Abstract
The association of voice disorders in laryngeal cancers has been studied extensively; however Dysphonia associated with chemo-radiation in non laryngeal Head and Neck cancer (HNC) is a new area of practice in voice clinics. This study thus aimed to evaluate the efficacy of voice rehabilitation among non-laryngeal HNC survivors who were treated with curative RadioTherapy (RT)/Chemoradiotherapy (CRT) in adjunct with or without surgery. This tertiary institutional assessor blinded quasi experimental study after inclusion and exclusion criteria consisted of a study cohort of 128 patients who within 1–3 months of completion of treatment for HNC reported to the laryngology clinic for voice complaints and throat discomfort. All patients underwent documentation of laryngeal endoscopic imaging, acoustics assessment, Aronson’s Laryngeal Palpatory Method (LPM) and Voice Handicap Index (VHI). Thereafter they were subjected to Vocal Rehabilitation Therapy (VRT) which constituted of Manual circumlaryngeal therapy, SOVTE, and vocal hygiene program. Re-evaluation of the vocal parameters was done at 6 weeks and 3 months from the start of the VRT. All parameters were significantly altered at 6 weeks and 3 months follow-up. Post VRT the videolaryngoscopic findings showed reduction in abnormal supraglottic MTPs with subsequent good approximation of true cords and reduction of involvement of supralaryngeal activities. The Dysphonia Severity Index (DSI) impairment levels and VHI scores showed significant improvement from the baseline to both at 6 weeks and 3 months of VRT (p < 0.001). DSI and VHI scores even showed significant improvement between 6 weeks to 3 months of therapy. There was highly significant correlation of VRT with/without surgery, with CRT and in non-smokers at 6 weeks and 3 months of VRT. In non-laryngeal head and neck malignancies, VRT offered as early as within 1–3 months of completion of treatment of HNC ameliorates surgical and chemo-radiation induced Muscle Tension Dysphonia.
Keywords: Chemo radiation, Non-laryngeal head and neck cancer, VHI, DSI, Rehabilitation, SOVTE, Muscle tension dysphonia, VRT
Introduction
A voice disorder is characterized by the abnormal production and/or absence of vocal pitch, loudness, and quality, which are inappropriate for an individual's age, gender, cultural background, or geographic location [1]. The production of healthy voice requires effective use of many muscles as well as other tissues along with aerodynamic forces. When ineffective patterns result in overuse of laryngeal muscles, these behaviors could lead to Muscle Tension Dysphonia (MTD). Voice disorders like MTD can happen at any stage in the lifespan. In 2012, approximately 1.7% of the population was diagnosed with MTD and the prevalence of this disorder has grown since then [2]. When a person has a voice problem or voice disorders, voice therapy can help that person improve [3]. So to learn how to create phonation in a healthy manner especially for the person with a voice disorder, voice therapy is recommended with good outcomes. Voice therapy is among the services provided by a Speech-Language Pathologist (SLP) and has been used effectively for treating voice problems including MTD [2].
Radiotherapy (RT) alone or in combination with chemotherapy (CRT) is commonly used in the treatment of head and neck cancer (HNC). Approximately, 80% of patients undergoing radiotherapy develop mucositis leading to major impact on the QoL [4, 5]. Voice variability after RT/CRT is a very frequent complaint. Impact on voice post CRT has been reported, if the larynx is included in the treatment field. RT to the larynx has been found to result in muscle atrophy, fibrosis, dryness of the laryngeal mucosa, hyperemia, and erythema [6, 7]. Voice changes following radiotherapy may include difficulty in speech articulation, reduced vocal loudness, low modal speaking pitch, reduced phonic breath support, vocal roughness, breathiness hoarseness, and vocal fatigue [8–10]. Though there are many studies in literature of acoustic voice analysis in post RT/CRT of laryngopharyngeal cancer but, till date, in review of literature there is limited experience to assess the impact of RT/CRT on the voice especially in non-laryngeal cancers and its effective active management [11–13]. Therefore, the aim of this study was to investigate the patient-reported voice impairment and throat discomfort among non laryngeal HNC survivors who were treated with curative RT/CRT with or without surgery and document the efficacy of rehabilitation of MTD among these patients. The results from this study would help the development of targeted voice and speech-preserving interventions in patients, and in future research to optimize communication function among survivors and improve their quality of life (QoL).
Methodology
Patients
This study was approved by the ethical committee of the institute and all participants gave written consent. It included a cohort of 140 patients presenting to the laryngology clinic in the department of Otorhinolaryngology of a tertiary Institute of North India.
Inclusion Criteria
The study cohort was assembled from patients who within 1–3 months of completion of treatment for HNC reported to the laryngology clinic for voice impairment and discomfort during the study period 2010–2021. The complete treatment modality comprised either single modality treatment, i.e. either RT or chemotherapy, or multimodality treatment, included patients who received combination treatment with CRT or those who received surgery followed by adjuvant RT or CRT as per institutional protocols.
Exclusion Criteria
Patients with cancer involving the larynx or hypopharynx, non-resectable disease, recurrence, distant metastasis, diseases of central nervous system/thorax or death due to co-morbidity (cardiac, pulmonary, systemic, renal),previous history of laryngeal surgery or thyroid surgery, laryngo-tracheal trauma, predominant laryngeal mucosal lesions(cysts, polyps, nodules), puberphonia, transgender voice, neurological voice problems, episode of acute or chronic upper respiratory tract infection during the assessment and those with inadequate follow-up data were excluded from the study.
Study Design
Assessor blinded quasi experimental study.
Procedure
The study was conducted to document the outcome of voice therapy in patients presenting symptoms of voice disorders post RCT/RT. The patients who complained of vocal discomfort or voice changes went through the following assessment and treatment protocol:
Assessment Protocol
The assessment included a thorough case history. We followed the American Speech Language Hearing Association (ASHA) protocol for Instrumental Assessment of Vocal Function (IVAP). The assessment included laryngeal endoscopic imaging, acoustics assessment, Aronson’s LPM [14] and VHI (Voice Handicap Index).
