Subjective and Objective Assessment of Effect of Allergic Rhinitis on Voice in Indian Patients

Abstract

To perform a subjective and objective assessment of vocal complaints in patients of allergic rhinitis (AR) using voice handicap index and video-stroboscopy respectively and find the association of their parameters with severity of the disease. Cross-sectional-observational study design. Outpatient department of Otorhinolaryngology of a tertiary centre. Seventy-five adult patients diagnosed with AR and classified according to ‘Allergic Rhinitis and its Impact on Asthma’ guidelines were compared with same number of normal subjects as controls, with the same age and sex, to ensure uniformity. Both the groups were asked to fill a self-answered questionnaire called Voice Handicap Index (VHI) and underwent laryngeal examination with Video-Stroboscopy (VS). The mean VHI score of the AR group (29.45 ± 32.11) was significantly higher (p < 0.05) than that of controls (12.07 ± 16.62). VS parameters including amplitude, supraglottic activity, vocal edge and phase closure also showed significant difference between cases and controls (p < 0.05). VHI scores increased, but the VS findings did not change significantly with the severity of the disease. AR patients show subjective and objective derangements of voice quality. VHI scores show increase, while VS parameters do not change with the severity of AR.

Introduction

Allergic rhinitis (AR) is the commonest manifestation of atopy [1]. AR affects 10 to 25% of the world population and 20–30% of the Indian population [2]. It presents as watery rhinorrhoea, paroxysmal sneezing, nasal obstruction and itching. About 19–38% of AR patients have asthma and 30–80% of asthmatics have AR [3]. Allergy has its impact on the entire immune system of human being and can affect any organ or any tissue. According to the concept of unified airway, inflammation in any part of the airway can lead to inflammation of the whole, including larynx [4]. Voice changes occurring due to AR poses to be a major concern in non-professional and professional voice users as the voice changes have been commonly associated with allergy. However, the general population considers it trivial, even though it causes significant worsening of quality of life [2, 5]. Voice handicap index (VHI) and Video-Stroboscopy (VS) have emerged as valuable tools in researching the effect of allergy in phonation [5–15].

The effects of allergy in phonation have not been explored in Indian population and there is a paucity of literature in this regard. On searching Google Scholar and Pubmed with keywords ‘allergic rhinitis’, ‘voice changes’ and ‘India’ on 2nd June 2020, we found 2250 and 20 articles respectively. Several authors from different parts of the world have tried to find out the effect of AR on phonation using different parameters. Though, the factors that affect the genesis and course of disease vary in different geographical locations of the world, we however, could not find any published work from India that seems to have investigated the effect of AR on voice, without medical treatment, using the above search criteria. Therefore, the aim of this study is to perform a subjective and objective assessment of vocal complaints in patients of AR using VHI and VS respectively and find the relation of their parameters with severity of the disease.

Methods

The present study follows a cross-sectional-observational study design, where authors have tried to compare the findings of VHI and VS in normal and AR patients. All patients and controls were taken from the out-patient-department (OPD) of Otorhinolaryngology of a tertiary care centre. Seventy-five adult patients diagnosed with AR from October 2018 to February 2020 were compared with same number of normal subjects as controls. The subjects taken as controls were of the same age and sex as that of patients with AR, but they did not have any kind of history related with allergy in any part of the body. This was done to maintain uniformity in the results. The patients were selected on the basis of common symptoms of AR like sneezing, nasal itching, rhinorrhoea, nasal congestion, pharyngeal itching and watering of eyes. They were then classified according to ARIA (Allergy and its impact on asthma), 2001 guidelines [16]. Subjects and patients having confounding factors like professional voice users, workers of chemical related (dye, cement etc.) factories, wool-cotton industries, coal mine, patients on anti-allergic medications for more than 4 weeks, laryngeal intubation within past 3 months, smokers, patients of hypothyroidism, asthma, laryngopharyngeal reflux diseases, vocal fold pathology like vocal nodule, malignancy etc. and any kind of surgery to the vocal fold (VF), were excluded from the study.

