Olfactory function in laryngectomised patients: tracheo-oesophageal versus oesophageal speech| ACTA Otorhinolaryngologica Italica

Abstract

Objective. This study aimed to evaluate olfactory function in patients rehabilitated with oesophageal (ES) voice or tracheo-oesophageal (TES) prosthesis to further verify whether there were differences in smell alterations depending on voice rehabilitation modality.
Methods. A total of 40 patients who had undergone total laryngectomy participated in the study. Speech rehabilitation was achieved through TES in 20 patients (Group A) or ES in 20 patients (Group B). Olfactory function was evaluated using the Sniffin’ Sticks test.
Results. At olfactory evaluation, in Group A, 4/20 patients (20%) were anosmic, whereas 16/20 patients (80%) were hyposmic; in Group B, 11/20 patients (55%) were anosmic whereas 9/20 patients (45%) were hyposmic. A significant difference (p = 0.04) was found at global objective evaluation.
Conclusions. The study shows that the rehabilitation with TES contributes to maintaining a functioning, albeit limited, sense of smell.

Introduction

In the last three decades, the incidence of laryngeal cancer has increased by 12%, with Europe recording the highest number of deaths ¹. The type of the treatment for laryngeal cancer depends on the stage of the disease at diagnosis and can benefit from different modalities, including transoral laser microsurgery, open partial horizontal laryngectomy, and (chemo)radiotherapy, with good oncological and functional outcomes ^2-4. In the last two decades, organ preservation strategies have increased; this can be attributed to improvements in preoperative staging and follow-up as a result of enhanced imaging techniques ^5-7. Organ preservation surgery is aimed at preventing the highly mutilating intervention of total laryngectomy (TL) and maintaining laryngeal function in light of oncological radicality.

TL has significant psychophysical and social consequences for the patient’s quality of life ^8,9; this is attributed to the immediate loss of phonation, resulting from the removal of the larynx, and to alterations in respiratory and olfactory functions due to the permanent separation of the upper from the lower airways, which consequently results in a disconnection between the airways and the mouth and nose. Recovery of phonatory function can be achieved by an oesophageal speech (ES) or with a tracheo-oesophageal voice prosthesis (TES). In both methods of voice rehabilitation, an internal substitute sound source is placed in the pharyngoesophageal segment.

In recent years, functional recovery of phonation and pulmonary rehabilitation in patients undergoing TL ¹⁰ have received increasing attention ¹¹. However, the alteration in olfactory function is still underestimated.

Odours are perceived through the flow of air at the level of the olfactory cleft (orthonasal perception) and through odours derived from food (retronasal perception). Hypo-anosmia following TL can be attributed either to a reduction in airflow at the level of the olfactory cleft or to the interruption of complex neurosensory feedback mechanisms following multiple damage to peripheral nerves related to the surgical procedure ¹²; the former hypothesis is the most widely accepted ¹³.

Because the two methods of phonatory rehabilitation exploit a different mechanism for the passage of air to the upper and lower airways, they can affect the alteration of smells differently.

This study aims to evaluate olfactory function in patients rehabilitated with ES or TES, using the objective, Sniffin’ Sticks test, methodology, in order to determine whether there are differences in the alterations of smell depending on the voice rehabilitation modality used.

Materials and methods

Patients

This multicentric study was conducted among patients who had undergone TL and who were recruited during follow-up visits over the period from June 2020 to May 2021 at (1) Otolaryngology Unit, Department of Health Science, University of Catanzaro, Italy; (2) the Otolaryngology Unit, Cannizzaro Hospital, Catania, Italy. The only inclusion criterion was completion of a speech rehabilitation course with ES or TES for at least 6 months. Smell rehabilitation patients, patients previously affected by alterations of smell, inflammatory or neoplastic sinonasal pathologies, patients who did not undergo voice rehabilitation or used electrolaryngeal speech, non-self-sufficient patients with disabilities of the upper limbs or with cognitive impairments, patients with loco-regional recurrence, and patients who refused to participate in the study were excluded.