-
(i)
Laryngeal imaging: all the patients were assessed using Laryngeal Videoendoscopy (LVE) and Laryngeal Videostroboscopic (LVS) examination (Kay Pentax 9400). The LVE examination was done by 90º Storz rigid endoscope with HD camera using a constant light to assess the nonvibratory function of the larynx. This gross level visual perceptual assessment included inspection of the vocal fold medial edges, vocal fold mobility, supraglottic activity during phonation, and laryngeal maneuvers during transitional behaviors [15], and this evaluation was done at minimum 3 complete breath cycles of rest breathing and producing i/i/i/i/i/i without breaths in between. LVS was done with Pentax fibreoptic nasolaryngoscope. Stroboscopic visual–perceptual assessment was done to rule out mucosal changes of the glottis and such cases were excluded from this study.
-
(ii)
Acoustic assessment: these are the quantitative noninvasive measures for vocal function. We used the ASHA protocol for IVAP [16]. Dr. SPEECH software version 6.0 was used to analyze and display features of sustained vowel a wide range of parameters (jitter, shimmer, etc.) was used to guide diagnostic assessment for voice disorder and DSI was calculated. DSI is a recognized assessment tool based on a weighted combination of maximum phonation time, highest frequency, lowest intensity, and jitter (%) of an individual [17] (Table 1). Though DSI is not a gold standard tool to assess MTD but it was used in this study with an objective to quantify and document the efficacy of VRT and to avoid the possibility of subjective variations.
-
(iii)
Patient self report scale: the VHI was used in this study which aimed to measure self-perception of voice problems, through evaluating the emotional, functional, and physical aspects of the problem. It was used to assess the impact of voice in terms of physical complaint and restriction in participation of the daily activities [17] (Table 2). The voice samples of each patient were analyzed by speech and language pathologist (SLP) with 12 years experience in this field.
Table 1.
Dysphonia severity index (DSI) impairment level
| Impairment group level | DSI range | Description of impairment level |
|---|---|---|
| 0 | ≤ 2.0 | Severe persistent aphonia: patient has no voice,unable to phonate |
| 1 | − 1.9 to + 0.3 | Constant dysphonia: sporadic periods of phonation, aphonic periods may be present |
| 2 | + 0.4 to + 2.2 | Moderate dysphonia: patient can produce voice but there are frequent periods of dysphonia |
| 3 | + 2.3 to + 3.3 | Slight to moderate dysphonia: less frequent periods of disturbed phonation or slight persisting dysphonia |
| 4 | + 3.4 to + 4.3 | Slight dysphonia: sporadic dysponic moments for short periods |
| 5 | > 4.4 | No dysphonia |
Table 2.
Voice handicap Index (VHI) grading
| Score range | Severity |
|---|---|
| 0–30 | Mild |
| 31–60 | Moderate |
| 60–120 | Severe |
All patients who within 1–3 months of completion of treatment for HNC reported to the laryngology clinic for voice impairment and throat discomfort during the study period 2010–2021 were included in the study cohort. The Cohort consisted of 140 patients out of whom 8 patients were identified with vocal nodule and another 4 patients with vocal cyst during laryngeal stroboscopic examination and hence was excluded from the cohort, so we had a cohort of only 128 patients for statistical analysis.
Treatment Protocol
All 128 cases with diagnosed MTD were thereafter subjected to vocal rehabilitation therapy (VRT) which constituted of:
-
(i)
Manual circumlaryngeal therapy [18, 19]: the therapeutic procedure for MTD involved the following techniques considering the patient’s problems: (a) Palpation assessment of the larynx region to evaluate muscle tone at rest, range of motion, and facilitation and convenience of motion. (b) Reposturing maneuvers with the aim of removing muscle patterns and improper use of muscles. The first kneading involves compression of the larynx by applying anteroposterior pressure on superficial regions and below the hyoid bone (“hyoid pushback”). Another maneuver involves downward pressure on the upper angle of laryngeal cartilage (“pull-down”). (c) Rotational massage, which involves systematic kneading of the extralaryngeal region. It is believed that this type of massage causes stretching of muscles and fascia, resulting in increased local blood circulation, removal of waste due to metabolism, diminished muscle tension, and reduced pain and discomfort because muscle cramps [19]. Thereafter Manual tension reduction techniques were commenced [19]. The hyoid bone was surrounded by thumbs and index fingers, and we proceeded back up towards the posterior horn of the hyoid bone. Pressure was applied using circular movements on the horn of the hyoid bone. Pressure was also applied for the thyrohyoid space, starting from the thyroid notch and moving backwards. The same procedure was applied for the posterior margins of thyroid cartilage, which are located in the middle of sternocleidomastoid muscles.
The larynx was pulled down by the fingers on the upper edge of thyroid notch; at the same time, it was moved towards the surrounding parts. Special attention was paid to sites with superficial sensitivity, nodularity, or stiffness; slow or continual massage could also involve these regions. Massage was initiated superficially, and then, its depth increased with respect to areas surrounding the region with severe sensitivity or pain; then, the region of interest was approached [19]. In the event of severe tension, the practitioner applied techniques for the middle or lateral regions of suprahyoid muscles. The immediate effects of massage were noticeable on the skin; friction and rotational movements caused increased blood circulation, redness, and skin warmth.
-
(i)
Semi-occluded vocal tract exercises (SOVTE) [20, 21]: we used them to improve the source and filter interaction by changing the acoustic characteristics and the impedance of the vocal tract and there is a use of lip trills, tongue trills, bilabial fricatives, humming, and phonation into tubes or straws which has been hailed by clinicians, singing teachers, and voice coaches as efficacious for training and rehabilitation [20–23].
-
(ii)
Vocal hygiene program: It was developed emphasizing adequate hydration, healthy vocal diet, posture and alignment, vocal practices. All patients received instructions on vocal education and vocal hygiene including the anatomic and physiologic mechanisms of phonation.
Dosage and Duration of Voice Therapy
Each patient was subjected to intensive guided VRT of 30 min duration followed by home training program of 5 times a day × 10 repetitions per day. Post VRT evaluation (included videolaryngoscopy, DSI, Aronsons LPM and VHI) was done at 6 weeks and 3 months of the start of the VRT. For reliability and robustness the expert assessor was blinded during voice recordings, LVE, LVS, acoustic assessment and Aronson’s LPM findings (at 6 weeks and 3 months) and did not know about the modality of treatment that the HNC patient received and whether the patient received VRT or not. All patients were monitored and evaluated by the same clinician and SPL to avoid subjective variation throughout the study period.
