that it is a reasonable trade-off in order to limit the confounding effect that non-TVCP etiologies of dyspha gia may have had on ability to discern impact of vocal fold medialization. Lastly, despite our strict criteria, it was challenging to identify cases with comorbid conditions that could be con founding such as esophageal cancer, other cranial neuropa thies, radiation to the head and neck as this was not always reported.

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after vocal fold injection medialization for unilateral vocal fold paralysis/paresis. Head Neck. 2019;41:2389–97. 25. Laccourreye O, Paczona R, Ageel M, Hans S, Brasnu D, Crevier Buchman L. Intracordal autologous fat injection for aspiration after recurrent laryngeal nerve paralysis. Eur Arch Otorhinolaryn gol. 1999;256:458–61. 26. Ohmae Y, Kitahara S, Tamura E, Karaho T. Inouye T [Effects of transcutaneous silicon injection for aspiration caused by uni lateral vocal cord paralysis]. Nihon Jibiinkoka Gakkai Kaiho. 1995;98:1788–95. 27. Pinna BR, Herbella FAM, de Biase N. Pharyngeal motility in patients submitted to type I thyroplasty. Braz J Otorhinolaryngol. 2019;S1808–8694(19):30155–7. 28. Wang C-C, Chang M-H, Wang C-P, Liu S-A, Liang K-L, Wu S-H, et al. Laryngeal electromyography-guided hyaluronic acid vocal fold injection for unilateral vocal fold paralysis–preliminary results. J Voice. 2012;26:506–14. 29. Pan S, Sadoughi B. Effectiveness of injection laryngoplasty for aspiration in acute iatrogenic vocal fold paralysis: a systematic review. The laryngoscope [Internet]. [cited 2021 Jun 21];n/a. http://onlinelibrary.wiley.com/doi/abs/https://​doi.​org/​10.​1002/​ lary.​29326 30. Belafsky PC, Mouadeb DA, Rees CJ, Pryor JC, Postma GN, Allen J, et al. Validity and reliability of the Eating Assessment Tool (EAT-10). Ann Otol Rhinol Laryngol. 2008;117:919–24. 31. McHorney CA, Martin-Harris B, Robbins J, Rosenbek J. Clinical validity of the SWAL-QOL and SWAL-CARE outcome tools with respect to bolus flow measures. Dysphagia. 2006;21:141–8. 32. Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8. 33. O’Rourke A, Humphries K, Lazar A, Martin-Harris B. The phar yngeal contractile integral is a useful indicator of pharyngeal swallowing impairment. Neurogastroenterol Motil. 2017. https://​ doi.​org/​10.​1111/​nmo.​13144. Publisher's Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

