Changes in the Scandinavian Odor-Identification Test (SOIT) categories in nonsmellers (A) and smellers (B) during the 6-week Nasal Airflow–Inducing Maneuver (NAIM) intervention. Category 1, anosmia (SOIT score, ≤7); category 2, hyposmia (SOIT score, 8-10); category 3, normosmia (SOIT score, 11-16).
Birgit Risberg-Berlin, Riitta Ylitalo, Caterina Finizia. Screening and Rehabilitation of Olfaction After Total Laryngectomy in Swedish PatientsResults From an Intervention Study Using the Nasal Airflow–Inducing Maneuver. Arch Otolaryngol Head Neck Surg. 2006;132(3):301–306. doi:10.1001/archotol.132.3.301
To examine the olfactory function in patients with laryngectomy and to assess the results of the Nasal Airflow–Inducing Maneuver (NAIM) odor-rehabilitation technique.
A prospective intervention study.
Twenty-four patients, 21 men and 3 women, mean age 68 years, who underwent laryngectomy at least 5 months prior to intervention.
Speech therapists trained patients in the NAIM technique: simultaneous lowering of the jaw, floor of the mouth, tongue, base of the tongue, and soft palate while the lips are closed. Three interventions were given within 6 weeks.
Main Outcome Measure
Olfactory testing with semistructured interview, the Questionnaire on Olfaction, Taste, and Appetite (QOTA), and the Scandinavian Odor-Identification Test (SOIT). Quality of life was measured with European Organization for Research and Treatment of Cancer QLQ-C30 and QLQ-H&N35 questionnaires. The patients were categorized as smellers or nonsmellers based on the SOIT results.
Before the treatment, 10 patients (42%) were smellers (ie, 6 had normosmia and 4 hyposmia), while 14 patients (58%) were nonsmellers (ie, all had anosmia). Thus, 18 patients had impaired olfaction. Using the NAIM technique, 13 (72%) of 18 patients with impaired olfaction showed improvement. Of the 14 nonsmellers, 7 converted to smellers after only 1 intervention session, giving us a success rate of 50% in anosmic patients after 1 session.
Olfactory impairment is common in patients who underwent laryngectomy. The NAIM method is easy to learn and rapidly improves smell and taste. A single intervention session is sometimes sufficient, but many patients benefit from repeated training. The SOIT test is an effective and simple test for the assessment of olfaction acuity after laryngectomy.
Total laryngectomy results in a permanent disconnection of the upper and lower airways with a wide range of adverse effects. This change in anatomy leads to deterioration in pulmonary function as well as loss of the normal senses of smell and taste, loss of voice, and associated physical and psychosocial problems. As the normal passive nasal airflow and thereby the odor stimulation to the olfactory epithelium will be lacking, the patient's ability to smell will severely deteriorate.1 This may have serious consequences to daily life, as the patients are unable to detect spoiled food, smoke, or leaking gas. Moreover, since most so-called tastes (eg, chocolate, coffee, tea, meat, and others) are dependent on retronasal stimulation of the olfactory receptors, the perception of such tastes will also be negatively influenced.2- 4 It is evident that these adverse effects on taste and smell have an impact on patients' quality of life.2,3,5,6
Until now, the fact that most people who undergo laryngectomy experience a deterioration of olfaction has not received much clinical attention.1,5 Some patients have tried to improve smell by using a so-called larynx bypass, in which airflow from the stoma is directed to the mouth, creating an artificial airflow into the nose. However, this method is troublesome and impractical for use in every day life.7 Other techniques (eg, the glossopharyngeal press) have also been described but have not been incorporated into routine rehabilitation methods, nor has their effectiveness been systematically evaluated.8 Recently a patient-friendly method that can restore the sense of smell (and taste) in patients who had undergone laryngectomy has been developed by Hilgers and his coworkers.4 This olfaction rehabilitation technique, Nasal Airflow–Inducing Maneuver (NAIM) or “polite yawning technique” works by creating a negative pressure in the oral cavity and oropharynx to induce nasal airflow, thus enabling odorous substances to reach olfactory epithelium. Patients are instructed to make an extended yawning movement while keeping their lips closed and simultaneously lowering their jaw, floor of the mouth, tongue, base of the tongue, and soft palate. According to the authors, the technique is easily mastered by the patient but has to be repeated rapidly to increase its effectiveness. An intervention study performed on 33 patients with laryngectomy categorized as “nonsmellers” showed a success rate of 46% after only one 30-minute training session, while long-term rehabilitation effect was achieved in approximately 50% of the patients.4,9
Several methods are available to measure olfaction. The odor detection test used in the original study on NAIM technique consists of 16 trials with 2 bottles, 1 containing an odorless solvent and the other a floral trigeminal odor in progressively lower concentrations.1 The Smell Disk Test10 is an identification test in which the tested person has to identify 8 different smells (coffee, vanilla, smoke, peach, pineapple, rose, coconut, and vinegar). This test has been validated, and the results have been compared with the Sniffin’ Sticks, another European odor-identification test.10,11 The recently published Scandinavian Odor-Identification Test (SOIT), including 16 different stimuli with 4 response alternatives, was chosen for our study because it has shown satisfactory validity and reliability and includes odors that are easy to identify for Scandinavian people.12,13
The aim of the present study was to examine the olfactory function in Swedish patients who had undergone total laryngectomy. We also wanted to prospectively assess the results of repeated interventions with the odor-rehabilitation NAIM.