Statistical Analysis
We had a cohort 128 patients for statistical analysis. Data was represented as Number, Percentage. Association among different categorical variables was done using Fisher Exact Test. Paired t test was used for before and after rehabilitation therapy. All analysis was performed using SPSS 23.0 version. A p-value less than 0.05 were considered significant, and a p-value less than 0.01 were considered highly significant.
Results
Demographic and Clinic-Pathological Variable Analysis
This assessor blinded quasi experimental study consists of a study cohort of 128 cases that met the inclusion criteria. In our study we found that 89.8% were males while 11.2% were females with age ranging from 31 to 74 years. Out of all the participants 48% were in TNM stage 3 while 52% were in TNM stage 4. The major primary sites included buccal mucosa (26%), buccogingival sulcus (2%), mandible (26%), maxilla (6%), palate (4%) and tongue (36%). As per histological grade, 23.4% tumours were well differentiated squamous cell carcinoma (SCC), 68.75 were moderately differentiated SCC while 7.8% were poorly differentiated SCC. 51.56% showed vascular invasion, 56.25% showed perineural invasion while 59.4% showed muscle invasion on histopathology. Demographic and clinic-pathological variables of the cohort are summarized in Table 3.
Table 3.
Demographic and clinicopathological characteristics
| Characterictics | No. of cases |
|---|---|
| Sex | |
| Males | 113 |
| Females | 15 |
| Site of lesion | |
| Buccal mucosa | 42 |
| Gingivobuccal sulcus | 21 |
| Palate | 8 |
| Tongue | 18 |
| Mandible | 24 |
| Maxilla | 15 |
| Grade | |
| Well differentiated | 30 |
| Moderately differentiated | 88 |
| Poorly differentiated | 10 |
| Vascular invasion present in | 66 |
| Perineural invasion present in | 72 |
| Muscle invasion present in | 76 |
| Smoking | |
| Former smoker | 5 |
| Non smoker | 123 |
| Treatment modality received | |
| Surgery | 109 |
| RT | 128 |
| Chemotherapy | 64 |
| DSI impairment level | |
| ≤ 2 | 82 |
| 3 or more | 46 |
| VHI severity | |
| Mild | 5 |
| Moderate | 53 |
| Severe | 70 |
The Pre and Post Therapy Outcomes of this Study Show the Following Results
Laryngeal Imaging Pre and Post VRT
The pre-VRT LVE findings of 128 patients revealed abnormal muscle tension patterns (MTPs) like excess supraglottic activity. The characteristics of videolaryngoscopic findings showed hyperactivity and compression of ventricular bands (80.5%), complete anterioposterior compression of larynx (3.1%), complete supraglottic closure (sphincteric larynx) and minimal vocal cord length visibility(17.18%), vertical movement of the larynx (27.34%), lateral hyperadduction (35.15), partial antero-posterior contraction of the supraglottis (1.5%), supraglottic anteroposterior compression of larynx (0.78%), only ventricular fold contribution (21.09%), associated ventricular fold contribution (31.25%). Post VRT the patients showed reduction in abnormal supraglottic MTPs with subsequent good approximation of true cords and reduction of involvement of supralaryngeal activities thus implying less phonation effort/ compensation after 6 weeks and 3 months of therapy. Out of 128 patients at the end of 3 months 42 patients still showed predominantly ventricular involvement.
Aronson’s Palpatory Method to Assess Tensioning of Laryngeal Muscles in Pre and Post VRT
The Pre VRT assessment of these patients using Aronson’s LPM method by the palpation of the larynx at rest and during voicing showed excessive tension during palpation over the major horns of the hyoid bone, over the superior cornu of the thyroid cartilage, along the anterior border of the sternocleidomastoid muscle and throughout the suprahyoid musculature. Post VRT showed that the tension of the supralaryngeal muscles was much reduced along with proper positioning of the larynx in these patients.
Objective Acoustic Outcome of VRT using DSI
The DSI impairment levels in patients showed significant improvement from the baseline to both at 6 weeks and 3 months of VRT (p < 0.001) and the DSI values even showed significant improvement between 6 weeks and 3 months of therapy (Table 4).
Table 4.
Effect of therapy on DSI category
| DSI category | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P value | Z value | P value | Z value | P value | |
| ≤ − 2.00 | 36 | 28.1 | 22 | 17.2 | 3 | 2.3 | 6.856 | < 0.001** | 9.400 | < 0.001** | 8.186 | < 0.001** |
| − 2.01 to 0.30 | 32 | 25.0 | 37 | 28.9 | 25 | 19.5 | ||||||
| 0.31–2.20 | 14 | 10.9 | 15 | 11.7 | 26 | 20.3 | ||||||
| 2.21–3.30 | 18 | 14.1 | 16 | 12.5 | 21 | 16.4 | ||||||
| 3.31–4.30 | 15 | 11.7 | 19 | 14.8 | 20 | 15.6 | ||||||
| > 4.30 | 13 | 10.2 | 19 | 14.8 | 33 | 25.8 | ||||||
Wilcoxon signed rank test: **p < 0.001; highly significant
Subjective Patient Outcome Report using VHI
After 6 weeks of VRT the VHI category which was severe in 53.9% patients was reduced to 46.1% patients and was further reduced to only 19.5% patients after 3 months of intensive VRT. The VHI scores were moderate in 42.2% patients which reduced to 37.5% patients after 6 weeks of VRT (p < 0.001) (Table 5 showing highly significant role of VRT in MTD.
Table 5.
Effect of therapy on VHI severity
| VHI Grp | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P value | Z value | P value | Z value | P value | |
| Mild | 5 | 3.9 | 21 | 16.4 | 51 | 39.8 | 6.856 | < 0.001** | 9.400 | < 0.001** | 8.186 | < 0.001** |
| Moderate | 54 | 42.2 | 48 | 37.5 | 52 | 40.6 | ||||||
| Severe | 69 | 53.9 | 59 | 46.1 | 25 | 19.5 | ||||||
Wilcoxon signed rank test: **p < 0.001; highly significant
Overall Comparison of Outcomes of VRT in Patients Who had Undergone CRT/RT in Adjunct with Surgery
The correlation of VRT in patients with/without surgery: total with surgery n = 109 and total without surgery n = 19 (Tables 6, 7). Out of 109 patients who underwent surgical intervention, maximum patients i.e. 22.9% were in DSI impairment level − 2.01 to 0.30 and which was reduced to 21.1% patients in the same category after rigorous VRT, while in the VHI scores 53.1% patients were in severe category before intervention of VRT, and this reduced to 20.1% after therapy, thus proving that VRT played a highly significant role in improving the scores in patients with surgery (p < 0.001 for both DSI & VHI)).
