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Long-term Results of Olfaction Rehabilitation Using the Nasal Airflow–Inducing ("Polite Yawning") Maneuver After Total Laryngectomy
Frans J. M. Hilgers, MD, PhD;
Helma A. Jansen, MSc;
Corina J. van As, PhD;
Marianne F. Polak;
Martin J. Muller, MSc;
Frits S. A. M. van Dam, PhD
Arch Otolaryngol Head Neck Surg. 2002;128:648-654.
ABSTRACT
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Objectives To study the long-term results of the nasal airflow–inducing maneuver
(NAIM) as an olfaction rehabilitation tool after laryngectomy and to investigate
the effectiveness of a new, simpler odor detection test (ODT) called the smell
disk test (SDT), or Zürcher Geruchstest.
Design Intervention study.
Settings National cancer center.
Patients Forty-one laryngectomees who received olfaction rehabilitation training
with the NAIM 4 months to 2 years earlier. This so-called polite yawning maneuver
creates an "underpressure" in the oral cavity, which, in turn, generates a
nasal airflow that enables odor molecules to again reach the olfactory epithelium.
Main Outcome Measures Olfaction acuity testing with a standard ODT, along with a questionnaire,
providing a subjective olfaction score (present odor perception scale [POPS]),
and the SDT, as well as assessment of the patients' correct execution of the
NAIM by speech-language pathologists on video recordings made during odor
testing and long-term assessment of olfaction acuity.
Results The correlation between the previously used ODT-POPS combination and
the SDT was  = 0.56 (P<.001). Based on
these results, we preferred to use the much simpler SDT instead of the laborious
combination of the ODT-POPS. Based on the SDT results, 19 (46%) of the 41
laryngectomees were "smellers" and could be considered normosmic. There was
a significant relationship (P = .03) between the
patient's correct execution of the NAIM and whether or not the laryngectomee
was a smeller according to the SDT.
Conclusions The effectiveness of the NAIM, or so-called polite yawning technique,
for the rehabilitation of olfaction in individuals who have undergone total
laryngectomy was reconfirmed. Long-term olfaction rehabilitation was achieved
in about 50% of the patients, but more intensified training may be needed
to increase the percentage of successfully rehabilitated individuals. The
SDT is an effective and simple test for the assessment of olfaction acuity
after laryngectomy.
INTRODUCTION
TOTAL LARYNGECTOMY has a wide range of adverse effects, mainly as a
result of the permanent disconnection of the upper and lower airways. Not
only is the natural voice lost, but other physiological systems, which require
a more or less normal nasal airflow, are disrupted and/or hampered as well.
This change in anatomy often leads to deterioration in pulmonary function,
with an associated range of physical and psychosocial problems, and a loss
(or at least a serious decrease) of the sense of smell and taste.1-2
Olfaction is either a passive process that occurs during normal nasal
breathing (so-called passive smelling) or an active process (so-called active-smelling
or sniffing). Total laryngectomy inevitably results in the loss of passive
smelling, and only a minority of patients are still able to actively smell
anything. In a recent study of 63 laryngectomees, we found that about two
thirds of the patients were anosmic and that the rest had difficulty in smelling.3 Several techniques have been described that might
generate an airflow in the nose and thereby restore olfactory function.4-7 However,
these techniques have not been incorporated into routine rehabilitation methods,
and their effectiveness has not yet been evaluated either.
Recently, we developed a technique that makes use of a simple physical
mechanism by creating an "underpressure" in the oral cavity, which then generates
a flow of air through the nose.8 Patients are
instructed to make an extended yawning movement while keeping their lips securely
closed and simultaneously lowering their jaw, floor of the mouth, tongue,
base of the tongue, and soft palate. The underpressure thus created in the
oral cavity results in an airflow through the nose. This technique, which
is easily mastered by the patient, is taught by explaining that this movement
resembles what one does when yawning with the mouth closed, ie, so-called
polite yawning. This polite yawning maneuver has to be repeated rapidly to
increase its effectiveness. In an intervention study, we were able to show
that after only one 30-minute training session, 25 (57%) of the 44 laryngectomees
were able to smell using this technique.8
Although this polite yawning technique is potentially an important adjunct
to the rehabilitation process, no data are available on the long-term use
of this technique; eg, do patients continue to apply this method after some
months or years and do they apply it in daily life? Therefore, a follow-up
study was conducted to study long-term results. Also, because our original
studies used complicated techniques to assess olfactory function,3, 8 in the present study we also assessed
whether a new simple odor detection test (ODT) could replace our previous
method of odor testing.
