AbstractBackground and ObjectivesInjection laryngoplasty (IL) is a common surgical treatment for unilateral vocal fold paralysis (UVFP). Although UVFP affects voice and airway protection, and the effects of IL on voice are well documented, its impact on swallowing function remains unclear. This study aimed to better understand the effect of IL on swallowing function in UVFP.
Materials and MethodA retrospective chart review was conducted among 14 patients with UVFP who underwent swallowing evaluation before and after IL. Swallowing function was evaluated by comparing penetration–aspiration scale (PAS) scores and swallowing timing measures in video fluoroscopic swallowing studies (VFSS) pre- and post-injection. Swallowing function was assessed using different consistencies, including small and large liquid barium, yogurt, soft blend diet (SBD), and a normal regular diet.
ResultsAlthough PAS scores showed numerical improvements in the small liquid, yogurt, and SBD groups after injection, only the change in yogurt was statistically significant (Z=-2.375, p=0.018). The timing measures did not differ significantly after IL. Dietary levels improved in 11 of 14 patients (78.6%), whereas 3 patients (21.4%) showed no change, all of whom had comorbidities such as lung cancer, esophageal stricture, or esophageal cancer.
ConclusionDespite the absence of measurable changes in VFSS timing parameters, clinical outcomes, including dietary advancement, should be considered alongside instrumental findings while evaluating the swallowing treatment effects of IL in patients with UVFP. Future studies incorporating structured rehabilitation and larger sample sizes are required to clarify the therapeutic scope of IL for dysphagia management.
INTRODUCTIONUnilateral vocal fold paralysis (UVFP) is the most common neurological disorder of the larynx [1]. The main cause of UVFP is iatrogenic injury during dissection or retraction along the course of the recurrent laryngeal or vagus nerves. However, traumatic causes, including thoracic surgeries and tumor invasion, can also result in UVFP [1-3]. Treatment options range from watchful observation to surgical medialization procedures aimed at closing the glottic gap [4]. Injection laryngoplasty (IL) is a preferred technique that modifies glottic incompetence of paralyzed vocal fold (VF) by injecting bulking agents such as hyaluronic acid or calcium hydroxyapatite [5,6]. IL reduces the anterior and/or mid-glottal gap and improves phonation and airway protection, requiring near or complete glottal closure [1,7,8]. Compared to medialization thyroplasty for permanent manipulation, IL is temporary, cost-effective, non-invasive, and technically simple [9-11].
UVFP can affect voice, airway protection, and quality of life [3,12]. To date, most studies have focused on voice, and the vocal characteristics associated with UVFP have been well established. Patients with UVFP commonly present with a breathy voice, reduced pitch range and loudness, shortened phonation duration, and diplophonia [13-16]. These symptoms significantly reduce the voice-related quality of life [13,15-17].
Although approximately 60% of patients with UVFP reported dysphagia [18], the effect of IL on swallowing function in UVFP remains unclear [2,11]. Grant et al. [19] retrospectively evaluated swallowing outcomes after IL in 15 patients with UVFP using self-reported symptoms, advancement to oral intake, and a video fluoroscopic swallowing study (VFSS). More than 80% of the participants showed improved self-reported swallowing function and dietary advancement. Zuniga et al. [20] retrospectively analyzed 21 patients with UVFP who underwent IL. Swallowing outcomes were measured using the fiberoptic endoscopic evaluation of swallowing, eating assessment tool-10 (EAT-10), and functional oral intake scale (FOIS). Significant improvements were observed in both EAT-10 and FOIS scores after IL, along with an increase in dietary intake. In contrast, Kammer et al. [21] evaluated the swallowing function in 17 patients with UVFP using the penetration–aspiration scale (PAS) and pharyngeal high-resolution manometry following IL. No significant improvement was observed in PAS scores and normalized glottal area. Moreover, the maximum pressure and rate of mesopharyngeal pressure rise increased, indicating that the patients exerted more effort during bolus swallowing. Kang et al. [22] also investigated the swallowing function after IL in 15 patients with UVFP. Swallowing function was assessed via VFSS using the videofluoroscopic dysphagia scale, PAS, American Speech-Language-Hearing Association National Outcome Measurement System Swallowing Scale, and the Anderson dysphagia inventory. No significant improvements in the swallowing outcomes were observed.
