10.14639/0392-100X-N2253
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.
text/xml
1827-675X
2253
en
Eugenia Allegra
http://creativecommons.org/licenses/by-nc-nd/4.0
ACTA Otorhinolaryngologica Italica
smell dysfunction
Olfactory function in laryngectomised patients: tracheo-oesophageal versus oesophageal speech
Text.Serial.Journal
https://www.actaitalica.it/
43
Head and neck
2023-02-27
2022-08-02
2023-02-28
2023-02-28
20-25
1
Eugenia Allegra
2023/02/27
10.14639/0392-100X-N2253
20
Otolaryngology, Department of Health Science, University of Catanzaro, Italy
1827-675X
smell dysfunction
en
25
Olfactory function in laryngectomised patients: tracheo-oesophageal versus oesophageal speech
https://www.actaitalica.it/article/download/2253/914
43
ACTA OTORHINOLARYNGOLOGICA ITALICA 2023;43:20-25; doi: 10.14639/0392-100X-N2253




Head and neck


Olfactory function in laryngectomised patients:
tracheo-oesophageal versus oesophageal speech
Funzione olfattiva nei pazienti laringectomizzati: voce tracheo-esofagea versus voce
esofagea
Maria Rita Bianco1, Grazia Ornella Pricoco1, Alfio Azzolina2, Gaetano Davide Drago2, Vincenzo Saita2, Eugenia Allegra1
1
    Otolaryngology, Department of Health Science, University of Catanzaro, Italy; 2 Otolaryngology Unit, Cannizzaro Hospital, Catania, Italy


SUMMARY
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, where-
as 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.
KEY WORDS: total laryngectomy, oesophageal speech, voice prosthesis, Sniffin’ Sticks
test, smell dysfunction

RIASSUNTO
Obiettivo. Questo studio si propone di valutare la funzione olfattiva nei pazienti laringec-    Received: August 2, 2022
tomizzati totali riabilitati con voce esofagea (ES) e con protesi tracheo-esofagea (TES)        Accepted: December 23, 2022
per valutare se esistono differenze nell’alterazione dell’olfatto a seconda delle modalità di
riabilitazione vocale.                                                                          Correspondence
Metodi. Un totale di 40 pazienti sottoposti a laringectomia totale hanno partecipato allo       Maria Rita Bianco
studio. La riabilitazione del linguaggio è stata ottenuta attraverso TES (Gruppo A) in 20       Otolaryngology-Head and Neck Surgery, De-
pazienti o mediante ES in 20 pazienti (Gruppo B). La funzione olfattiva è stata valutata        partment of Health Sciences, University Magna
utilizzando lo Sniffin’ Sticks test.                                                            Graecia of Catanzaro, viale Europa, 88100 Germa-
Risultati. Alla valutazione della funzione olfattiva, nel Gruppo A, 4/20 pazienti (20%) era-    neto (CZ), Italy
no anosmici mentre 16/20 pazienti (80%) erano iposmici; nel gruppo B, 11/20 pazienti            E-mail: mrbianco@unicz.it
(55%) erano anosmici mentre 9/20 pazienti (45%) erano iposmici. È stata riscontrata una
differenza statisticamente significativa tra i due gruppi alla valutazione oggettiva globale      How to cite this article: Bianco MR, Prico-
con Sniffin’ Sticks test (p = 0,04).                                                              co GO, Azzolina A, et al. Olfactory function
Conclusioni. Lo studio mostra che la riabilitazione con protesi tracheo-esofagea contribu-        in laryngectomised patients: tracheo-oesopha-
isce a mantenere una funzionalità, seppur limitata, dell’olfatto.                                 geal versus oesophageal speech. Acta Otorhi-
                                                                                                  nolaryngol Ital 2023;43:20-25. https://doi.
PAROLE CHIAVE: laringectomia totale, voce esofagea, protesi fonatoria, Sniffin’ Sticks            org/10.14639/0392-100X-N2253
test, disfunzione dell’olfatto
                                                                                                © Società Italiana di Otorinolaringoiatria
                                                                                                e Chirurgia Cervico-Facciale

Introduction                                                                                                   OPEN ACCESS

In the last three decades, the incidence of laryngeal cancer has increased by                   This is an open access article distributed in accordance with
                                                                                                the CC-BY-NC-ND (Creative Commons Attribution-Non-
12%, with Europe recording the highest number of deaths 1. The type of the                      Commercial-NoDerivatives 4.0 International) license. The
treatment for laryngeal cancer depends on the stage of the disease at diagno-                   article can be used by giving appropriate credit and mentio-
                                                                                                ning the license, but only for non-commercial purposes and
sis and can benefit from different modalities, including transoral laser micro-                 only in the original version. For further information: https://
surgery, open partial horizontal laryngectomy, and (chemo)radiotherapy, with                    creativecommons.org/licenses/by-nc-nd/4.0/deed.en