7. Birkent H, Sardesai M, Hu A, Merati AL. Prospective study of voice outcomes and patient tolerance of in-office percutaneous injection laryngoplasty. Laryngoscope. 2013;123:1759–62. 8. Sulica L, Rosen CA, Postma GN, Simpson B, Amin M, Courey M, et al. Current practice in injection augmentation of the vocal folds: indications, treatment principles, techniques, and complications. Laryngoscope. 2010;120:319–25. 9. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred report ing items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097. 10. Peinemann F, Tushabe DA, Kleijnen J. Using Multiple Types of Studies in Systematic Reviews of Health Care Interventions—A Systematic Review. PLoS One. 2013;8:e85035. 11. OCEBM Levels of Evidence — Centre for Evidence-Based Medi cine (CEBM), University of Oxford [Internet]. [cited 2021 Mar 22]. https://​www.​cebm.​ox.​ac.​uk/​resou​rces/​levels-​of-​evide​nce/​ ocebm-​levels-​of-​evide​nce 12. Chapter 25: Assessing risk of bias in a non-randomized study [Internet]. [cited 2022 Jan 2]. https://t​raini​ng.c​ochra​ne.o​ rg/h​ andb​ ook/​curre​nt/​chapt​er-​25 13. Covidence - Better systematic review management [Internet]. Covidence. [cited 2021 Jul 18]. https://​www.​covid​ence.​org/ 14. Zotero | Your personal research assistant [Internet]. [cited 2021 Jul 18]. https://​www.​zotero.​org/ 15. Suiter DM, Sloggy J, Leder SB. Validation of the Yale Swallow Protocol: a prospective double-blinded videofluoroscopic study. Dysphagia. 2014;29:199–203. 16. Belafsky PC, Kuhn M. The Clinician’s Guide to Swallowing Fluoroscopy [Internet]. New York: Springer-Verlag; 2014 [cited 2019 Jan 28]. //www.​sprin​ger.​com/​us/​book/​97814​93911​080 17. Langmore SE, Schatz K, Olsen N. Fiberoptic endoscopic exami nation of swallowing safety: a new procedure. Dysphagia. 1988;2:216–9. 18. Omari TI, Ciucci M, Gozdzikowska K, Hernández E, Hutcheson K, Jones C, et al. High-resolution pharyngeal manometry and impedance: protocols and metrics-recommendations of a high resolution pharyngeal manometry international working group. Dysphagia. 2020;35:281–95. 19. Higgins JPT, Altman DG, Gøtzsche PC, Jüni P, Moher D, Oxman AD, et al. The Cochrane collaboration’s tool for assessing risk of bias in randomised trials. BMJ. 2011;343:d5928. 20. AbdelAziz MF, el-Hak NA, Carding PN. Thyroplasty for func tional rehabilitation of the incompetent larynx. J Laryngol Otol. 1998;112:1172–5. 21. Atallah I, Manjunath MK, Castellanos PF. Transoral silastic medialization for unilateral vocal fold paralysis. Head Neck. 2019;41:2947–51. 22. Bhattacharyya N, Kotz T, Shapiro J. Dysphagia and aspiration with unilateral vocal cord immobility: incidence, characterization, and response to surgical treatment. Ann Otol Rhinol Laryngol. 2002;111:672–9. 23. Dworkin JP, Shah AG, Stachler RJ, Meleca RJ. Medialization thyroplasty versus injection laryngoplasty for unilateral vocal fold paralysis: A comparative analysis of functional outcomes. J Med Speech-Lang Pathol. 2006;14:1–11. 24. Kammer RE, Jones CA, Johnson AM, Dailey SH, McCulloch TM, Thibeault SL. High-resolution manometry and swallow outcomes

Shumon I. Dhar MD Marisa A. Ryan MD, MPH Ashley C. Davis MS Erin Jedlanek MS Kristine M. Pietsch MA Carrie Price MLS Martin B. Brodsky PhD ScM Lee M. Akst MD

1 3

Invited Article

Otolaryngology – Head and Neck Surgery 2023, Vol. 168(4) 571 – 592

Expert Consensus Statement: Management of Dysphagia in Head and Neck Cancer Patients

© 2023 American Academy of Otolaryngology – Head and Neck Surgery Foundation.

DOI: 10.1002/ohn.302 http://otojournal.org

Maggie A. Kuhn, MD, MAS 1 , M. Boyd Gillespie, MD, MSc 2 , Stacey L. Ishman, MD, MPH 3 , Lisa E. Ishii, MD, MHS 4 , Rebecca Brody, PhD, RD, CNSC 5 , Ezra Cohen, MD, FRCPSC, FASCO 6 , Shumon I. Dhar, MD 7 , Kate Hutcheson, PhD 8 , Gina Jefferson, MD 9 , Felicia Johnson, MD 10 , Anais Rameau, MD, MPhil 11 , David Sher, MD, MPH 7 , Heather Starmer, MA, CCC-SLP, BCS-S 12 , Madeleine Strohl, MD 13 , Karen Ulmer, MS, RN, CORLN 14 , Vilija Vaitaitis, MD 15 , Sultana Begum, MPH 16 , Misheelt Batjargal, MD, MHA 16 , and Nui Dhepyasuwan, MEd 16

warranted to address additional controversies related to dysphagia in HNC patients.