Similarly, the heterogeneity of swallowing outcome measures and findings has made it difficult to clearly determine the effects of IL on swallowing in UVFP. Swallowing timing measures in VFSS can capture the physiological components of individual swallowing [23,24], such as pharyngeal and/or contralateral compensatory mechanisms that may occur prior to injection to prevent swallowing dysfunction caused by UVFP. However, to our knowledge, timing measures have not been previously used to compare swallowing function before and after IL in patients with UVFP. Thus, this study aimed to better characterize the effects of IL on swallowing function in UVFP by analyzing VFSS-based swallowing timing measures, in addition to the PAS score.
MATERIALS AND METHODParticipantsThis study was approved by the Institutional Review Board of the National Cancer Center (NCC2025-0196). In light of the retrospective design of the study, the requirement for individual informed consent was waived. This retrospective chart review included patients with UVFP who underwent swallowing evaluation before and after IL between September 2013 and May 2023. Patients were included only if they had swallowing outcome data for at least one identical food consistency pre- and post-injection and had not received any voice or dysphagia treatment between the pre- and post-evaluations. Once eligible participants were identified, demographic data were collected, including age, sex, etiology of UVFP, and side of paralysis. As hyaluronic acid (Restylane Perlane [Galderma, Lausanne, Switzerland]) was the standardized injection material used at the institute, the amount of material injected was also recorded.
Swallowing evaluationSwallowing evaluations were performed at both pre- and post-injection appointments. All evaluations were conducted by a single occupational therapist with >10 years of experience. A VFSS was performed with the patient seated in a lateral projection. Baritop HD® barium contrast agents (liquid barium sulfate for suspension, 200% w/v after reconstitution) were used as the contrast agent for all consistencies. The patients were administered 2 cc of small liquid barium, 5 cc of large liquid barium, 3 cc of yogurt (Fresh Cream Yogurt Original, Dongwon F&B) mixed with barium, 3 cc of a soft blend diet (SBD: chopped Korean rice and side dishes) mixed with barium, and 3 cc of normal regular diet (NRD: Korean rice mixed with side dishes) mixed with barium. All VFSS procedures were recorded at eight frames per second.
Swallowing outcome measuresThe highest (worst) PAS score (Table 1) [25] observed in the VFSS for the same food consistency before and after injection was recorded. Six VFSS-based swallowing timing measures, adapted from the work of Anderson et al. [23] and Molfenter and Steele [24], were also analyzed: 1) stage transition duration (STD): the time between the first superior and/or anterior burst of motion of the hyoid (hyoid burst) and the head of the bolus passing the ramus of the mandible (bolus head into the pharynx); 2) duration of laryngeal vestibule closure (dLVC): the time between the first frame of LVC and the first frame of laryngeal vestibule opening; 3) duration to LVC: the time between hyoid burst and the first frame of LVC; 4) duration to upper esophageal sphincter opening (UESO): the time between hyoid burst and the first frame of UESO; 5) duration of UESO (dUESO): the time between the first frame of UESO and the first frame of UES closing; and, 6) pharyngeal transit time (PTT): the time between entering of the bolus head into the pharynx and the exit of the bolus tail from the pharynx. As the VFSS recordings began after bolus entry into the oral cavity, only timing measures related to the pharyngeal stage were analyzed.
Statistical analysisAll data were analyzed using SPSS Statistics version 25 (IBM Corp.). Descriptive statistics were used to summarize the participant demographics. The non-parametric Wilcoxon signed-rank test was used to compare swallowing measures before and after injection. Statistical significance was defined as p<0.05.
RESULTSPatient characteristicsFourteen patients with UVFP (13 male and 1 female) who underwent swallowing evaluations for at least one identical food consistency before and after IL were included. The mean age was 71.3±7.5 years (range 55–78). The etiology of UVFP was iatrogenic and neoplastic in 10 and 4 patients, respectively. Eight patients had left-sided paralysis, whereas six had right-sided paralysis. The injection volume ranged from 0.5 to 1.0 cc, depending on the degree of VF augmentation required. The mean duration from pre-swallowing evaluation to injection was 18.21±21.7 days (range 0–57), and that from injection to post-swallowing evaluations was 21.6±20.15 days (range 1–67) (Table 2).
Swallowing outcomes before and after ILThe number of patients according to food consistency was 14 for yogurt; three, small liquid; three, NRD; two, SBD; and one, large liquid (Table 3). Most consistencies and both pre- and post-injection showed normal or penetration (PAS≤5); however, one patient showed a PAS score of 8 with thick SBD pre-injection, and with yogurt pre-injection, three patients showed a PAS score of 7 and one patient showed a PAS score of 8 (Tables 1 and 3). A significant difference in PAS scores was observed for yogurt between pre- and post-injection (Z=-2.375, p=0.018), whereas no significant changes were found in other PAS scores or swallowing timing measures (Table 3 and Fig. 1).