20
                                                                                            Olfactory function in laryngectomised patients




good oncological and functional outcomes 2-4. In the last           Unit, Cannizzaro Hospital, Catania, Italy. The only inclu-
two decades, organ preservation strategies have increased;          sion criterion was completion of a speech rehabilitation
this can be attributed to improvements in preoperative stag-        course with ES or TES for at least 6 months. Smell rehabil-
ing and follow-up as a result of enhanced imaging tech-             itation patients, patients previously affected by alterations
niques 5-7. Organ preservation surgery is aimed at prevent-         of smell, inflammatory or neoplastic sinonasal pathologies,
ing the highly mutilating intervention of total laryngectomy        patients who did not undergo voice rehabilitation or used
(TL) and maintaining laryngeal function in light of onco-           electrolaryngeal speech, non-self-sufficient patients with
logical radicality.                                                 disabilities of the upper limbs or with cognitive impair-
TL has significant psychophysical and social consequences           ments, patients with loco-regional recurrence, and patients
for the patient’s quality of life 8,9; this is attributed to the    who refused to participate in the study were excluded.
immediate loss of phonation, resulting from the removal             The rehabilitation programme with ES was accomplished
of the larynx, and to alterations in respiratory and olfac-         from the 15th through the 20th day after TL, as soon as the
tory functions due to the permanent separation of the up-           patient was able to eat orally, whereas rehabilitation with
per from the lower airways, which consequently results in           TES began the day after the insertion of the prosthesis and
a disconnection between the airways and the mouth and               included specific training that consisted, initially, of train-
nose. Recovery of phonatory function can be achieved by             ing the emission of isolated vowels, gradually building up
an oesophageal speech (ES) or with a tracheo-oesophageal            to the pronunciation of short sentences. The average time
voice prosthesis (TES). In both methods of voice rehabili-          for administration of the programmed speech therapy with-
tation, an internal substitute sound source is placed in the        in which the ES was learned was three months, whereas the
pharyngoesophageal segment.                                         time needed to learn TES was a few weeks. All the patients
In recent years, functional recovery of phonation and pul-          were instructed by speech language pathologists with ex-
monary rehabilitation in patients undergoing TL 10 have             tensive experience in the rehabilitation of laryngectomised
received increasing attention 11. However, the alteration in        patients.
olfactory function is still underestimated.                         Patients underwent endoscopic evaluation of the nasal
Odours are perceived through the flow of air at the level           cavities through optical fibre rhinoscopy to assess the
of the olfactory cleft (orthonasal perception) and through          absence of rhinosinus pathologies. Olfactory function
odours derived from food (retronasal perception). Hypo-             was evaluated using the Sniffin’ Sticks test (Burghardt®,
anosmia following TL can be attributed either to a reduc-           Wedel, Germany) for smell threshold and odour dis-
tion in airflow at the level of the olfactory cleft or to the in-   crimination tests. The Sniffin’ Sticks test is a validated
terruption of complex neurosensory feedback mechanisms              olfactory test that evaluates olfactory Threshold Discrim-
following multiple damage to peripheral nerves related to           ination and Identification (TDI) score by administering
the surgical procedure 12; the former hypothesis is the most        felt-tipped pens filled with odours to patients’ nostrils 14.
widely accepted 13.                                                 For the olfactory threshold test, the threshold concentra-
Because the two methods of phonatory rehabilitation ex-             tion at which the patient can identify n-butanol is estab-
ploit a different mechanism for the passage of air to the           lished using a scale technique based on a forced choice of
upper and lower airways, they can affect the alteration of          three alternatives. Among the pens presented, the patient
smells differently.                                                 must indicate the one they think contains the odorous
This study aims to evaluate olfactory function in patients          substance. Odour discrimination ability is determined us-
rehabilitated with ES or TES, using the objective, Sniffin’         ing 16 individual tests. Among the triplet presented, the
Sticks test, methodology, in order to determine whether             patient must identify the marker that contains an odor-
there are differences in the alterations of smell depending         ous substance that differs from the other two. The odour
on the voice rehabilitation modality used.                          identification test is conducted using 16 common odours.
                                                                    The patient must identify the smell by choosing the im-
                                                                    age or term that identifies it from the four variables pre-
Materials and methods                                               sented. The numerical value obtained in the three tests is
Patients                                                            added to obtain the TDI score. TDI values ≥ 30.5 indicate
This multicentric study was conducted among patients who            normosmia, those from 16.6-30.5 hyposmia, and those
had undergone TL and who were recruited during follow-              ≤ 16.5 anosmia 15. The test was performed in a large and
up visits over the period from June 2020 to May 2021 at             airy room, and patients were asked not to eat at least 2
(1) Otolaryngology Unit, Department of Health Science,              hours before the test. Patients were also asked not to use
University of Catanzaro, Italy; (2) the Otolaryngology              body perfumes on the day they were tested. All the pa-