Abstract Objective. To develop an expert consensus statement (ECS) on the management of dysphagia in head and neck cancer (HNC) patients to address controversies and offer oppor tunities for quality improvement. Dysphagia in HNC was de fi ned as swallowing impairment in patients with cancers of the nasal cavity, paranasal sinuses, nasopharynx, oral cavity, oropharynx, larynx, or hypopharynx. Methods. Development group members with expertise in dysphagia followed established guidelines for developing ECS. A professional search strategist systematically reviewed the literature, and the best available evidence was used to compose consensus statements targeted at providers mana ging dysphagia in adult HNC populations. The development group prioritized topics where there was signi fi cant practice variation and topics that would improve the quality of HNC patient care if consensus were possible. Results. The development group identi fi ed 60 candidate consensus statements, based on 75 initial proposed topics and questions, that focused on addressing the following high yield topics: (1) risk factors, (2) screening, (3) evaluation, (4) prevention, (5) interventions, and (6) surveillance. After 2 iterations of the Delphi survey and the removal of duplicative statements, 48 statements met the standardized de fi nition for consensus; 12 statements were designated as no consensus. Conclusion. Expert consensus was achieved for 48 state ments pertaining to risk factors, screening, evaluation, prevention, intervention, and surveillance for dysphagia in HNC patients. Clinicians can use these statements to improve quality of care, inform policy and protocols, and appreciate areas where there is no consensus. Future research, ideally randomized controlled trials, is

1 Department of Otolaryngology-Head and Neck Surgery, University of California Davis, Sacramento, California, USA 2 Department of Otolaryngology-Head and Neck Surgery, University of Tennessee Health Science Center, Memphis, Tennessee, USA 3 Department of Otolaryngology, Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio, USA 4 Department of Otolaryngology-Head & Neck Surgery, Johns Hopkins University Medical Institute, Cockeysville, Maryland, USA 5 Department of Clinical and Preventive Nutrition Sciences, Rutgers University, West Linn, Oregon, USA 6 Moores Cancer Center at UC San Diego Health, La Jolla, California, USA 7 UT Southwestern Medical Center, Dallas, Texas, USA 8 Department of Head and Neck Surgery, Division of Surgery, The University of Texas MD Anderson Center, Houston, Texas, USA 9 Department of Otolaryngology-Head & Neck Surgery, Division of Head & Neck Surgical Oncology/Microvascular Reconstruction, University of Mississippi Medical Center, Jackson, Mississippi, USA 10 ENT Ozarks, Springdale, Arkansas, USA 11 Department of Otolaryngology-Head and Neck Surgery, Weill Cornell Medicine, New York City, New York, USA 12 Department of Otolaryngology-Head and Neck Surgery, Stanford University, Stanford, California, USA 13 Department of Otolaryngology-Head and Neck Surgery, University of California-San Francisco, San Francisco, California, USA 14 Milton J Dance, Jr Head and Neck Cancer at GBMC, Baltimore, Maryland, USA 15 Department of Otolaryngology-Head and Neck Surgery, Louisiana State University Health Science Center, New Orleans, Charleston, South Carolina, USA 16 American Academy of Otolaryngology-Head and Neck Surgery Foundation, Alexandria, Virginia, USA Corresponding Author: Maggie A. Kuhn, MD, MAS, Department of Otolaryngology – Head and Neck Surgery, University of California Davis, 2521 Stockton Boulevard Suite 7200, Sacramento, CA 95817-2207, USA. Email: makuhn@ucdavis.edu

10976817, 2023, 4, Downloaded from https://aao-hnsfjournals.onlinelibrary.wiley.com/doi/10.1002/ohn.302, Wiley Online Library on [08/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

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Otolaryngology – Head and Neck Surgery 168(4)