PATIENTS AND METHODS
PATIENT SELECTION AND SOCIODEMOGRAPHIC DATA
Thirty-five patients who were trained with the nasal airflow–inducing
maneuver (NAIM) about 1 to 2 years earlier were available for this
study. Four patients declined to participate (1 "smeller" and 3 "nonsmellers").
The study population was augmented with 10 patients who had recently undergone
laryngectomy, and at least 4 months had to have past since their operation
or postoperative radiotherapy. None of this latter group had participated
in the original intervention study, and during their speech rehabilitation
program they were taught how to use the NAIM. Finally, the study population
consisted of 31 men (76%) and 10 women (24%); the mean age was 63 years, with
a range of 43 to 81 years; and the time since total laryngectomy ranged from
4 months to 20 years, with a mean of 6.5 years (Table 1). All patients underwent an otorhinolaryngological examination
to rule out nasal obstruction. If anosmia was suspected, a well-known odorous
substance was applied in the nose, while a nasal airflow was induced by means
of a larynx bypass.6, 9 The medical-ethical
protocol institutional review board approved the study, and all patients gave
their informed consent.
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Table 1. Characteristics of the Study Population*
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OLFACTION REHABILITATION
The NAIM is intended to restore a nasal airflow by creating an underpressure
in the oral cavity and oropharynx,8 which in
brief is achieved by having the patient make an extended yawning movement
while keeping the lips securely closed and simultaneous lowering the jaw,
floor of the mouth, tongue, base of the tongue, and soft palate (which is
best explained to the patient as a polite yawning movement). This movement
has to be repeated rapidly several times to increase its effectiveness. The
NAIM is schematically shown in Figure 1.
The initial instruction and training of this maneuver by the speech-language
pathologist (SLP) takes approximately 30 minutes for most patients. During
the training session, a simple water manometer is used to visualize the nasal
airflow (Figure 2). A movement of
the water column toward the nasal vestibule gives the SLP and the patient
real-time visual feedback as to whether the maneuver is being executed correctly.
Furthermore, odors well known to most patients, such as vanilla, flowers,
mint, and anise, are used to support the training.
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Figure 1. A, Schematic drawing before use
of the nasal airflow–inducing maneuver. B, Schematic drawing of the
nasal airflow–inducing maneuver, during which a volume increase in the
oral cavity and oropharynx is created by lowering the jaw, floor of the mouth,
tongue, base of the tongue, and soft palate with the lips securely closed.
In this way, an "underpressure" is induced and a nasal airflow is generated,
allowing odorous molecules to again reach the olfactory epithelium.
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Figure 2. Simple water manometer shows the
movement of a column of air toward the nose during the nasal airflow–inducing
maneuver, providing the patient and the speech-language pathologist with real-time
visual feedback about the correct execution of the maneuver.
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OLFACTION ACUITY TESTING
In brief, the ODT10 (the standard test
used in our previous study3) consists of 16
trials with 2 coded 250-mL bottles, one containing the odorless solvent dipropylene
glycol and the other containing dipropylene glycol with phenylethyl alcohol,
a liquid with a floral nontrigeminal odor. The concentration of phenylethyl
alcohol is lowered stepwise with 0.5 log (from -1 to -4.5 log
vol/vol). Each concentration is offered twice, resulting in a maximum of 16
trials. If patients were unable to smell something in the first 2 trials,
2 additional trials with the same and strongest concentration were added.
Patients had to indicate which bottle contained the floral scent. Progressively
lower concentrations were applied to prevent fatigue and olfactory saturation.
To prevent olfactory saturation, the interval between applications of the
2 samples was at least 45 seconds. The ODT was ended when the patient indicated
that in 2 successive trials no odor was detected or when 4 successive trials
were judged incorrect. The ODT result was considered positive if at least
the 2 first trials with the highest concentration of phenylethyl alcohol were
correctly indicated. If only the first 2 trials were correct, the 2 additional
trials with the same concentration had to be correct as well. All other test
results were considered incorrect. This test can be demanding for a laryngectomee
to accomplish and generally takes up to 30 minutes to be completed.