The rehabilitation programme with ES was accomplished from the 15^th through the 20^th day after TL, as soon as the patient was able to eat orally, whereas rehabilitation with TES began the day after the insertion of the prosthesis and included specific training that consisted, initially, of training the emission of isolated vowels, gradually building up to the pronunciation of short sentences. The average time for administration of the programmed speech therapy within which the ES was learned was three months, whereas the time needed to learn TES was a few weeks. All the patients were instructed by speech language pathologists with extensive experience in the rehabilitation of laryngectomised patients.

Patients underwent endoscopic evaluation of the nasal cavities through optical fibre rhinoscopy to assess the absence of rhinosinus pathologies. Olfactory function was evaluated using the Sniffin’ Sticks test (Burghardt^®, Wedel, Germany) for smell threshold and odour discrimination tests. The Sniffin’ Sticks test is a validated olfactory test that evaluates olfactory Threshold Discrimination and Identification (TDI) score by administering felt-tipped pens filled with odours to patients’ nostrils ¹⁴. For the olfactory threshold test, the threshold concentration at which the patient can identify n-butanol is established using a scale technique based on a forced choice of three alternatives. Among the pens presented, the patient must indicate the one they think contains the odorous substance. Odour discrimination ability is determined using 16 individual tests. Among the triplet presented, the patient must identify the marker that contains an odorous substance that differs from the other two. The odour identification test is conducted using 16 common odours. The patient must identify the smell by choosing the image or term that identifies it from the four variables presented. The numerical value obtained in the three tests is added to obtain the TDI score. TDI values ≥ 30.5 indicate normosmia, those from 16.6-30.5 hyposmia, and those ≤ 16.5 anosmia ¹⁵. The test was performed in a large and airy room, and patients were asked not to eat at least 2 hours before the test. Patients were also asked not to use body perfumes on the day they were tested. All the patients had their eyes covered before beginning the smell threshold and odour discrimination tests.

Statistical analysis

Statistical analysis was performed using Med-Calc software Version 19.4 (Mariakerke, Belgium). Means and standard deviations were further calculated. Fisher’s exact test was used to ascertain the differences between the demographic and clinicopathologic data of the two cohorts of patients. Mann Whitney test for independent samples was used to compare the results of the Sniffin’ Sticks test between Group A and Group B. A p-value less than 0.05 was considered statistically significant.

Results

A total of 40 patients participated in the study; 8 (20%) were females, and 32 (80%) were males. The mean age at diagnosis was 65.72 ± 10.34 SD (range 46-85) years. According to the TNM classification, 16 (40%) patients were in stage III, and 24 (60%) in stage IV. Eight (20%) of the enrolled patients were subjected to TL alone, 20 (50%) to TL and neck dissection (ND), and 12 (30%) to TL, ND, and adjuvant chemo/radiotherapy. The mean time elapsed from TL was 57.86 ± 85.74 SD months. Speech rehabilitation was achieved through TES in 20 patients (Group A) and ES in 20 patients (Group B). A primary TES prosthesis positioning was performed in all patients. A Provox Vega prosthesis (ATOS Medical) was also placed in all patients. Group A comprised 14 males (70%) and 6 females (30%) with a mean age of 66.1 ± 9.60 SD years (range 46-81). Group B comprised 18 males (90%) and 2 females (10%) with a mean age of 65.41 years ± 10.90 SD (range 54-85). The mean time elapsed from TL was 46.2 ± 93.06 SD (range 6-324) months and 70.5 ± 75.54 SD (range 6-252) months in groups A and B, respectively, with no significant difference (p = 0.32). Table I shows the demographic and clinical data for the two groups of patients.