Analysis of the mean values showed that STD decreased after injection in both the small liquid and SBD groups, whereas dLVC decreased after injection in the small liquid and yogurt groups, with no change observed in the NRD group. Post-injection, the duration to LVC was reduced in the SBD group, whereas the duration to UESO was shorter in the small liquid group. No change in LVC duration was observed for the small liquid group. The dUESO increased in the large liquid and SBD groups, whereas the PTT increased in the small liquid, yogurt, SBD, and NRD groups, although the dUESO remained unchanged in the NRD group. The PAS scores improved after the injection of small liquids, yogurt, and SBD, but only the change in yogurt reached statistical significance. In contrast, the PAS score worsened in the NRD group after injection, and no change was observed in the large liquid group.
Changes in dietary level after injection laryngoplastyAmong the 14 patients, 6 patients (42.9%) were on tube feeding, and none were able to tolerate NRD before IL. After injection, only 2 patients (14.3%) remained on tube feeding, whereas 6 patients (42.9%) progressed to NRD, and another six remained on SBD. Ultimately, the dietary levels advanced in 11 of 14 patients (78.6%). Three patients (21.4%) who showed no improvement had underlying conditions such as lung cancer with chemotherapy, esophageal stricture, and esophageal cancer.
DISCUSSIONThis study aimed to investigate the effect of IL on swallowing function in patients with UVFP using PAS scores and six swallowing timing measures obtained from the VFSS. In the swallowing evaluation protocol of the institution where this study was conducted, the assessment begins with yogurt. If any abnormality is observed, further testing is not performed, based on the assumption that normal swallowing would be unlikely with other consistencies. This led to differences in the number of participants assessed at each consistency. However, to identify additional characteristics of swallowing function, such as dietary advancement, analyses were performed on small and large fluids, yogurt, SBD, and NRD. Among the various swallowing outcomes, a statistically significant improvement was observed only in the PAS score with yogurt. Clinically, however, many patients showed functional gains as evidenced by advancements in dietary intake, including progression to NRD. These findings suggest that IL may contribute to improvements in swallowing function that are not always reflected in instrumental metrics.
Previous studies have yielded inconsistent results regarding the effects of IL on swallowing function. Grant et al. [19] observed an improvement in self-reported swallowing ability and advancement in oral intake, in addition to reduced PAS scores in the VFSS, after injection. Zuniga et al. [20] also reported improvements in the EAT-10 and FOIS scores post-injection, but not in objective VFSS metrics. In contrast, Kang et al. [22] found no statistically significant differences in the dysphagia scale and swallowing function using VFSS. Kammer et al. [21] used high-resolution manometry and observed increased mesopharyngeal pressure after IL, suggesting that greater effort is required during post-injection swallowing, rather than indicating improved efficiency. These findings indicate that although improved glottic competence is expected to enhance intrabolus pressure generation, other biomechanical factors, such as pharyngeal strength and UESO, may also influence the safety and efficiency of swallowing.
To better identify the effects of IL on swallowing outcomes, we extended previous studies by incorporating swallowing timing measures in addition to the PAS score to capture the underlying physiological changes in the present study. We hypothesized that patients with UVFP may have compensatory pharyngeal or laryngeal mechanisms to overcome glottic insufficiency. Such adaptations could be reflected in changes in STD, timing of LVC, or PTT. However, none of the timing parameters showed statistically significant differences for all consistencies before and after IL. This may suggest that compensatory mechanisms in pharyngeal or laryngeal function, if present, did not manifest as measurable temporal changes, or that such changes could not be revealed due to the limited sample size or resolution constraints of VFSS.
As demonstrated by the advancement of dietary levels in this study, the therapeutic benefit of IL appears to be most effective in cases where swallowing impairment is primarily due to glottal insufficiency without comorbid impairments. The lack of changes in timing measures in this study may reflect constraints in physiological recovery in patients with UVFP, particularly in those with coexisting pharyngeal weakness or sensory deficits [1,11,20]. Even when glottal closure improves, inadequate pharyngeal strength may lead to residues in the vallecula or pyriform sinuses, increasing the risk of post-swallow aspiration [26]. This may be particularly relevant in thicker consistencies, where increased viscosity contributes not only to pressure but also to residue. In our study, the PAS score for NRD worsened after injection, which may reflect these dynamics. In addition, the effects of IL may be limited if sensory deficits are present. Swallowing is a complex sensory-motor process, and intact sensory input is essential for initiating and regulating safe and effective swallowing [27]. Generally, in patients with UVFP, except for isolated recurrent laryngeal nerve injury, sensory impairment is frequently observed and may contribute to persistent dysphagia [28-30]. Although IL improved glottal closure, it did not restore sensory function, which may limit the therapeutic effect in the patients in this study. Paradoxically, this dietary advancement may suggest that the improvement in swallowing function, which was not reflected in PAS or timing measures, is attributable to the IL.