All the patients lived in the western part of Sweden. They had undergone total laryngectomy at least 5 months earlier and were contacted by the speech language pathologist (SLP) and asked to participate in the study. Thirty-five patients were identified, and 24 patients were included in the study. The criterion for inclusion was that the patients' mental and physical condition was good enough to complete the intervention. Eleven patients did not participate owing to poor general health (n = 6); lack of motivation (n = 3); and residing outside of our catchment area at the time of this study (n = 2).
The study was conducted in accordance with the Declaration of Helsinki and was approved by the ethical committee at the Sahlgrenska University Hospital, Göteborg, Sweden.
During the first session, all patients underwent a flexible nasal endoscopy to detect any anatomic abnormalities that could prevent nasal airflow. Furthermore, anatomic and neurologic deficits possibly interfering with lip closure, intraoral and extraoral mobility, or swallowing were evaluated. To test for possible anosmia, an odorous substance well known to the patient was applied in front of the nose while nasal airflow was induced by means of a larynx bypass. To learn whether the patient used a personal technique to smell, the SLP observed the patients carefully before intervention and videotaped the odor testing. The result was then noted on the study form. In addition, the patients were videotaped during each treatment session, and the recordings were then used for biofeedback. The results of these recordings are reported separately.
The objective of the NAIM is to induce nasal airflow by creating negative pressure in the oral cavity and oropharynx. This is attained by lowering of the jaw, floor of the mouth, tongue, base of the tongue, and soft palate while the lips are closed (an extended polite yawning movement).4,9 Three intervention sessions were performed during a 6-week period. Two SLPs were involved at each session; one was responsible for the testing and teaching of the NAIM technique, while the other was responsible for observation and video documentation. A water manometer was used for real-time visual feedback during practice in the clinic as well as at home. For memorizing the technique, the patient received a written program with instructions on the NAIM and how the water should move in the manometer when the maneuver was performed correctly. The patients were instructed to actively use the maneuver as often as possible between interventions and to try to integrate the technique into daily life situations.
A semistructured interview was conducted by the SLP at the first study visit and included questions on olfaction and taste before the laryngectomy and at the time of the interview. Calculated scale scores ranged from 0 to 100, where 0 corresponds with “very bad” and 100 with “very good.” In addition, patients were asked whether they used a special method to smell in their daily life, and if so to describe it.
Olfactory acuity was tested with the SOIT before treatment and at each intervention session. The SOIT has demonstrated satisfactory reliability and validity in previous testing.12 The test involves 16 different odors (pine needle, peppermint, juniper, violet, anise, clove, vanilla, bitter almond, orange, cinnamon, lemon, lilac, vinegar, tar, ammonia, and apple) and 4 alternative responses per odor to choose from. Three of the odors—peppermint, vinegar, and ammonia—are trigeminal stimulants. The smell is generated by 5 mL of odor stimulus placed in a 10-mL glass jar. The test has age- and sex-related cut-off scores and categorizes the sense of smell into 3 diagnoses: normosmia, hyposmia, or anosmia. The cut-off scores used in this study (for age groups 55-74 years) were 11 to 16 for normosmia, 8 to 10 for hyposmia, and 7 or lower for anosmia. Thus, 3 different categories are given: 1, anosmia; 2, hyposmia; and 3, normosmia.
On the basis of performance on the SOIT, patients were categorized as smellers or nonsmellers. Smellers are patients diagnosed with functional hyposmia or normosmia, and nonsmellers are patients with anosmia, according to SOIT scores.