Evaluation of olfactory function

At olfactory evaluation, using the Sniffin’ Sticks test, 15/40 (37.5%) were anosmic whereas 25/40 (62.5%) were hyposmic. In Group A, 4/20 patients (20%) were anosmic whereas 16/20 patients (80%) were hyposmic; in Group B, 11/20 patients (55%) were anosmic whereas 9/20 patients (45%) were hyposmic. Groups A and B were found to be significantly different at global olfactory evaluation (p = 0.04), highlighting that patients rehabilitated with TES have significantly better olfactory function than those rehabilitated with ES (Tab. II).

In Group A patients, the threshold result was 3.37 ± 4.49 SD whereas in Group B it was 1.41 ± 1.44 SD; discrimination in patients of Group A was 9.3 ± 3.30 SD whereas in Group B it was 7.75 ± 3.81 SD; identification in patients of Group A was 7.4 ± 2.41 SD and in Group B it was 6.66 ± 1.54 SD; TDI was 20.07 ± 6.75 SD and 15.83 ± 4.94 SD in Group A and Group B, respectively (Fig. 1). The results of the Sniffin’ Sticks test show a trend towards better outcomes with TES compared to ES, although the difference was not significant: threshold (p = 0.22); discrimination (p = 0.11); identification (p = 0.54); and TDI (p = 0.11) (Fig. 2).

Discussion

It is known that TL, performed for advanced stage laryngeal carcinomas or subglottic carcinomas, or as a salvage surgery for relapsing carcinomas, is associated with loss of laryngeal and nasal physiological functions.

Odorous substances reach the olfactory epithelium through the nasal airflow, where the olfactory neurons pick them up. The interruption of nasal airflow results in a lack of perception of odorous substances by the olfactory epithelium ¹⁶, causing hypo-anosmic conditions in laryngectomised patients. Odours are perceived through the passage of air at the level of the olfactory cleft (orthonasal perception) but also from odours in food (retronasal perception).

Over the years, several methods have been used to rehabilitate the sense of smell. Rehabilitation manoeuvers, such as the Nasal Airflow-Inducing Maneuver (NAIM), described by Hilgers et al. are currently being used. This manoeuver creates a negative pressure in the oral cavity and oropharynx to induce orthonasal airflow ¹⁷.

Another technique is that of the larynx bypass, described by Schwartz et al. ¹⁸, which is a device consisting of a flexible tube that connects the tracheostoma to the mouth, restoring orthonasal airflow. This method, although effective, is rarely used at present due to the poor handling of the device ¹⁹.

In our study, none of the patients had undergone olfaction rehabilitation prior to evaluation. Altogether, 37.5% of patients were anosmic and 62.5% were hyposmic.

To date, there are few studies on olfactory functionality with objective methodology, such as the Sniffin’Sticks test. Riva et al. ²⁰ noted hyposmia in all 50 laryngectomised patients enrolled in their study. Kesimli et al. ²¹ noted severe hyposmia and anosmia in 60 and 40% of cases, respectively, in 15 patients who had undergone total laryngectomy.

Haxel et al. ²² reported 72% anosmic, 16% hyposmic and 12% normo-osmic patients. However, in these studies, the modality of phonatory rehabilitation was not considered.

To the best of our knowledge, this study is the first to evaluate olfactory function in laryngectomised patients in relation to the modality of speech rehabilitation.

Patients rehabilitated with TES showed a lesser loss of smell than patients rehabilitated with ES. The smaller alteration in olfactory functionality in patients rehabilitated with TES can be explained by the different pathway of airflow in the vocal tract. Schutte et al. ²³ evaluated pressure and airflow parameters at the level of the sound source, the voice prosthesis, and the trachea in patients rehabilitated with ES and TES. In this study, it was found that the airflow expelled during the sound production in TES voice was considerably greater (131 ml/s) than in ES phonation (82 ml/s). Ng ²⁴ obtained a similar result: airflow in TES speakers was considerably greater (134.15 ml/s) than in ES patients (70.5 ml/s). These results correlated with the different anatomical/physiological situations in the two groups of patients. In TES phonation, air is supplied directly from the tank of the lungs, while in ES phonation, the volume of the air tank depends on the patient’s ability to aspirate and retain air in the oesophagus and stomach.