After enrolment, participants answered a validated questionnaire termed as VHI, which comprises of 30 questions. Each of these questions grades the difficulty these patients experience either physically, emotionally or functionally due to abnormal changes in voice. All the participants provided answers in the form of ratings against individual questions, given on a 5-point scale (0–4), and the cumulative sum of the points is categorized into mild, moderate, and severe with the score of 0 to 30, 31 to 60, and 61 to 120 respectively. All subjects were also examined with video-stroboscope (40160120 Karl Storz Pulsar II). VS parameters assessed were vocal cord symmetry, amplitude, non-vibratory segment, phase closure, glottic closure pattern, supra-glottic activity, vocal edge and mucosal wave.

Nonparametric tests like Mann Whitney U test, Chi square and Fischer’s exact test were used to analyse qualitative data obtained by comparing the results. All differences associated with a chance probability of < 0.05 were considered statistically significant. Sample size was calculated using the formula: n = (2 × (zα + zβ) 2 × s2) ÷ d2.

Results

All the participants of the study were between the age group 18–65 years, male: female ratio was 1.7:1. Youngest participant was 18 years and the eldest was 62 years. The mean age of cases was 32.85 ± 11.09 and that of controls was 32.92 ± 10.71 (no significant difference).

The mean VHI score of the AR group (29.45 ± 32.11) was significantly higher (Mann–Whitney U Test, p < 0.05) than that of controls (12.07 ± 16.62) (Table 1). Majority (60% in cases, and 90.7% in controls) of the participants in both the groups had VHI score between 0 and 30 (mild VHI severity) (Table 2). It was found that VHI scores significantly increased with severity of AR which was determined as per ARIA guidelines (Fisher’s Exact Test, p < 0.05) (Table 3).

Table 1.

Mean VHI score of cases and controls

VHI Score	Group		Mann–Whitney U test
	Case¥	Control¥¥	U	p value
Mean (SD)	29.45 ± 32.11	12.07 ± 16.62	3568.500	0.004
Median (IQR)	17 (43)	5 (7)
Range	0–109	0–66

VHI Voice handicap index

n^¥ = 75; n^¥¥ = 75

Table 2.

Severity of VHI score among cases and controls

VHI severity	Group		Chi-squared test
	Case¥ (%)	Control¥¥ (%)	X^2	p value
Mild	60.0	90.7	18.979	< 0.001
Moderate	22.7	5.3
Severe	17.3	4.0
Total	100.0	100.0

n^¥ = 75; n^¥¥ = 75

VHI Voice handicap index

Table 3.

Association between severity of AR and severity of VHI

VHI Severity	Severity of AR (ARIA)				Fisher's exact test
	Mild intermittent¥ (%)	Mild persistent¥¥ (%)	Moderate/severe intermittent¥¥¥ (%)	Moderate/severe persistent¥¥¥¥ (%)	X^2	p value
Mild	66.7	33.3	55.2	84.2	13.131	0.028
Moderate	33.3	40.0	20.7	5.3
Severe	0.0	26.7	24.1	10.5

n^¥ = 12; n^¥¥ = 15, n^¥¥¥ = 29, n^¥¥¥¥ = 19

Comparison of VS parameters in cases and controls is shown in Table 4. Amplitude was significantly lower in AR patients than controls (Fisher’s Exact Test, p < 0.05) (Fig. 1). Phase closure pattern was ‘predominantly open’ type in both the groups. However, the percentage of ‘predominantly closed’ type and ‘half open–half closed’ type was significantly more in AR patients (Fisher’s Exact Test for all, p < 0.05) (Fig. 2). Presence of ventricular band and anterior–posterior hypercontraction type of supra-glottic activity was greater in AR group (Fisher’s Exact Test for all, p < 0.05) (Fig. 3). Abnormal vocal edge patterns of concave and convex types were seen more frequently in AR patients than controls (Chi-square test for vocal fold edges, p < 0.05) (Fig. 2). It was also noted that VS findings did not change significantly the severity of AR determined as per ARIA guidelines (Table 3).