Table 6.
Correlation of therapy in patients without surgery (total patients without surgery = 19)
| Category | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P Value | Z value | P value | Z value | P value | |
| DSI ≤ − 2.00 | 4 | 21.0 | 2 | 10.5 | 0 | 0.0 | 2.828 | 0.005* | 3.827 | < 0.001* | 3.127 | 0.002** |
| − 2.01 to 0.30 | 7 | 36.8 | 5 | 26.3 | 2 | 10.5 | ||||||
| 0.31–2.20 | 2 | 10.5 | 5 | 26.3 | 7 | 36.8 | ||||||
| 2.21–3.30 | 2 | 10.5 | 2 | 10.5 | 4 | 21.0 | ||||||
| 3.31–4.30 | 2 | 10.5 | 3 | 15.8 | 2 | 10.5 | ||||||
| > 4.30 | 2 | 10.5 | 2 | 10.5 | 4 | 21.0 | ||||||
| VHI mild | 1 | 5.3 | 4 | 21.0 | 8 | 42.1 | 2.000 | 0.046 | 3.873 | < 0.001 | 3.317 | 0.001 |
| Moderate | 7 | 36.8 | 5 | 26.3 | 8 | 42.1 | ||||||
| Severe | 11 | 57.9 | 10 | 52.7 | 3 | 15.8 | ||||||
p < 0.01: significant
**p < 0.001; highly significant
Table 7.
Correlation of therapy in patients with surgery (total patients with surgery = 109)
| Category | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P Value | Z value | P value | Z value | P value | |
| DSI ≤ − 2.00 | 32 | 29.4 | 20 | 18.4 | 3 | 2.7 | 6.245 | < 0.001* | 8.861 | < 0.001* | 7.582 | < 0.001** |
| − 2.01 to 0.30 | 25 | 22.9 | 32 | 29.4 | 23 | 21.1 | ||||||
| 0.31–2.20 | 12 | 11.0 | 10 | 9.2 | 19 | 17.4 | ||||||
| 2.21–3.30 | 16 | 14.7 | 14 | 12.8 | 17 | 15.6 | ||||||
| 3.31–4.30 | 13 | 11.9 | 16 | 14.7 | 18 | 16.5 | ||||||
| > 4.30 | 11 | 10.1 | 17 | 15.6 | 29 | 26.6 | ||||||
| VHI mild | 4 | 3.7 | 17 | 15.6 | 43 | 39.5 | 4.690 | < 0.001 | 8.435 | < 0.001 | 7.147 | < 0.001 |
| Moderate | 47 | 43.2 | 43 | 39.5 | 44 | 40.4 | ||||||
| Severe | 58 | 53.1 | 49 | 45.9 | 22 | 20.1 | ||||||
p < 0.01: significant
**p < 0.001; highly significant
In patients without surgery, maximum number of patients i.e. 21% were in the DSI impairment level ≤ 2.00 and which was reduced to 10.5% and further reduced to 0% patients in the same category after rigorous rehabilitation therapy of 6 weeks and 3 months respectively, while in the VHI scores 57.9% patients were in severe category before intervention of rehabilitation therapy, and this reduced to 52.7 and 15.8% after 6 weeks and 3 months of therapy, thus proving that rehabilitation therapy played a highly significant role in improving the scores even in patients without surgery (p < 0.001 for both DSI & VHI)).
Overall Comparison of Outcomes of VRT in Patients with CRT and Only RT
Correlation of VRT in patients with/without CT (total patients with/without CT = 64 each) (Tables 8, 9). In patients without CT, maximum number of patients i.e. 43.8% were in the DSI impairment level ≤ 2.00 and which was reduced to 26.5% and further reduced to 3.1% patients in the same category after rigorous rehabilitation therapy of 6 weeks and 3 months respectively, while in the VHI scores 78.1% patients were in severe category before intervention of rehabilitation therapy, and this reduced to 65.7 and 32.8% after 6 weeks and 3 months of therapy, thus proving that rehabilitation therapy played a highly significant role in improving the scores in patients with CT (p < 0.001 for both DSI & VHI).
Table 8.
Correlation of therapy in patients without CT (total patients without CT = 64)
| Category | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P value | Z value | P value | Z value | P value | |
| DSI ≤ − 2.00 | 8 | 12.5 | 5 | 7.8 | 1 | 1.6 | 4.359 | < 0.001* | 6.565 | < 0.001* | 5.742 | 0.001** |
| − 2.01 to 0.30 | 12 | 18.7 | 14 | 21.8 | 5 | 7.7 | ||||||
| 0.31–2.20 | 9 | 14.1 | 5 | 7.7 | 9 | 14.1 | ||||||
| 2.21–3.30 | 13 | 20.3 | 12 | 18.7 | 8 | 12.5 | ||||||
| 3.31–4.30 | 12 | 18.7 | 14 | 21.8 | 16 | 25.0 | ||||||
| > 4.30 | 10 | 15.6 | 14 | 21.8 | 25 | 39.1 | ||||||
| VHI mild | 4 | 6.2 | 16 | 25.0 | 38 | 59.4 | 3.742 | < 0.001 | 6.861 | < 0.001 | 5.916 | < 0.001 |
| Moderate | 41 | 64.1 | 31 | 48.4 | 22 | 34.4 | ||||||
| Severe | 19 | 29.7 | 17 | 28.6 | 4 | 6.2 | ||||||
p < 0.01: significant
**p < 0.001; highly significant
Table 9.