                                                                                                                                      21
M.R. Bianco et al.




tients had their eyes covered before beginning the smell                      prosthesis (ATOS Medical) was also placed in all patients.
threshold and odour discrimination tests.                                     Group A comprised 14 males (70%) and 6 females (30%)
                                                                              with a mean age of 66.1 ± 9.60 SD years (range 46-81).
Statistical analysis                                                          Group B comprised 18 males (90%) and 2 females (10%)
Statistical analysis was performed using Med-Calc soft-                       with a mean age of 65.41 years ± 10.90 SD (range 54-85).
ware Version 19.4 (Mariakerke, Belgium). Means and                            The mean time elapsed from TL was 46.2 ± 93.06 SD
standard deviations were further calculated. Fisher’s exact                   (range 6-324) months and 70.5 ± 75.54 SD (range 6-252)
test was used to ascertain the differences between the de-                    months in groups A and B, respectively, with no significant
mographic and clinicopathologic data of the two cohorts of                    difference (p = 0.32). Table I shows the demographic and
patients. Mann Whitney test for independent samples was                       clinical data for the two groups of patients.
used to compare the results of the Sniffin’ Sticks test be-
tween Group A and Group B. A p-value less than 0.05 was                       Evaluation of olfactory function
considered statistically significant.                                         At olfactory evaluation, using the Sniffin’ Sticks test, 15/40
                                                                              (37.5%) were anosmic whereas 25/40 (62.5%) were hypos-
                                                                              mic. In Group A, 4/20 patients (20%) were anosmic where-
Results
                                                                              as 16/20 patients (80%) were hyposmic; in Group B, 11/20
A total of 40 patients participated in the study; 8 (20%)                     patients (55%) were anosmic whereas 9/20 patients (45%)
were females, and 32 (80%) were males. The mean age at                        were hyposmic. Groups A and B were found to be signifi-
diagnosis was 65.72 ± 10.34 SD (range 46-85) years. Ac-                       cantly different at global olfactory evaluation (p = 0.04),
cording to the TNM classification, 16 (40%) patients were                     highlighting that patients rehabilitated with TES have sig-
in stage III, and 24 (60%) in stage IV. Eight (20%) of the                    nificantly better olfactory function than those rehabilitated
enrolled patients were subjected to TL alone, 20 (50%) to                     with ES (Tab. II).
TL and neck dissection (ND), and 12 (30%) to TL, ND,                          In Group A patients, the threshold result was 3.37 ± 4.49 SD
and adjuvant chemo/radiotherapy. The mean time elapsed                        whereas in Group B it was 1.41 ± 1.44 SD; discrimination
from TL was 57.86 ± 85.74 SD months. Speech rehabilita-                       in patients of Group A was 9.3 ± 3.30 SD whereas in Group
tion was achieved through TES in 20 patients (Group A)                        B it was 7.75 ± 3.81 SD; identification in patients of Group
and ES in 20 patients (Group B). A primary TES prosthesis                     A was 7.4 ± 2.41 SD and in Group B it was 6.66 ± 1.54 SD;
positioning was performed in all patients. A Provox Vega                      TDI was 20.07 ± 6.75 SD and 15.83 ± 4.94 SD in Group


Table I. Demographic and clinical data of the Group A (TES) and Group B (ES).
                                                                      Group A (n = 20)         Group B (n = 20)             P-value
 Age (years)
   < 60                                                                  6 (30%)                   11(55%)                   0.20
   > 60                                                                  14 (70%)                  9 (45%)
 Sex
   Male                                                                  14 (70%)                 18 (90%)                   0.23
   Female                                                                 6 (30%)                  2 (10%)
 Time since TL
   Mean ± SD (months)                                                  46.2 ± 93.06              70.5 ± 75.54                0.32
 Stage
   III                                                                   7 (35%)                  9 (45%)                    0.74
   IV                                                                    13 (65%)                 11 (55%)
 Neck dissection
   No                                                                    16 (80%)                 18 (90%)                   0.66
   Yes                                                                    4 (20%)                  2 (10%)
 Adjuvant treatment
   No                                                                    6 (30%)                  12 (60%)                   0.06
   Yes                                                                   14 (70%)                  8 (40%)
TL: Total laryngectomy.