The smell disk test (SDT), or Zürcher Geruchstest, was recently developed as a rapid screening test for hyposmia and
anosmia.11-12 This ODT (Novimed
Medizin Technik, Dietikon, Switzerland) consists of 8 different odors (coffee,
vanilla, smoke, peach, pineapple, rose, coconut, and vinegar) that have to
be identified correctly by the patient. The patient receives a multiple-choice
list with 3 options per odor, from which the correct one has to be identified
(Figure 3). The odors are contained
within special cassettes, which can be opened by the test person, setting
a surplus (well above the normal olfaction threshold) of the scent free. According
to the original description of the SDT, there is a normal sense of smell if
the test person identifies 7 or 8 of the odors correctly. In all other cases,
the test person is either hyposmic or anosmic. The likelihood that an anosmic
individual by chance scores 7 or 8 odors correctly is only 0.26%.11-12 The SDT can be easily performed by
a laryngectomee and generally takes only a few minutes to complete. The much
weaker smelling ODT was always conducted well in advance of the much stronger
smelling SDT; moreover, care was taken to bring the latter test into the room
only immediately before testing in order to prevent saturating the room with
strong-smelling scents.
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Figure 3. The smell disk test, or Zürcher Geruchstest, during which the patient identifies
the different scents. A total score of 7 or 8 correctly identified odors indicates
a normal sense of smell (from Simmen et al11
and Briner and Simmen12).
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Each patient's subjective experience was assessed with a smell-and-taste
questionnaire consisting of 31 questions.13
Each question has 5 answer categories from which the patient has to choose.
For the present study, we report only on the present odor perception scale
(POPS), which consists of 3 questions that indicate how well the patient thinks
he or she can smell. Patients are considered to have a normal olfaction acuity
if the POPS score (range, 3-15) is equal to or better than 10.8
We compared the combination of the ODT and the POPS3, 8
(which was used in our previous study as the criterion for the ability to
smell) with the SDT.11 If the SDT proved to
yield similar results to the ODT-POPS combination, then clinicians would have
a user-friendlier test at hand to assess the laryngectomee's ability to smell.
Finally, patients were interviewed about the use of the NAIM in everyday life.
VIDEO ASSESSMENT OF THE NAIM
During the ODT, a video recording was made of the patient and later
judged by 2 SLPs who independently filled in a checklist on which the constituent
parts of the NAIM were itemized. Furthermore, the number of times the NAIM
was performed within a certain time frame was counted. Finally, the SLPs gave
an overall judgment on the quality of the patient's execution of the NAIM
as a whole (poor, insufficient, sufficient, good).
STATISTICAL ANALYSIS
All analyses were performed with SPSS 9.0 statistical software (SPSS
Inc, Chicago, Ill) and a t test for independent samples
was used to test for possible differences in POPS scores between smellers
and nonsmellers. Logistic regression analysis was used to test whether sociodemographic
and clinical data were associated with olfaction acuity and the use of the
NAIM. Cohen statistics were calculated for the interobserver reliability
for the independent judgments of the video recording of the NAIM and for the
concordance between the results of the ODT-POPS and the SDT. All other relationships
were tested with a  2 test.
RESULTS
OLFACTION ACUITY TESTING
Results of the 3 odor tests are given in Table 2. When the criteria of the former study (positive ODT results
and/or POPS score  10) were applied to the present study, 19 (46%) of the
41 patients were categorized as smellers (compared with 57% of the patients
in our previous study). On the SDT, 19 patients (46%) identified 7 or 8 odors
correctly (mean [SD] score, 5.7 [2.3]) and thus met the criteria for a normal
sense of smell.
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Table 2. Results of the 3 Olfaction Tests*
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The correlation between the cutoff score of the ODT-POPS combination
for smell and the cutoff score of 7 or more for smellers on the SDT is given
in Table 3. The correlation between
the combination of ODT-POPS (previously used by us to assess olfactory sensitivity)
and the SDT was 0.56 (Cohen ; P <.001),
with 32 patients being classified as smellers or nonsmellers on both tests.
Three patients who had negative results according to the previous criteria
had positive results on the SDT, and 6 who had positive results according
to the previous criteria had negative results on the SDT. Based on these findings,
we decided to use the easier applied and user-friendlier SDT to classify patients
into smellers (normosmia) or nonsmellers (hyposmia or anosmia) in the present
study.