Correlation of therapy in patients with CT (total patients with CT = 64)
| Category | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P value | Z value | P value | Z value | P value | |
| DSI ≤ − 2.00 | 28 | 43.8 | 17 | 26.5 | 2 | 3.1 | 5.292 | < 0.001* | 6.758 | < 0.001* | 5.857 | 0.001** |
| − 2.01 to 0.30 | 20 | 31.2 | 23 | 35.9 | 20 | 31.2 | ||||||
| 0.31–2.20 | 5 | 7.7 | 10 | 15.6 | 17 | 26.5 | ||||||
| 2.21–3.30 | 5 | 7.7 | 4 | 6.2 | 13 | 20.3 | ||||||
| 3.31–4.30 | 3 | 4.7 | 5 | 7.7 | 4 | 6.2 | ||||||
| > 4.30 | 3 | 4.7 | 5 | 7.7 | 8 | 12.5 | ||||||
| VHI mild | 1 | 1.6 | 5 | 7.7 | 13 | 20.3 | 3.464 | 0.001 | 6.252 | < 0.001 | 5.209 | < 0.001 |
| Moderate | 13 | 20.3 | 17 | 26.5 | 30 | 46.9 | ||||||
| Severe | 50 | 78.1 | 42 | 65.7 | 21 | 32.8 | ||||||
p < 0.01: significant
**p < 0.001; highly significant
In patients without CT, maximum number of patients i.e. 20.3% were in the DSI impairment level 2.21–3.30 and which was reduced to 18.7% and further reduced to 12.5% patients in the same category after rigorous rehabilitation therapy of 6 weeks and 3 months respectively, while in the VHI scores 64.1% patients were in moderate category before intervention of rehabilitation therapy, and this reduced to 48.4 and 34.4% after 6 weeks and 3 months of therapy, thus proving that rehabilitation therapy played a highly significant role in improving the scores even in patients without CT (p < 0.001 for both DSI & VHI).
Overall Comparison of Outcomes of VRT in Patients Who had a History of Smoking Before VRT
The Correlation of VRT with former smoker/nonsmoker patients: (total former smokers = 5 and nonsmokers n = 123) as shown in (Tables 10, 11) Out of 123 non-smokers, maximum patients i.e. 27.6% were in DSI impairment level ≤ 2.00 and which was reduced to 17.1% and further reduced to 2.4% in the same category after rigorous rehabilitation therapy, while in the VHI scores 52.8% patients were in severe category before intervention of rehabilitation therapy, and this reduced to 44.7% and further reduced to 18.8% in the same category after therapy, thus proving that rehabilitation therapy played a highly significant role in improving the scores in nonsmokers after complete treatment of cancer (p < 0.001 for both DSI & VHI).
Table 10.
Correlation of therapy with former smoker patients: (total former smokers = 5)
| Category | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P Value | Z value | P value | Z value | P value | |
| DSI ≤ − 2.00 | 2 | 40 | 1 | 20 | 0 | 00 | 1.000 | 0.317 | 1.890 | 0.059 | 1.633 | 0.102 |
| − 2.01 to 0.30 | 2 | 40 | 3 | 60 | 2 | 40 | ||||||
| 0.31–2.20 | 0 | 00 | 0 | 00 | 1 | 20 | ||||||
| 2.21–3.30 | 0 | 00 | 0 | 00 | 1 | 20 | ||||||
| 3.31–4.30 | 0 | 00 | 0 | 00 | 0 | 00 | ||||||
| > 4.30 | 1 | 20 | 1 | 20 | 1 | 20 | ||||||
| VHI mild | 0 | 00 | 1 | 20 | 1 | 20 | 1.000 | 0.317 | 1.732 | 0.083 | 1.414 | 0.157 |
| Moderate | 1 | 20 | 0 | 00 | 2 | 40 | ||||||
| Severe | 4 | 80 | 4 | 80 | 2 | 40 | ||||||
p < 0.01: significant
**p < 0.001; highly significant
Table 11.
Correlation of therapy in nonsmoker patients (total nonsmokers = 123)
| Category | Baseline | 6 weeks | 3 months | Baseline to 6 wks | Baseline to 3 mths | 6 wks to 3 mths | ||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| N | % | N | % | N | % | Z value | P Value | Z value | P value | Z value | P value | |
| DSI ≤ − 2.00 | 34 | 27.6 | 21 | 17.1 | 3 | 2.4 | 6.782 | < 0.001* | 9.221 | < 0.001* | 8.036 | 0.001** |
| − 2.01 to 0.30 | 30 | 24.4 | 34 | 27.6 | 23 | 18.7 | ||||||
| 0.31–2.20 | 14 | 11.4 | 15 | 12.2 | 25 | 20.3 | ||||||
| 2.21–3.30 | 18 | 14.6 | 16 | 13.0 | 20 | 16.3 | ||||||
| 3.31–4.30 | 15 | 12.2 | 19 | 15.4 | 20 | 16.3 | ||||||
| > 4.30 | 12 | 9.7 | 18 | 14.6 | 32 | 26.1 | ||||||
| VHI mild | 5 | 4.1 | 20 | 16.3 | 50 | 40.6 | 5.000 | < 0.001 | 9.118 | < 0.001 | 7.750 | 0.001 |
| Moderate | 53 | 43.1 | 48 | 39.0 | 50 | 40.6 | ||||||
| Severe | 65 | 52.8 | 55 | 44.7 | 23 | 18.8 | ||||||
p < 0.01: significant
**p < 0.001; highly significant
In former smokers, maximum number of patients i.e. 40% each were in the DSI impairment level ≤ 2.00 and − 2.01 to 0.3 respectively and which was reduced to 20% and further reduced to 0% patients in the category ≤ 2.00 while the smokers in the second category did not show any improvement even after rigorous rehabilitation therapy of 6 weeks and 3 months (p = 0.102 non-significant), while in the VHI scores 80% patients were in severe category before intervention of rehabilitation therapy, and this remained the same after 6 weeks of therapy but was reduced to 40% after 3 months of therapy (p = 0.157), thus proving that rehabilitation therapy did not play significant role in improving the scores in former smokers after complete treatment of cancer.