access to timely and evidence ‐ based swallowing evaluation, management, and education for HNC patients and their families. 11,12 Reasons for disparities in dysphagia care among HNC patients include the predominant focus on cancer treatment with reduced emphasis on the management of cancer ‐ related complications, lack of appropriate resources or expertise, and con fl icting evidence supporting which inter ventions are most likely to improve dysphagia ‐ related outcomes. As a result, there is substantial practice variation in the management of HNC ‐ related dysphagia, with many patients referred for dysphagia evaluation months to years after HNC treatment, if they are ever referred at all. 12 Given discrepancies in care and substantial knowledge gaps, the management of dysphagia in HNC patients was selected as a topic for expert consensus statement (ECS) development by the American Academy of Otolaryngology ‐ Head and Neck Surgery Foundation (AAO ‐ HNSF) Guidelines Task Force (GTF). The objective of this ECS is to formulate areas of consensus among a group of experts in the fi eld to identify potential methods to reduce the burden of dysphagia in HNC patients from the time of diagnosis and throughout the lifespan. The primary aim was to highlight areas of controversy and identify opportunities to improve the recognition and rehabilitation of swallowing impairment, as well as to reduce the severity and duration of dysphagia and its impact on the quality of life in the HNC population. Methods This ECS was developed according to an a priori protocol 13 (previously used by AAO ‐ HNS to successfully develop other consensus statements) with the following steps: (1) de fi ne the subject of the ECS as management of dysphagia in HNC patients, (2) recruit the expert development group, (3) vet potential con fl icts of interest among proposed development group members, (4) per form a systematic literature review, (5) determine the scope and population of interest for the ECS, (6) develop topic questions and consensus for statements for each topic question, (7) develop and implement modi fi ed Delphi method surveys, (8) revise the ECS in an iterative fashion based on survey results, and (9) aggregate the data for analysis and presentation. The pertinent details of each of these steps will be brie fl y described. The topic of “ Prevention and Management of Dysphagia in Head & Neck Cancer Patients ” was proposed for an ECS by the AAO ‐ HNS Airway and Swallowing Committee. After deliberation, the AAO ‐ HNSF GTF approved and prioritized the suggestion; development group leadership was selected; and administrative support was allocated. Development group membership was strategically established to ensure appropriate representation of all relevant stakeholder groups and organizations within otolaryngology, head and neck ECS Topic Clari fi cation, Scope Re fi nement, and Development Group Recruitment

Keywords dysphagia, head and neck cancer, laryngeal cancer, nasophar yngeal cancer, oral cavity cancer, oropharyngeal cancer, radiation, swallowing

Received September 8, 2022; accepted February 1, 2023.

S wallowing is a life ‐ sustaining function that is critical for hydration, nutrition, management of secretions, and consumption of required medications. Swallowing function also contributes to the quality of life through the enjoyment of food and beverage, the social interaction of mealtime, and the shared cultural experience of the cuisine. Safe and ef fi cient swallowing is the result of a series of complex and well ‐ coordinated voluntary and involuntary musculoskeletal actions which are intricately regulated via mucosal sensory receptors, cranial nerves, brainstem centers, and higher cortical controls. Disruption of one or multiple of these components may result in the development of swallowing symptoms, or dysphagia. Dysphagia at diagnosis is common in head and neck cancer (HNC) patients due to tumor involvement of upper aerodigestive tissues important for normal swal lowing. Dysphagia is reported at presentation in up to 28% of all HNC patients, and in up to 50% of patients with pharyngeal cancers. 1 Dysphagia is also an acute and chronic side effect of HNC treatment due to the traumatizing effects of surgery, radiation, and che motherapy on the tissues of the upper aerodigestive tract. Therefore, dysphagia prevalence typically increases from disease presentation through treatment to long ‐ term posttreatment surveillance, ultimately affecting up to 45% to 75% of HNC survivors. 2,3 With the global incidence of HNC increasing by 36% over the past decade, partly driven by increasing numbers of human papillomavirus ‐ associated oropharyngeal cancers in younger patients, the prevalence of survivors with 4 HNC ‐ related dysphagia is likewise expected to increase into the foreseeable future. 5 HNC patients with dysphagia are at risk of complica tions including medication noncompliance, malnutrition, dehydration, pneumonia, and death. 6,7 Aspiration pneu monia has been observed in 24% of HNC patients treated with chemoradiotherapy over a 5 ‐ year period. 8 Outcomes from aspiration among HNC patients are poor with reports of approximately one ‐ third of those hospitalized dying within 30 days of admission. 8 Additionally, HNC patients with dysphagia have signi fi cantly reduced quality of life and higher rates of anxiety and depression as well as decisional regret 9 about their cancer treatment compared to those without dysphagia. 10 Despite increasing awareness that modern organ ‐ preservation treatment protocols do not necessarily translate into function preservation, there continues to be limited

10976817, 2023, 4, Downloaded from https://aao-hnsfjournals.onlinelibrary.wiley.com/doi/10.1002/ohn.302, Wiley Online Library on [08/07/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

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Kuhn et al.