These results could explain why patients with TES may have a greater chance of perceiving odorous substances in a retronasal way, because a greater quantity of air at higher pressure arrives compared to patients with ES. Thus, the cells of the olfactory epithelium could be subjected to greater stimulation, which would allow them to reduce the degenerative phenomena of the neuroepithelium ¹²_.

Loss of laryngeal and nasal functions negatively affect the quality of life of these patients ^10,25. Over the years, specialists have placed much effort into rehabilitating patients for speech, breathing and smell, which are important functions when ensuring an adequate level of psycho-physical well-being ^{10,11,13,18,19,26}.

These results suggest that phonatory rehabilitation of total laryngectomised patients with TES improves quality of life not only because of good speech recovery, but also due to the partial maintenance of olfactory function.

This study is limited in that the number of patients recruited was small. These results need to be confirmed by additional studies with larger numbers of patients.

Conclusions

The present study shows that the rehabilitation of the laryngectomised patients with TES not only contributes to better quality of voice production, but also to maintaining functionality, albeit limited, of the sense of smell. It would, therefore, be useful to increase use of protocols for evaluation and rehabilitation of olfactory function by qualified personnel in these patients as quickly as possible after surgery.

Acknowledgements

We thank Mr. Taraso Luca, speech therapist, for his support in evaluation of patient’s olfactory function.

Conflict of interest statement

The authors declare no conflict of interest.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author contributions

MRB: study design, revision of the manuscript, final approval, final agreement; GOP: data collection and interpretation of data, drafting of the manuscript; AA: acquisition of data; GDD: acquisition of data; VS: study design of the manuscrip; EA: conception and design, interpretation of data, revising manuscript.

Ethical consideration

The study was approved by Ethics Committee Area Centro Regione Calabria -6/6/22-.

All the patients were informed of the purpose of the study before they gave written informed consent. This study was conducted ethically, with all study procedures being performed in accordance with the requirements of the World Medical Association’s Declaration of Helsinki.

Demographic and clinical data were collected.

Figures and tables

Figure 1.Results of Sniffin’ Sticks test.

Figure 2.Comparation of TDI results (Mann Whitney test for Indipendent samples).