Discussion
Head and Neck Cancer is the most common malignancy in India among males and fifth most common among females [24]. Surgery, RT and CRT are three variable options in the management of head and cancers. Each modality impacts the laryngeal anatomy in vastly different manners [25–27]. Radiation not only causes deleterious effects on the larynx when laryngeal disease is treated with radiation, while the larynx can also suffer radiation damage because of its proximity to the radiation field when the neck is irradiated in non-laryngeal cancers. Radiation is known to induce a fibroblastic response which causes long-term deposition of collagen and fibrosis throughout the radiated field yielding a significant decrease in laryngeal pliability. Fibrosis leads to reduced tissue viscosity, leads to a permanent change in the voice quality [28]. The addition of chemotherapy to RT provides a synergistic effect as chemo-therapeutic agents act as an enhancer or potentiator of radiation. Though CRT has a beneficial effect on tumour tissue, it unfortunately has a highly toxic effect on normal tissues in the irradiated field as it enhances the cytotoxic effects of radiotherapy [29]. So it impacts voice quality, and patients often complain of increased vocal effort, breathiness and hoarseness and discomfort. Reduced voice quality affects daily activities of the patient. This can be associated with severe functional and psychosocial problems and reduced QoL [30, 31].
Nonpharmacologic treatment is the mainstay of rehabilitation for the radiated larynx and can be broken down into indirect voice therapy/vocal hygiene and direct voice therapy [28]. Vocal hygiene primarily aims on hydration. RT causes damage to laryngeal and salivary tissue, which results in laryngeal desiccation. As a result, vocal performance is affected [32, 33], this occurs as a sequelae response to radiation either at an early or late phase. Patients are taught to maintain adequate systemic hydration to maximize vocal function during and after radiation treatment. Local hydration using environmental humidification or steam inhalation is also beneficial [28]. Voice therapy focuses on helping the patient produce voice without using inefficient compensatory behaviors such as increased laryngeal strain and supraglottic constriction [30].
It is recommended that voice rehabilitation should be focused on relaxation and on decreased phonatory effort with more support from respiration. This is expected to improve the harmonic noise ratio and perturbation results, improving patient-rated voice quality outcomes [34]. Literature is full of studies that have evaluated vocal function in patients with laryngeal tumours treated with radiotherapy, but only a few have concentrated on the undiseased larynx receiving radiation to the neck as a part of the treatment protocol [35, 36]. The aim of this study was to evaluate the effect of rehabilitation therapy on nonlaryngeal head and neck patients who received surgery, RT and CRT as single or combined modality of treatment according to the institutional protocols. The finding showed highly significant treatment effects on both DSI, LPM and VHI scores after 6 weeks and 3 months of rehabilitation therapy. There was strong correlation of the rehabilitation therapy with/without surgery, with/without chemotherapy and in nonsmoker patients, however no correlation was found in former smoker patients after 6 weeks and 3 months of vigorous rehabilitation therapy. Lierde et al. in his case study of 4 subjects with moderate to severe MTD reported that manual laryngeal therapy showed improvements in voice quality and DSI [37]. Lucchini et al. in his study sample of 52 subjects diagnosed with voice disorders used proprioceptive elastic method, an indirect voice therapy treatment approach, reported statistical improvement of perceptual evaluation of dysphonia and improvement of the parameters of periodicity and mucosal wave found on laryngostroboscopy in his study subjects. So it can be considered an effective method of voice therapy to improve voice in patients with MTD [38]. Roy and Leeper used the manual laryngeal musculoskeletal tension reduction method in their study of 17 subjects with functional dysphonia reported a significant change towards the direction of normal vocal function in the majority of the subjects after just one therapy session. Acoustic measures of voice showed significant improvements in jitter, shimmer, and signal-to-noise ratio [18]. Speyer in his systemic review of 14 articles in which both direct and indirect therapy programs were used summarized that direct voice therapies seemed to be more effective than indirect voice therapies in dysphonic patients [39]. Watts et al. concluded that both Stretch-and-Flow Voice Therapy and Resonant Voice Therapy produced positive treatment response in speakers with Muscle Tension Dysphonia [40]. In a study by Fung et al., fundamental frequency and harmonic noise ratio significantly worsened (compared with age and gender matched controls) while jitter and shimmer showed no statistical significance at 1 year after RT of the non-diseased larynx [41]. The study results showed that in the absence of voice intervention, some of the acoustic parameters showed significant worsening compared to controls at one year post RT, while study by A. Sreenivas et al. of twenty individuals with non-laryngeal malignancies of the head and neck who received chemoradiation results showed that all parameters (acoustic analysis, perceptual and subjective analysis of voice) returned to pretreatment levels at 6 months of voice rehabilitation. So they concluded that VRT offered at 1 month after treatment ameliorates chemoradiation induced dysphonia within 6 months [42]. Our study too shows that the changes in perceptual, acoustic and patient reported voice quality measures brought about by surgery, RT/CRT can be significantly improved by VRT as early as 6 weeks to 3 months. Out of 128 patients at the end of 3 months, forty two patients still showed predominantly ventricular involvement which might be because of the difficulty to change the laryngeal behavior in these patients hence they were further enrolled for intensive voice therapy.
The strengths of this study include (1) detailed analysis of pre and post rehabilitation therapy LVS and LVE, acoustic, LPM and VHI evaluation of all patients. (2) Assessor blinded study to provide unbiased pre and post LVE and LVS, LPM acoustic assessment and VHI of the patients. (3) We used both objective- clinician determined (DSI) as well as subjective (VHI & LPM) assessments of voice and speech production which can be quantified as well as check the quality of voice as sometimes patient reported voice can be exaggerated as compared to the standard objective tests but sometimes patient reported functional outcomes provide more precise, patient specific information and physician rated voice dysfunction may underestimate the patient rated voice dysfunction. The limitations of the study were. (1) Home practice monitoring of the rehabilitation therapy could not be done because of staff constraints. (2) Availability of a single SLP could have lead to some bias in both the rehabilitation therapy and evaluation process. (3) In our data number of patients who did not undergo surgery was low, so our results may not be generalizable to non-surgically treated patients. (4) This study did not directly measure specific muscle tension parameters and this study lacked long term follow up which impacts on the sustainability and maintenance of this rehabilitation therapy. A longer follow-up is important since radiation induced fibrosis can cause late changes in voice. If a longer follow up reveals recurrent or late changes in voice, patients may require prolonged vocal rehabilitation.
Conclusion
The obtained results of the present study proved the fact that VRT causes significant positive changes in the DSI, LPM and VHI scores in patients with MTD which is due to the sequelae of the effect of RT and CRT in these patients of head and neck cancer of non-laryngeal origin. So the rehabilitation techniques are an effective targeted treatment options and should be widely used in the treatment of MTD by SLPs to improve the QoL of these patients.