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Table 3. Comparison Between the ODT-POPS Combination and the SDT*
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USE OF THE NAIM
Twenty patients (49%) reported that they used the NAIM in daily life:
7 (17%) on a daily basis; 6 (15%) less frequently, but regularly; 5 (12%)
sometimes; and 2 (5%) only occasionally. The majority of the patients reported
that they applied the maneuver only if they expected to smell something. Only
2 patients made this maneuver into an "automatism," ie, whenever there was
a change in their environment (eg, entering a room or meeting another person).
Among the patients who no longer used the NAIM (51%), the reasons given included
"smell is not important to me" (n = 2), "forgot how to perform it" (n = 5),
"too obvious a movement" (n = 4), "technique is not effective" (n = 5), and
"my smell is good without it" (n = 5); not one patient reported thinking that
the maneuver was too difficult to perform.
Assessment of the execution of the NAIM (based on video recording) was
performed in 40 of the 41 patients: 1 patient was tested at home, where no
video equipment was available. The items judged are shown in Table 4; there was good interrater agreement between the 2 SLPs
(Cohen , 0.73).
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Table 4. Data on the Different Subaspects of the NAIM Judged by the
SLPs to Have Been Correctly and Incorrectly Executed*
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The results of the overall judgment of the NAIM were dichotomized as
negative (poor or insufficient) and positive (sufficient or good). Sixteen
patients (40%) received an overall positive judgment and 24 (60%) a negative
judgment for their execution of the NAIM. We analyzed whether the smellers
could be discriminated from the nonsmellers with regard to their performance
of the NAIM. The judgments for the different subaspects of the NAIM are given
in Table 5. It can be seen that
there is a significant relationship between correct execution of the NAIM
and the ability to smell (P = .03). The 6 patients
who were judged to execute the NAIM incorrectly but who were nevertheless
smellers according to the SDT received a negative judgment because of simultaneous
deep inhalation during the maneuver. Although they could smell, the inhalation
was considered unfavorable because it might cause hyperventilation. The 5
patients who were judged to execute the NAIM correctly but who were nevertheless
nonsmellers according to the SDT might have failed to create an airflow (movement
of the water column in the water manometer would have confirmed or denied
this). Furthermore, the number of repetitions of the maneuver was significantly
higher in the smellers (mean number of repetitive movements, 19 times in 15
seconds in the smeller group vs 3 times in the nonsmeller group; P<.001).
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Table 5. Relationship Between Correctness of NAIM Execution and Whether
the Patient Is a "Smeller" or a "Nonsmeller"*
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Logistic regression analysis showed no relationship between the ability
to smell and any of the sociodemographic variables studied (age, sex, level
of education, vocal rehabilitation method, oral denture status, and time since
laryngectomy; data not shown).
COMMENT
The correlation between the ODT-POPS combination and the SDT seems sufficient
to justify our decision to replace this laborious combination (used in our
previous study) with the much simpler SDT. The results with the combination
are slightly better (54% vs 46%), however, which could mean that the threshold
for being classified as a smeller might be somewhat lower with the combination
ODT-POPS than with the SDT. This outcome might be attributable to the strict
criterion of separating normosmia on the one hand from hyposmia/anosmia on
the other. The SDT has a proven validity and reliability,11-12
and for routine clinical practice the use of a single objective measure has
clear advantages. Similar results were recently reported using the Sniffin'
Sticks odor test in a series of laryngectomees.14
This latter test, however, consists of more odors and uses different concentrations
and is therefore much more time consuming. The simple SDT requires only a
few minutes to be completed.
The main aim of the study was to establish whether a single training
session in the past had a permanent effect on the use of the NAIM in daily
life. The majority of the patients who participated in the original intervention
study also took part in the present study (31 [63%] of 49 patients). Because
only 4 patients refused to participate (one of them being a smeller), selection
bias concerning the long-term results is probably minor.