Finally, even in the absence of statistically significant changes in swallowing timing measures and PAS scores, it cannot be conclusively stated that IL had no effect on compensatory adaptations in swallowing physiology. This study did not examine the effects of swallowing rehabilitation after IL, and it remains uncertain whether compensatory mechanisms could have been enhanced through post-injection rehabilitation therapy.
Despite the insights gained from the comparison of swallowing outcomes after IL, some limitations remain. Given that the VFSS was recorded at 8 fps in this study, it may not have been sufficient to detect subtle physiological changes. Moreover, the variability in the time intervals between the pre- and post-injection evaluations, as well as the small number of patients available for each food consistency, limit the generalizability of the findings.
CONCLUSIONOur study demonstrated a statistically significant improvement only in PAS scores for yogurt and a clinically meaningful advancement in dietary intake, whereas no significant changes were observed in VFSS-based timing measures. These findings suggest that the therapeutic effects of IL may not be fully represented by instrumental metrics alone, and that functional outcomes, including dietary level advancement, should be assessed alongside objective parameters. IL may improve functional swallowing outcomes in patients with UVFP, particularly in cases where glottic insufficiency is the primary cause of dysphagia. Further studies incorporating post-injection rehabilitation and more sensitive assessment tools are warranted to better elucidate the role of IL in the management of dysphagia associated with VF paralysis.
NOTESAuthors’ Contribution Conceptualization: Ja Young Kim, Chang Hwan Ryu. Data curation: Ja Young Kim, Youn Mi Ryu. Formal analysis: Ja Young Kim, Chang Hwan Ryu. Methodology: Ja Young Kim. Project administration: Ja Young Kim, Chang Hwan Ryu. Visualization: Ja Young Kim, Chang Hwan Ryu. Writing—original draft: Ja Young Kim. Writing—review & editing: all authors. Approval of final manuscript: all authors. Fig. 1.PAS scores and six swallowing timing measures in different consistencies with a standard error bar. There was a significant difference in the PAS score of yogurt between pre- and post-injection (p=0.018), but not in the PAS scores and swallowing timing measures of other consistencies. A: Small liquid. B: Large liquid. C: Yogurt. D: Soft blend diet. E: Normal regular diet. *p<0.05. PAS, penetration-aspiration scale; LVC, laryngeal vestibule closure; dLVC, duration of LVC; UESO, upper esophageal sphincter opening; dUESO, duration of UESO; PTT, pharyngeal transit time. Table 1.Penetration–aspiration scale score description Table 2.Patient characteristics (n=14) Table 3.Penetration–aspiration scale scores and the difference between pre- and post-injection
REFERENCES2. Dhar SI, Ryan MA, Davis AC, Jedlanek E, Pietsch K, Price C, et al. Does medialization improve swallowing function in patients with unilateral vocal fold paralysis? A systematic review. Dysphagia 2022;37(6):1769-76.
3. Misono S, Merati AL. Evidence-based practice: evaluation and management of unilateral vocal fold paralysis. Otolaryngol Clin North Am 2012;45(5):1083-108.
4. Korean Society of Laryngology, Phoniatrics and Logopedics Guideline Task Force, Ryu CH, Kwon TK, Kim H, Kim HS, Park IS, Woo JH, et al. Guidelines for the management of unilateral vocal fold paralysis from the Korean Society of Laryngology, Phoniatrics and Logopedics. Clin Exp Otorhinolaryngol 2020;13(4):340-60.
5. Hertegård S, Hallén L, Laurent C, Lindström E, Olofsson K, Testad P, et al. Cross-linked hyaluronan used as augmentation substance for treatment of glottal insufficiency: safety aspects and vocal fold function. Laryngoscope 2002;112(12):2211-9.
6. Hertegård S, Hallén L, Laurent C, Lindström E, Olofsson K, Testad P, et al. Cross-linked hyaluronan versus collagen for injection treatment of glottal insufficiency: 2-year follow-up. Acta Otolaryngol 2004;124(10):1208-14.