Appendix
Funding
No funding was received for conducting this study.
Declarations
Conflict of Interest
None.
Ethical Approval
This study was approved by institute ethical committee. The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.
Informed Consent
Informed consent was taken in written by all the participants.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.American Speech-Language-Hearing Association CEU Part IV: Meta-Analysis. SIG 2 Perspect Neurophysiol Neurogen Speech Lang Disord. 2001;11:15–18. doi: 10.1044/nnsld11.1.15. [DOI] [Google Scholar]
- 2.Pereira GD, Lemos ID, Gadenz CD, Cassol M. Effects of voice therapy on muscle tension dysphonia: a systematic literature review. J Voice. 2018;32(5):546–552. doi: 10.1016/j.jvoice.2017.06.015. [DOI] [PubMed] [Google Scholar]
- 3.Benninger M, Holy C, Bryson P, Milstein C. Prevalence and occupation of patients presenting with dysphonia in the United States. J Voice. 2017;31:594–600. doi: 10.1016/j.jvoice.2017.01.011. [DOI] [PubMed] [Google Scholar]
- 4.Treister N, Sonis S. Mucositis: biology and management. Curr Opin Otolaryngol Head Neck Surg. 2007;15:123–129. doi: 10.1097/MOO.0b013e3280523ad6. [DOI] [PubMed] [Google Scholar]
- 5.Boscolo-Rizzo P, Maronato F, Marchiori C. Long-term quality of life after total laryngectomy and postoperative radiotherapy versus concurrent chemoradiotherapy for laryngeal preservation. Laryngoscope. 2008;118:300–306. doi: 10.1097/MLG.0b013e31815a9ed3. [DOI] [PubMed] [Google Scholar]
- 6.Mendonca DR. State of the patient after successful irradiation for laryngeal cancer. Laryngoscope. 1975;85:534–539. doi: 10.1288/00005537-197503000-00011. [DOI] [PubMed] [Google Scholar]
- 7.Kraus DH, Pfister DG, Harrison LB. Larynx preservation with combined chemotherapy and radiation therapy in advanced hypopharynx cancer. Otolaryngol Head Neck Surg. 1994;111:31–37. doi: 10.1177/019459989411100108. [DOI] [PubMed] [Google Scholar]
- 8.Stoicheff ML. Voice following radiotherapy. Laryngoscope. 1975;85:608–618. doi: 10.1288/00005537-197504000-00002. [DOI] [PubMed] [Google Scholar]
- 9.Stoicheff ML, Ciampi A, Passi JE, Fredrickson JM. The irradiated larynx and voice: a perceptual study. J Speech Hear Res. 1983;26:482–485. doi: 10.1044/jshr.2604.482. [DOI] [PubMed] [Google Scholar]
- 10.Morris MR, Canonico D, Blank C. A critical review of radiotherapy in the management of T1 glottic carcinoma. Am J Otolaryngol. 1994;15:276–280. doi: 10.1016/0196-0709(94)90095-7. [DOI] [PubMed] [Google Scholar]
- 11.Van Gogh CD, Verdonck-de Leeuw IM, Wedler-Peeters J, Langendijk JA, Mahieu HF. Prospective evaluation of voice outcome during the first two years in male patients treated by radiotherapy or laser surgery for T1a glottis carcinoma. Eur Arch Otorhinolaryngol. 2012;269(6):1647–1652. doi: 10.1007/s00405-012-1947-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Tsunoda K, Soda Y, Tojima H, Shinogami M, Ohta Y, Nibu K, et al. Stroboscopic observation of the larynx after radiation in patients with T1 glottic carcinoma. Acta Otolaryngol Suppl. 1997;527:165–166. doi: 10.3109/00016489709124064. [DOI] [PubMed] [Google Scholar]
- 13.Van Gogh CD, Verdonck-de Leeuw IM, Boon-Kamma BA, Rinkel RN, de Bruin MD, Langendijk JA, et al. The efficacy of voice therapy in patients after treatment for early glottic carcinoma. Cancer. 2006;106(1):95–105. doi: 10.1002/cncr.21578. [DOI] [PubMed] [Google Scholar]
- 14.Aronson AE. Clinical voice disorders: an interdisciplinary approach. 3. New York: Thieme; 1990. [Google Scholar]
- 15.Mehta DD, Hillman RE. Current role of stroboscopy in laryngeal imaging. Curr Opin Otolaryngol Head Neck Surg. 2012;20(6):429–436. doi: 10.1097/MOO.0b013e3283585f04. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Patel RR, Awan SN, Barkmeier-Kraemer J, Courey M, Deliyski D, Eadie T, Paul D, Švec JG, Hillman R. recommended protocols for instrumental assessment of voice: American speech-language-hearing association expert panel to develop a protocol for instrumental assessment of vocal function. Am J Speech-Lang Pathol. 2018;27:887–905. doi: 10.1044/2018_AJSLP-17-0009. [DOI] [PubMed] [Google Scholar]
- 17.Karnell MP, Melton SD, Childes JM, Coleman TC, Dailey SA, Hoffman HT. Reliability of clinical-based (GRBAS and CAPE-V) and patient-based (V-RQOL and IPVI) documentation of voice disorders. J Voice. 2007;21(5):576–590. doi: 10.1016/j.jvoice.2006.05.001. [DOI] [PubMed] [Google Scholar]
- 18.Roy N, Leeper HA. Effects of the manual laryngeal musculoskeletal tension reduction technique as a treatment for functional voice disorders: perceptual and acoustic measures. J Voice. 1993;7(3):242–249. doi: 10.1016/S0892-1997(05)80333-9. [DOI] [PubMed] [Google Scholar]
- 19.Aronson AE, Bless DM. Clinical voice disorders. New York: Thieme; 2011. [Google Scholar]
- 20.Meerschman I, Van Lierde K, Peeters K, Meersman E, Claeys S, D’haeseleer, E. Short-term effect of two semi-occluded vocal tract training programs on the vocal quality of future occupational voice users: “resonant voice training using nasal consonants” versus “straw phonation”. J Speech Lang Hear Res. 2017;60(9):2519–2536. doi: 10.1044/2017_JSLHR-S-17-0017. [DOI] [PubMed] [Google Scholar]