oncology, speech ‐ language pathology, and nutrition. The stakeholders were contacted regarding the consensus statement project and the requirements and desired quali fi ca tions for development group membership; each group then nominated its own representative content expert to participate. The ECS development group included representa tives from the American Society for Radiation Oncology; the Society of Otorhinolaryngology and Head ‐ Neck Nurses; the American Broncho ‐ Esophagological Association; the American Head and Neck Society (AHNS); the American Society of Clinical Oncology; the American Speech ‐ Language ‐ Hearing Association; the Dysphagia Research Society; the Academy of Nutrition and Dietetics (AND); and appropriate committees within the AAO ‐ HNS, including the Head and Neck Surgery and Oncology Committee, the Airway and Swallowing Committee, the Board of Governors, and the Section for Residents and Fellows. The methodologists and the representa tive from the AND were the only nonvoting members of the development group. All proposed nominees for the development group practiced in the United States. All development group members are in active clinical practice, are content experts in dysphagia, and agreed in advance of the appointment to participate in all verbal discussions (performed via teleconference) and votes. Once the development group was assembled, the complete disclosure of potential con fl icts of interest was reported and vetted. Con fl icts of interest were managed consistent with the Council of Medical Specialty Societies Code for Interactions With Companies , 14 which requires that the chair and a majority of the participants do not have a direct con fl ictwith the deliberations. The development group chair and assistant chair led the development of the consensus statements and the Delphi process with input from 2 methodologists from AAO ‐ HNSF leadership and GTF, and with administrative support from an AAO ‐ HNSF staff liaison. The title of the ECS was adjusted to remove the word “ prevention ” as the development group felt that “ prevention ” was fully encompassed in “ management. ” The target audience of the ECS was de fi ned as otolaryngologists, radiation oncologists, speech ‐ language pathologists (SLP), oncology nurses, registered dietitian nutritionists (RDN), and medical oncologists who manage dysphagia, in HNC populations. The target population was de fi ned as adults with HNC who are 18 years or older. “ Dysphagia ” was de fi ned as swallowing impairment. Once the target popula tion and scope of practice were determined, the development group used the results of the literature reviews, combined with their expert opinion and stakeholder needs, to propose topics and questions for which knowledge gaps, uncertainty, or opportunities for quality improvement existed. Topics were focused on areas with signi fi cant practice variation that would most bene fi t from consensus from expert clinicians. These topics and questions were used as the basis for

formulating the initial statements, which were then evaluated through the Delphi survey method.

Delphi Survey Method Process and Administration A modi fi ed Delphi survey method was utilized to assess consensus for the proposed statements, 13 with multiple anonymous surveys completed to minimize bias within the development group and facilitate consensus. Web ‐ based software (www.surveymonkey.com) was used to administer con fi dential surveys to development group members. A potential topic list of 60 questions and draft statements was put together by the development group during the fi rst call and each development group member was invited to provide 1 draft statement for each of their top 5 ranked topic list choices. The survey period was divided into 2 Delphi rounds. All answers were deidenti fi ed and remained con fi dential to development group members; however, names were collected by staff to ensure proper follow ‐ up, if needed. Based on the outcomes of the top ‐ ranked topic list choices and resulting discussion, the development group chair and assistant chair developed the fi rst Delphi survey, which consisted of 60 statements. Prior to dissemination to the development group, the Delphi surveys were reviewed by the methodologist for content and clarity. Questions in the survey were answered using a 9 ‐ point Likert scale, where 1 = strongly disagree, 3 = dis agree, 5 = neutral, 7 = agree, and 9 = strongly agree. The surveys were distributed, and responses were aggregated, distributed back to the development group, discussed via teleconference, and revised if warranted. The purpose of the teleconference was to provide an opportunity to clarify any ambiguity, propose revisions, or drop any statements recommended by the development group. Criteria for consensus were established a priori as follows 1 : • Consensus : Statements achieving a mean score of 7.00 or higher and having no more than 1 outlier, de fi ned as any rating of 2 or more Likert points from the mean in either direction. • Near consensus : Statements achieving a mean score of 6.50 or higher and having no more than 2 outliers. • No consensus : Statements that did not meet the criteria of consensus or near consensus. Two iterations of the Delphi survey were performed. All group members completed all survey items in the fi rst Delphi survey; in the second iteration, there were 2 items that were only completed by 10 of the 12 voting members of the panel. The development group reviewed the results of all 60 items via teleconference after the fi rst Delphi survey. Twenty ‐ four statements were revised for improved clarity. Eight items did not reach consensus and were not discussed further. There were 10 statements that reached near consensus and were discussed thoroughly. Four of