Table 4.

Videostroboscopic findings in cases and controls

Parameters	Case (%)¥	Control (%)¥¥	p value
Vocal cord symmetry			0.137
Symmetrical	77.3	86.7
Asymmetrical	22.7	13.3
Amplitude (right)			0.013
Normal	70.7	88.0
Increased	4.0	0.0
Decreased	25.3	12.0
Amplitude (left)			0.095
Normal	73.3	85.3
Increased	4.0	0.0
Decreased	22.7	14.7
Non-vibratory segment (right)			0.163
None	84.0	86.7
Anterior 1/3rd	8.0	12.0
Middle 1/3rd	5.3	0.0
Posterior 1/3rd	2.7	1.3
Non-vibratory segment (left)			0.290
None	89.3	84.0
Anterior 1/3rd	4.0	12.0
Middle 1/3rd	4.0	1.3
Posterior 1/3rd	2.7	2.7
Phase closure			0.010
Predominantly closed	28.0	24.0
Half closed half open	28.0	10.7
Predominantly open	44.0	65.3
Closure			0.505
Complete closure	89.3	90.7
No closure	1.3	4.0
Hourglass	1.3	0.0
Spindle	2.7	2.7
Posterior glottic chink	4.0	0.0
Anterior glottic chink	1.3	2.7
Supraglottic activity			< 0.001
Normal	78.7	100.0
Ventricular band	10.7	0.0
Anterior posterior hyper-contraction	10.7	0.0
Vocal edge			0.002
Normal	69.3	92.0
Concave	12.0	2.7
Convex	18.7	5.3
Mucosal wave			0.120
Present	94.7	100.0
Restricted	5.3	0.0

n^¥ = 75; n^¥¥ = 75

Fig. 1.

Stroboscopic image showing a normal, b decreased amplitude

Fig. 2.

Stroboscopic image showing different patterns of glottic phase closure a predominantly open with concave edge of left vocal fold, b predominantly closed pattern

Fig. 3.

Stroboscopic image showing different patterns of supraglottic activity a antero-posterior hypercontraction, b ventricular hypercontraction

Discussion

Allergies are in the rising trend in the world since the last 10–15 years [17]. In western population, ‘hygiene hypothesis’ has recently been used to explain the increasing trend of AR [18]. In India, urbanization, changing life styles and increasing pollution attribute to increase in cases [17]. In India AR causes significant burden on the economy as patients self-treat themselves by taking over the counter medications frequently, instead of seeking a doctor’s advice. Consequently, they cause more loss of work productivity due to ‘presenteeism’ (percentage impairment at work) than ‘absenteeism’ (percentage work time missed) [19].

Interaction between respiratory, laryngeal and resonator systems is required for voice production, which gets disturbed in AR. The association between disease processes of upper and lower airway with respect to AR and asthma is well established, and its effect on larynx, which is the connection between upper and lower airway has well been reported by various authors using different parameters worldwide [13, 14]. However, these researches come from countries in which the factors, which determine the etiopathogenesis and natural progression of the disease such as allergens, weather, geographical location, pollutants, genetic make-up of population, pattern of addictions, lifestyle, healthcare facilities etc., are very different from that of India. Therefore, the authors of present study realised the need for a study that investigates the established assessment parameters of phonation in Indian population.

VHI is a simple questionnaire developed by Jacobson et. al. in 1997, to measure the patient’s perception of the impact of the voice disorder. It also serves as a tool to monitor the treatment efficacy [20]. It has been used to assess voice quality in many different voice disorders for several years after its invention. Several authors have established the presence of voice changes in patients of AR with the help of VHI [5–11] (Table 5). This study substantiates the discovery of significant changes in VHI scores of AR patients, and its increase in severity with increase in severity of AR (Table 3).

Table 5.