- 21.Boone DR, McFarlane SC, Von Berg SL (2005) The voice and voice therapy (7th ed.). Pearson/Allyn & Bacon. Retrieved July 18, 2022 from http://books.google.com/books?id=5b5sAAAAMAAJ
- 22.Meerschman I, Lierde K, Ketels J, Coppieters C, Claeys S, D’haeseleer, E. Effect of three semi-occluded vocal tract therapy programmes on the phonation of patients with dysphonia: lip trill, water-resistance therapy and straw phonation. Int J Lang Commun Disord. 2019;54(1):50–61. doi: 10.1111/1460-6984.12431. [DOI] [PubMed] [Google Scholar]
- 23.Stemple JC. Voice therapy: clinical case studies. St. Louis: Mosby-Year book, Inc; 1993. [Google Scholar]
- 24.Ferlay J, Soerjomataram I, Dikshit R, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–386. doi: 10.1002/ijc.29210. [DOI] [PubMed] [Google Scholar]
- 25.Brandwein-Gensler M, Smith RV. Prognostic indicators in head and neck oncology including the new 7th edition of the AJCC staging system. Head Neck Pathol. 2010;4:53–61. doi: 10.1007/s12105-010-0161-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Pan XB, Liu Y, Huang ST, Chen KH, Jiang YM, Zhu XD (2019) Predictors for improvement of xerostomia in nasopharyngeal carcinoma patients receiving intensity-modulated radiotherapy. Medicine (Baltimore) 98(36):1857–1866 [DOI] [PMC free article] [PubMed]
- 27.Dijkema T, Raaijmakers CP, Ten Haken RK, et al. Parotid gland function after radiotherapy: the combined Michigan and Utrecht experience. Int J Radiat Oncol Biol Phys. 2010;78(2):449. doi: 10.1016/j.ijrobp.2009.07.1708. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Villari CR, Courey MS. Management of dysphonia after radiation therapy. Otolaryngol Clin NA. 2016;48:601–609. doi: 10.1016/j.otc.2015.04.006. [DOI] [PubMed] [Google Scholar]
- 29.Kelly C (2018) Principles of chemotherapy. In: Watkinson J, Clarke R (eds) Scott Brown’s otorhinolaryngology and head neck surgery, vol 3, 8th edn. CRC Press, Boca Raton, pp 393–398
- 30.Lazarus CL. Effects of chemoradiotherapy on voice and swallowing. Curr Opin Otolaryngol Head Neck Surg. 2009;17:172–178. doi: 10.1097/MOO.0b013e32832af12f. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Kraaijenga SAC, Oskam IM, van Son RJJH, et al. Assessment of voice, speech, and related quality of life in advanced head and neck cancer patients 10-years + after chemoradiotherapy. Oral Oncol. 2016;55:24–30. doi: 10.1016/j.oraloncology.2016.02.001. [DOI] [PubMed] [Google Scholar]
- 32.Johns MM, Kolachala V, Berg E, et al. Radiation fibrosis of the vocal fold: from man to mouse. Laryngoscope. 2012;112:S107–S125. doi: 10.1002/lary.23735. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Hartley NA, Thibeault SL. Systemic hydration: relating science to clinical practice in vocal health. J Voice. 2014;28:652.e1–20. doi: 10.1016/j.jvoice.2014.01.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Tuomi L, Andréll P, Finizia C. Effects of voice rehabilitation after radiation therapy for laryngeal cancer: a randomized controlled study. Int J Radiat Oncol. 2014;89:964–972. doi: 10.1016/j.ijrobp.2014.04.030. [DOI] [PubMed] [Google Scholar]
- 35.Verdonck-de Leeuw IM, Keus RB, Hilgers FJM, et al. Consequences of voice impairment in daily life for patients following radiotherapy for early glottic cancer: voice quality, vocal function, and vocal performance. Int J Radiat Oncol Biol Phys. 1999;44:1071–1078. doi: 10.1016/S0360-3016(99)00110-8. [DOI] [PubMed] [Google Scholar]
- 36.Rovirosa A, Martinez-Celdran E, Ortega A, et al. Acoustic analysis after radiotherapy in T1 vocal cord carcinoma: a new approach to the analysis of voice quality. Int J Radiat Oncol Biol Phys. 2000;47:73–79. doi: 10.1016/S0360-3016(99)00524-6. [DOI] [PubMed] [Google Scholar]
- 37.Lierde KM, Ley SD, Clement G, Bodt MD, Cauwenberge PV. Outcome of laryngeal manual therapy in four Dutch adults with persistent moderate-to-severe vocal hyperfunction: a pilot study. J Voice. 2004;18(4):467–474. doi: 10.1016/j.jvoice.2004.02.003. [DOI] [PubMed] [Google Scholar]
- 38.Lucchini E, Maccarini AR, Bissoni E, Borragan M, Agudo M, González M, et al. Voice improvement in patients with functional dysphonia treated with the proprioceptive-elastic (PROEL) method. J Voice. 2018;32(2):209–215. doi: 10.1016/j.jvoice.2017.05.018. [DOI] [PubMed] [Google Scholar]
- 39.Speyer R. Effects of voice therapy: a systematic review. J Voice. 2008;22(5):565–580. doi: 10.1016/j.jvoice.2006.10.005. [DOI] [PubMed] [Google Scholar]
- 40.Watts CR, Hamilton A, Toles L, Childs L, Mau T. Intervention outcomes of two treatments for muscle tension dysphonia: a randomized controlled trial. J Speech Lang Hear Res. 2019;62(2):272–282. doi: 10.1044/2018_JSLHR-S-18-0118. [DOI] [PubMed] [Google Scholar]
- 41.Fung K, Yoo J, Leeper HA, et al. Effects of head and neck radiation therapy on vocal function. J Otolaryngol. 2001;30:133–139. doi: 10.2310/7070.2001.20192. [DOI] [PubMed] [Google Scholar]
- 42.Sreenivas A, Sreed-haran S, Narayan M, et al. Effect of vocal rehabilitation after chemoradiation for nonlaryngeal head and neck cancers. Acta Otorhinolaryngol Ital. 2021;41:131–141. doi: 10.14639/0392-100X-N0977. [DOI] [PMC free article] [PubMed] [Google Scholar]