The Questionnaire on Olfaction, Taste, and Appetite (QOTA) was derived from research by de Jong et al,14 who studied olfaction and gustation in elderly people, and has shown satisfactory validity and reliability. The QOTA has further been used in the studies of olfaction in patients who had undergone laryngectomy at the Netherlands Cancer Institute in Amsterdam.1,5 The QOTA consists of several multiple-choice questions addressing both the prelaryngectomy period and the present situation. Questions were divided into 5 scales: (1) subjective feelings of present smell or odor perception (POPS, 3 items); (2) appetite (6 items); (3) subjective feelings of present taste perception (8 items); (4) present smell perception compared with past (3 items); and (5) daily feelings of hunger (9 items). A low score indicates bad function or that these items have deteriorated compared with the preoperative situation. Conversely, a high score indicates good function or improvement in these attributes. The authors of the questionnaire have given us permission to translate and use the questionnaire in our studies. The QOTA questionnaire was translated into Swedish using a formal method of forward-backward translation by 2 independent bilingual translators. The wording of some of the items in the final QOTA version was slightly modified to aid in better comprehension in Swedish. This version was then pretested in 22 patients with laryngectomy (unpublished data, March 2002).
The European Organization for Research and Treatment of Cancer (EORTC) study group on quality of life has developed a modular measurement system for evaluating the quality of life in patients with cancer participating in clinical trials. We used the 30-item core questionnaire, the EORTC QLQ-C30, to assess patients' general physical and psychosocial functioning and symptoms.15,16 To address additional symptoms associated specifically with head and neck cancer and its treatment, we used the complementary 35-item questionnaire module, the QLQ-H&N35.17
When tested in large, cross-cultural samples of patients with cancer, both the QLQ-C3015 and the QLQ-H&N3518 have demonstrated satisfactory to excellent reliability and validity. Of particular importance is the ability of these questionnaires to distinguish between patient groups differing in clinical status and to detect changes in patients' clinical status over time. Calculated scores range from 0 to 100, where 100 corresponds to maximum functioning (functioning scales and global quality of life) or worst symptoms (symptom scales and items).19 In general, score differences over time of at least 10 points could be interpreted as indicating clinically important changes.20
The study protocol was conducted in the following order: semistructured interview, QOTA administration, olfactory testing by larynx bypass, and EORTC and SOIT administration. The intervention outcome was then measured with patients' self-estimation of smell and taste and QOTA, EORTC, and SOIT scores.
The Pearson correlation coefficient was calculated for descriptive purposes. For comparison between groups, the Fisher nonparametric permutation test was used. In addition, changes over time were analyzed with Fisher nonparametric permutation tests for matched pairs. All tests were 2-tailed and conducted at a 5% significance level.
Twenty-four patients, 21 men and 3 women, were included in the study group. Eleven patients did not participate owing to the previously mentioned criteria. The sociodemographic and clinical data for the 2 patient groups are summarized in Table 1. All patients reported having normal olfaction, taste, and appetite before the laryngectomy. There were no significant differences between the nonparticipating patients and the study patients concerning sex, age, smell, or taste according to the QOTA questionnaire, or quality of life according to the EORTC questionnaires. However, the nonparticipating patients estimated their own present olfactory function as well as their own olfaction and gustation before laryngectomy to be significantly better than the study group estimated their own function to be (P<.01 and P<.05, respectively) (Table 2). The nasal endoscopy showed no abnormalities in any patient, and none of the patients had anatomic or neurologic deficits. The larynx bypass investigation revealed that 5 patients were not able to smell with the device.
Before treatment, 10 patients (42%) were smellers, ie, categorized as having normosmia (n = 6) or functional hyposmia (n = 4) according to SOIT, while 14 patients (58%) were nonsmellers, ie, had anosmia. Consequently, 18 patients had the possibility of improvement after intervention with the NAIM technique (ie, patients having anosmia or functional hyposmia at baseline). The results at baseline (before intervention) for the 2 groups, smellers and nonsmellers, are summarized in Table 3. The 2 groups did not differ significantly from each other concerning their own estimation of smell or taste, QOTA results on smell, taste or appetite, or quality of life.
Of the 18 patients with impaired olfactory function, 13 (72%) experienced improvement after this intervention study. Of the 14 nonsmellers, 7 converted to smellers (6 to hyposmia and 1 to normosmia) after only 1 intervention session, resulting in a success rate of 50% in anosmic patients after 1 session. Of the remaining 7 nonsmellers, 3 converted to smellers after repeated sessions, while 4 nonsmellers did not get better after the treatment. Moreover, of the 4 patients with functional hyposmia, 3 (75%) converted to normosmia after 1, 2, and 3 interventions, respectively. Thus, 1 patient with hyposmia did not improve after the treatment (Figure). Of those 5 patients who were not able to smell with larynx bypass, 2 were categorized as smellers after the study. The changes from pretreatment to posttreatment evaluation are summarized in Table 4.