7. Barbu AM, Gniady JP, Vivero RJ, Friedman AD, Burns JA. Bedside injection medialization laryngoplasty in immediate postoperative patients. Otolaryngol Head Neck Surg 2015;153(6):1007-12.
8. Périé S, Laccourreye O, Bou-Malhab F, Brasnu D. Aspiration in unilateral recurrent laryngeal nerve paralysis after surgery. Am J Otolaryngol 1998;19(1):18-23.
9. Buchanan MA, Riffat F, Palme CE. Endoscopic vocal fold injection using a 25-gauge butterfly needle. J Laryngol Otol 2016;130(4):398-400.
10. Iwanaga Y, Maeyama T, Umezaki T, Shin T. Intracordal injection increases glottic closing force in recurrent laryngeal nerve paralysis. Otolaryngol Head Neck Surg 1992;107(3):451-6.
11. Pan S, Sadoughi B. Effectiveness of injection laryngoplasty for aspiration in acute iatrogenic vocal fold paralysis: a systematic review. Laryngoscope 2022;132(4):813-21.
12. Daniero JJ, Garrett CG, Francis DO. Framework surgery for treatment of unilateral vocal fold paralysis. Curr Otorhinolaryngol Rep 2014;2(2):119-30.
13. 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(7):1759-62.
14. Elsaeed A, Afsah O, Moneir W, Elhadidy T, Abou-Elsaad T. Respiratory and voice outcomes of office-based injection laryngoplasty in patients with unilateral vocal fold paralysis. Egypt J Otolaryngol 2021;37:1
15. Fang TJ, Li HY, Gliklich RE, Chen YH, Wang PC, Chuang HF. Outcomes of fat injection laryngoplasty in unilateral vocal cord paralysis. Arch Otolaryngol Head Neck Surg 2010;136(5):457-62.
16. Wang CC, Wu SH, Tu YK, Lin WJ, Liu SA. Hyaluronic acid injection laryngoplasty for unilateral vocal fold paralysis—a systematic review and meta-analysis. Cells 2020;9(11):2417
17. Hogikyan ND, Wodchis WP, Terrell JE, Bradford CR, Esclamado RM. Voice-related quality of life (V-RQOL) following type I thyroplasty for unilateral vocal fold paralysis. J Voice 2000;14(3):378-86.
18. Brunner E, Friedrich G, Kiesler K, Chibidziura-Priesching J, Gugatschka M. Subjective breathing impairment in unilateral vocal fold paralysis. Folia Phoniatr Logop 2011;63(3):142-6.
19. Grant JR, Hartemink DA, Patel N, Merati AL. Acute and subacute awake injection laryngoplasty for thoracic surgery patients. J Voice 2008;22(2):245-50.
20. Zuniga S, Ebersole B, Jamal N. Improved swallow outcomes after injection laryngoplasty in unilateral vocal fold immobility. Ear Nose Throat J 2018;97(8):250-6.
21. Kammer RE, Jones CA, Johnson AM, Dailey SH, McCulloch TM, Thibeault SL. High-resolution manometry and swallow outcomes after vocal fold injection medialization for unilateral vocal fold paralysis/paresis. Head Neck 2019;41(7):2389-97.
22. Kang MG, Seo HG, Chung EJ, Lee HH, Yun SJ, Keam B, et al. Effects of percutaneous injection laryngoplasty on voice and swallowing problems in cancer-related unilateral vocal cord paralysis. Laryngoscope Investig Otolaryngol 2021;6(4):800-6.
23. Anderson C, Macrae P, Taylor-Kamara I, Serel S, Vose A, Humbert IA. The perturbation paradigm modulates error-based learning in a highly automated task: outcomes in swallowing kinematics. J Appl Physiol (1985) 2015;119(4):334-41.
24. Molfenter SM, Steele CM. Temporal variability in the deglutition literature. Dysphagia 2012;27(2):162-77.
25. Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia 1996;11(2):93-8.
26. Bhattacharyya N, Kotz T, Shapiro J. The effect of bolus consistency on dysphagia in unilateral vocal cord paralysis. Otolaryngol Head Neck Surg 2003;129(6):632-6.
27. Troche MS, Brandimore AE, Godoy J, Hegland KW. A framework for understanding shared substrates of airway protection. J Appl Oral Sci 2014;22(4):251-60.
28. Erdur O, Gul O, Ozturk K. Evaluation of upper oesophageal sphincter in unilateral vocal fold paralysis. J Laryngol Otol 2019;133(2):149-54.
|
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||