References

1. Nocini R, Molteni G, Mattiuzzi C. Updates on larynx cancer epidemiology. Chin J Cancer Res. 2020; 32:18-25. DOI
2. Garozzo A, Allegra E, La Boria A. Modified supracricoid laryngectomy. Otolaryngol Head Neck Surg. 2010; 142:137-139. DOI
3. De Vincentiis M, De Virgilio A, Bussu F. Oncologic results of the surgical salvage of recurrent laryngeal squamous cell carcinoma in a multicentric retrospective series: emerging role of supracricoid partial laryngectomy. Head Neck. 2015; 37:84-91. DOI
4. Allegra E, Saita V, Azzolina A. Impact of the anterior commissure involvement on the survival of early glottic cancer treated with cricohyoidoepiglottopexy: a retrospective study. Cancer Manag Res. 2018; 10:5553-5558. DOI
5. Allegra E, Ferrise P, Trapasso S. Early glottic cancer: role of MRI in the preoperative staging. Biomed Res Int. 2014; 2014:890385. DOI
6. Allegra E, Saita V, De Natale M. Use of PET/CT to detect local and regional laryngeal cancer recurrence after surgery. Rep Med Imaging. 2017; 10:31-36. DOI
7. Allegra E, Bianco MR, Ralli M. Role of clinical-demographic data in survival rates of advanced laryngeal cancer. Medicina. 2021; 57:267. DOI
8. Hilgers FJ, Ackerstaff AH, Aaronson NK. Physical and psychosocial consequences of total laryngectomy. Clin Otolaryngol Allied Sci. 1990; 15:421-425. DOI
9. Li X, Li J, Shi Y. Psychological intervention improves life quality of patients with laryngeal cancer. Patient Prefer Adherence. 2017; 11:1723-1727. DOI
10. Allegra E, La Mantia I, Bianco MR. Respiratory rehabilitation with heat moisture exchanger after total laryngectomy: long-term evaluation. Otorinolaringologia. 2019; 69:63-68.
11. Allegra E, La Mantia I, Bianco MR. Verbal performance of total laryngectomized patients rehabilitated with esophageal speech and tracheoesophageal speech: impacts on patient quality of life. Psychol Res Behav Manag. 2019; 12:675-681. DOI
12. Miani C, Ortolani F, Bracale AM. Olfactory mucosa histological findings in laryngectomees. Eur Arch Otorhinolaryngol. 2003; 260:529-535. DOI
13. Manestar D, Tićac R, Maričić S. Amount of airflow required for olfactory perception in laryngectomees: a prospective interventional study. Clin Otolaryngol. 2012; 37:28-34. DOI
14. Bianco MR, Ralli M, Minni A. Evaluation of olfactory dysfunction persistence after COVID-19: a prospective study. Eur Rev Med Pharmacol Sci. 2022; 26:1042-1048. DOI
15. Oleszkiewicz A, Schriever VA, Croy I. Updated Sniffin’ Sticks normative data based on an extended sample of 9139 subjects. Eur Arch Otorhinolaryngol. 2019; 276:719-728. DOI
16. Caldas AS, Facundes VL, Melo TM. Modifications and evaluation of smell and taste functions in total laryngectomy: systematic review. J Soc Bras Fonoaudiol. 2011; 23:82-88. DOI
17. Hilgers FJ, van Dam FS, Keyzers S. Rehabilitation of olfaction after laryngectomy by means of a nasal airflow-inducing maneuver: the “polite yawning” technique. Arch Otolaryngol Head Neck Surg. 2000; 126:726-732. DOI
18. Schwartz DN, Mozell MM, Youngentob SL. Improvement of olfaction in laryngectomized patients with the larynx bypass. Laryngoscope. 1987; 97:1280-1286. DOI
19. Göktas O, Lammert I, Berl J. Rehabilitation des Riechvermögens nach Laryngektomie – der Riechschlauch. [Rehabilitation of the olfactory sense after laryngectomy – the larynx bypass.]. Laryngorhinootologie. 2005; 84:829-832. DOI
20. Riva G, Sensini M, Corvino A. Smell and taste impairment after total laryngectomy. Ann Otol Rhinol Laryngol. 2017; 126:548-554. DOI
21. Kesimli MC, Kaya D, Aydemir L. A simple method for olfactory rehabilitation following total laryngectomy. Eur Arch Otorhinolaryngol. 2021; 278:4917-4921. DOI
22. Haxel BR, Fuchs C, Fruth K. Evaluation of the efficacy of the ‘nasal airflow-inducing manoeuvre’ for smell rehabilitation in laryngectomees by means of the Sniffin’ Sticks test. Clin Otolaryngol. 2011; 36:17-23. DOI
23. Schutte HK, Nieboer GJ. Aerodynamics of esophageal voice production with and without a Groningen voice prosthesis. Folia Phoniatr Logop. 2002; 54:8-18. DOI
24. Ng ML. Aerodynamic characteristics associated with oesophageal and tracheoesophageal speech of Cantonese. Int J Speech Lang Pathol. 2011; 13:137-144. DOI
25. Hummel T, Nordin S. Olfactory disorders and their consequences for quality of life. Acta Otolaryngol. 2005; 125:116-121. DOI
26. Hamerlińska A. Applying nasal airflow – inducing maneuvers with patients with hyposmia after total laryngectomy. Contemp Oncol (Pozn). 2019; 23:141-145. DOI