It is remarkable that the percentage of smellers in this follow-up study
is very similar to that found in the earlier intervention study (54% vs 57%,
respectively).8 The effectiveness of the NAIM
could be confirmed: there is a relationship between the correct execution
of the NAIM, as judged on the video recording, and whether the laryngectomee
was a smeller or a nonsmeller. However, the small number of patients (16)
who are still performing the NAIM correctly indicates that a single training
session may be insufficient to achieve effective long-term results. On the
other hand, 2 patients made use of the NAIM an automatism whenever something
in the environment urged them to do so. In this way, they compensated for
the loss of passive smelling, which is a "bonus" of normal nasal breathing
and an important aspect of natural olfaction. As with other speech-language
pathology problems, behavioral changes are difficult to achieve and repetition
of the training is often a key to success. More intense training, focusing
on the important movements (lowering of the floor of the mouth and the jaw
while simultaneously avoiding breathing in) and the fast repetition of the
NAIM is needed to restore olfaction in a higher percentage of patients and
to make the NAIM into an automatism that may allow passive smelling to occur
again. Two other aims are to perform the maneuver as discreetly as possible
by trying to lower only the floor of the mouth and to reduce the movement
of the jaw. This attempt to make the NAIM more inconspicuous is relevant,
because one of the reasons reported by patients for no longer using the maneuver
was that it was too noticeable.
Whether the patency of the nose and the volume of air that can be moved
with the polite yawning maneuver have an influence on olfaction acuity is
a question that cannot be answered by the findings of the present study. Although
none of our patients had overt nasal obstruction, which was more or less ruled
out by nasal endoscopy, it remains unclear whether improvement of nasal patency
would have a beneficial effect on the olfactory end result, as recently has
been suggested.15 Along with studies on the
volume of air that can be moved with the NAIM, rhinometry could maybe provide
more insight in this respect.16
Some of the older literature suggests that there is a positive correlation
between the quality of the esophageal voice and the olfaction acuity of the
patient.17-18 We were not able
to evaluate this aspect because all but 2 of the patients were using a voice
prosthesis. Nevertheless, the aforementioned relationship might be merely
a result of the better control of the oropharyngeal musculature in good esophageal
speakers, enabling them to "pump" air into the nasal cavity retronasally,
as has been advocated in the past.4 However,
we think that this retronasal route is not very important and that in the
majority of cases the oropharyngeal movements result in an anteronasal flow
of air.
It should also be noted that the SDT criterion of a normal sense of
smell was strictly followed, ie, 7 or 8 of the odors scored correctly.11-12 Some of the patients scored fewer
than 7 odors correctly and could be considered to be to some extent hyposmic
and probably not totally anosmic, which might lead to an underestimation of
the results of the olfaction rehabilitation. However, by applying the cutoff
scores of the SDT, the norms of "normal" smelling can be used to compare the
results of laryngectomees.
Recently, Miwa et al19 reconfirmed the
effects of olfactory impairment on the quality-of-life and level of disability.
Patients reporting persistent olfactory impairment after previously documented
olfactory loss indicate a higher level of disability and a lower quality of
life than those with perceived resolution of olfactory compromise. These observations
are in agreement with our earlier finding that laryngectomees who were able
to smell reported having a better taste and appetite.3
They emphasize the benefits that can be gained from olfaction rehabilitation
in laryngectomees.
CONCLUSIONS
Odor testing in individuals who have undergone a total laryngectomy
is now possible in a relatively simple way using the easily applied SDT. The
NAIM (best explained to the laryngectomee as a polite yawning technique) is
a patient-friendly method that can restore the sense of smell. However, a
single training session is probably insufficient, and most patients may need
more training. This intensified training may then serve to rehabilitate olfaction
in a higher percentage of patients and to make this maneuver an automatism
to compensate for the loss of passive smelling after total laryngectomy. In
view of this reconfirmation that it is possible to restore olfaction in individuals
after total laryngectomy, rehabilitation of the sense of smell should form
an integral part of the multidisciplinary postlaryngectomy rehabilitation
program.
AUTHOR INFORMATION
Accepted for publication October 26, 2001.
We thank Els Groeneveld for preparing the ODTs in her laboratory, and
all of our patients, without whom these studies would not be possible. We
also thank Alfons J. M. Balm, MD, PhD, for his critical review of the manuscript.
Corresponding author: Frans J. M. Hilgers, MD, PhD, Department of
Otolaryngology–Head and Neck Surgery, Netherlands Cancer Institute,
Plesmanlaan 121, 1066 CX Amsterdam, the Netherlands (e-mail: fhilg{at}nki.nl).
From the Departments of Otolaryngology–Head and Neck Surgery
(Drs Hilgers and van As and Ms Polak) and Psychosocial Research and Epidemiology
(Mr Muller and Dr van Dam), Netherlands Cancer Institute, and the Institute
of Psychology, University of Amsterdam (Ms Jansen and Dr van Dam), Amsterdam,
the Netherlands.
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