22
                                                                                                     Olfactory function in laryngectomised patients




Table II. Objective olfactory test (Sniffin’ Sticks test).
 Sniffin’ Sticks test                                Hyposmia                                   Anosmia                               P-value
                                        (values between 16.6 and 30.5)                       (values ≤ 16.5)
 Group A                                         16 (80%)                                        4 (20%)                             P = 0.04
 Group B                                          9 (45%)                                       11 (55%)



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 laryn-
geal 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 percep-
tion of odorous substances by the olfactory epithelium 16,
causing hypo-anosmic conditions in laryngectomised pa-                   Figure 2. Comparation of TDI results (Mann Whitney test for Indipendent
tients. Odours are perceived through the passage of air at               samples).
the level of the olfactory cleft (orthonasal perception) but
also from odours in food (retronasal perception).
                                                                         the Nasal Airflow-Inducing Maneuver (NAIM), described
Over the years, several methods have been used to rehabili-
tate the sense of smell. Rehabilitation manoeuvers, such as              by Hilgers et al. are currently being used. This manoeuver
                                                                         creates a negative pressure in the oral cavity and orophar-
                                                                         ynx 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 flex-
                                                                         ible tube that connects the tracheostoma to the mouth, re-
                                                                         storing 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 pa-
                                                                         tients 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 laryngecto-
                                                                         mised patients enrolled in their study. Kesimli et al. 21 not-
                                                                         ed severe hyposmia and anosmia in 60 and 40% of cases,
                                                                         respectively, in 15 patients who had undergone total lar-
                                                                         yngectomy.
                                                                         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.
Figure 1. Results of Sniffin’ Sticks test.                               To the best of our knowledge, this study is the first to evalu-



                                                                                                                                                23
M.R. Bianco et al.




ate olfactory function in laryngectomised patients in rela-         Acknowledgements
tion to the modality of speech rehabilitation.                      We thank Mr. Taraso Luca, speech therapist, for his support
Patients rehabilitated with TES showed a lesser loss of             in evaluation of patient’s olfactory function.
smell than patients rehabilitated with ES. The smaller al-
teration in olfactory functionality in patients rehabilitated       Conflict of interest statement
with TES can be explained by the different pathway of air-          The authors declare no conflict of interest.
flow in the vocal tract. Schutte et al. 23 evaluated pressure
and airflow parameters at the level of the sound source, the        Funding
voice prosthesis, and the trachea in patients rehabilitated         This research did not receive any specific grant from fund-
with ES and TES. In this study, it was found that the air-          ing agencies in the public, commercial, or not-for-profit
flow expelled during the sound production in TES voice              sectors.
was considerably greater (131 ml/s) than in ES phonation
(82 ml/s). Ng 24 obtained a similar result: airflow in TES          Author contributions
speakers was considerably greater (134.15 ml/s) than in             MRB: study design, revision of the manuscript, final ap-
ES patients (70.5 ml/s). These results correlated with the          proval, final agreement; GOP: data collection and interpre-
different anatomical/physiological situations in the two            tation of data, drafting of the manuscript; AA: acquisition
groups of patients. In TES phonation, air is supplied di-           of data; GDD: acquisition of data; VS: study design of the
rectly from the tank of the lungs, while in ES phonation,           manuscrip; EA: conception and design, interpretation of
the volume of the air tank depends on the patient’s ability         data, revising manuscript.
to aspirate and retain air in the oesophagus and stomach.
These results could explain why patients with TES may               Ethical consideration
have a greater chance of perceiving odorous substances in           The study was approved by Ethics Committee Area Centro
a retronasal way, because a greater quantity of air at higher       Regione Calabria -6/6/22-.
pressure arrives compared to patients with ES. Thus, the            All the patients were informed of the purpose of the study
cells of the olfactory epithelium could be subjected to             before they gave written informed consent. This study was
greater stimulation, which would allow them to reduce the           conducted ethically, with all study procedures being per-
degenerative phenomena of the neuroepithelium 12.                   formed in accordance with the requirements of the World
Loss of laryngeal and nasal functions negatively affect the         Medical Association’s Declaration of Helsinki.
quality of life of these patients 10,25. Over the years, special-   Demographic and clinical data were collected.
ists have placed much effort into rehabilitating patients for
speech, breathing and smell, which are important functions          References
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     s2179-64912011000100017                                                        (Pozn) 2019;23:141-145. https://doi.org/10.5114/wo.2019.86688




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