Comparison of variations in mean VHI scores in various studies

Authors	Year	Mean VHI score
		Cases	Controls
Krouse et al	2008	9.52	4.15
Millqvist et al	2008	18.3 ± 17.2 (pollen season) 13.9 ± 11.3 (non-pollen season)	2.8 ± 5.3 (pollen season) 6.0 ± 9.1 (non-pollen season)
Develioglu et al	2013	24.82 ± 7.59 (pre-treatment) 14.76 ± 3.87 (post-treatment)	–
Koc et al	2014	18.3 ± 17.2	2.8 ± 5.3
Erkan et al	2019	Group 1 Pre-treatment: 7 Post treatment: 5.15 Group 2 Pre-treatment: 6.25 Post treatment: 4.65
Present study	2020	29.45 ± 32.11	12.07 ± 16.62

VS objectively assesses the parameters resulting in change of voice. Bless et al. [21] identified stroboscopic parameters and introduced VS rating form for better assessment of VS findings. There occur acute changes in the vocal folds (VF) soon after exposure to the allergen, which have shown to cause derangement of VS parameters although the results vary in chronic cases [12, 13]. Thick tenacious secretions produced by nasal glands in AR patients hinder with the movement of the mucosa causing abnormal vibration. AR patients also have frequent need to clear their throat that could lead to minor trauma to the VF and VF oedema. Inflammatory mediators also can lead to VF oedema [14]. Earlier researchers could not explain any allergic pathophysiologic process known to occur with the VF as it occurs in the nasal mucosa, but Roth et. al. in 2010 reported that changes in the vocal function could be the result of some type of inflammatory process within the larynx, laryngeal irritation due to secretions or a generalized airway response initiated by sinonasal mucosa. They also explained that lower airway inflammation or constriction can independently affect the voice [14, 15]. The findings of VS of past researchers and the present study are mentioned in (Table 6). Most studies including the present study have reported significant changes in parameters like amplitude, phase closure, vocal fold edge, and supra-glottic activity.

Table 6.

Comparison of variations in VS findings in various studies

Authors	Year	Stroboscopic findings
		Positive	Negative
Menaldi et. al	1997	Phase closure, amplitude, supraglottic activity
Dixon et. al	1999	Irregular waveform noted post stimulation of nasal allergy up to 10 min after stimulation
Reidy et. al	2003	Minimal abnormal vocal fold vibrations post exposure to allergen
Koc et. al	2014		Vocal fold edge, closure level, supraglottic involvement, amplitude, mucosal wave, non-vibratory portion and closure phase
Present study	2020	Phase closure, vocal fold edge, amplitude, supraglottic activity

In the literature that authors could explore as per the limited search criteria, no study had reported the relation of severity of AR as per ARIA (Allergic Rhinitis and its Impact on Asthma) guidelines with the given parameters [16]. It is however, interesting to note in the present study that, though VHI scores increased significantly with the severity of the disease, the VS findings did not appear to change significantly with it (Table 3).

Conclusions

Cases suffering from AR show a subjective–objective derangement of voice quality as determined with VHI and VS respectively. The changes of parameters of VHI and VS observed in Indian population suffering from AR is similar to the studies published in other parts of the world. VHI scores increased, but the VS findings did not change significantly with the severity of the disease. VHI and VS can be used in AR patients to assess the degree of severity, understand the pathophysiology better and to monitor the effect of treatment. The authors however, realise the need for a prospective pre-test and post-test study design with a larger number of patients and follow-up. Studying the voice parameters separately in seasonal and perineal AR can further deepen our understanding on the subject.

Author’s Contribution

VS, MM, MP, AB: conception, design, acquisition, analysis, and interpretation of data. AKT, VA, NK, AM: responsible for revising the manuscript critically for intellectual content.

Funding

The authors declare that this study has received no financial support.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with ethical standards of the institutional and/or National research committee. This article does not contain any studies on animals performed by any authors.

Informed Consent

Written informed consent was obtained from all participants prior to the study.