After the intervention, the nonsmellers' own estimations of their olfaction and gustation were significantly higher than they were before the treatment. Although not significant, the nonsmellers showed an improvement according to the smell item on QLQ-H&N35 (a change of −9.5), where score differences over time of at least 10 score points could be interpreted as indicating changes of clinical importance. In addition, the smeller group had significantly better sense of smell based on their own estimation, and significantly better appetite and taste according to QOTA (Table 4).
There were 3 major findings in this study. First, 75% of the patients who had undergone laryngectomy had impaired olfaction (n = 18), and more than 50% had anosmia (n = 14). Second, after undergoing training in the NAIM technique, 72% of the patients with anosmia and hyposmia (n = 13) improved their olfactory capacity. Finally, even the patients with preintervention normosmia experienced improved olfactory capacity after using the NAIM technique.
There are few recent studies about olfactory function in patients who had undergone laryngectomy, most of which show a deterioration of olfactory capacity in this group. Welge-Luessen et al21 reported a prevalence of 28% for hyposmia and 72% for anosmia, while van Dam et al1 found that 75% of the patients with laryngectomy had anosmia. One prospective study from Japan showed that even if olfactory function was diminished 3 months postoperatively, olfaction was normalized to preoperative levels within 1 year.22 However, in the Communication by Fujii et al,22 the methods to study olfaction differed substantially from traditional olfactory tests: 3 odorants were sprayed directly into the nasal cavity and 1 was injected intravenously. Our results suggest that when diagnosis of olfactory dysfunction is based on SOIT outcome, a considerable olfactory dysfunction is present among patients who had undergone laryngectomy even years after the procedure.
Hilgers et al,4 who introduced the NAIM technique, reported that almost half of the nonsmellers converted to smellers after only 1 intervention session. These results are in concordance with the outcome after the first session in our study. Despite promising results, Hilgers et al discuss further improvement of the olfactory rehabilitation by means of more interventions per patient. Consequently, we extended our rehabilitation program to include 3 sessions within 6 weeks, which obviously is advantageous: progress was noticed even between the second and third intervention sessions. As with other aspects of postlaryngectomy rehabilitation (eg, voice and pulmonary status), olfactory rehabilitation might benefit from early and repeated training.9 Repeated, intensified training will encourage the patient to implement the new technique in everyday life and will aid in making it a habit, which is crucial for positive results in the long term. The data in our study suggest that at least 3 treatment sessions should be recommended. Long-term results of this technique will be reported in a future article.
Another key issue is to determine for which patients olfactory rehabilitation is appropriate treatment. In the present study, patients categorized as smellers at baseline experienced an improvement in olfaction after intervention and had better appetite and taste based on QOTA. Their changes were not as prominent as among the nonsmellers, and this might partly be a placebo effect since the study is focused on olfaction; but the changes were measurable with validated tests. In addition, 2 of the 5 patients who were not able to smell with the larynx bypass were able to smell with the NAIM technique and were categorized as smellers after the study. Hence, the results from laryngeal bypass cannot predict whether a patient will benefit from olfactory rehabilitation. Based on our own experience, the NAIM technique is an easy-to-learn and inexpensive and effective method to improve olfaction and should therefore be included in all rehabilitation programs for patients with laryngectomy.
Our results cannot directly be compared with those from Hilgers et al4 because different olfactory tests were used to categorize the patients as smellers and nonsmellers. As the odor detection test used by Hilger et al probably was a relatively insensitive test for this type of study, they later used the Smell Disk Test,10 which discriminates between nonsmellers and nonsmellers in a more simplified way. However, the limitation of the Smell Disk Test may be that a typical Scandinavian person is unable to easily identify odors such as coconut or pineapple. Thus, we chose the SOIT odor differentiation test, a validated Swedish test that also gives age- and sex-dependent cut-off scores for the olfactory diagnoses normosmia, functional hyposmia, and anosmia.12,13 This test was easy to perform in the patients who had undergone laryngectomy and provided a useful way of tracking olfaction results over time.
While we managed to contact all the patients who had undergone laryngectomy living in our catchment area, the size of this cohort is relatively small. Nonparticipating patients did not undergo objective olfactory testing but reported subjectively better smell and taste than those included in this study. Thus, it might be that the prevalence of olfactory impairment in the total population of patients who had undergone laryngectomy is somewhat lower than our data indicated. Otherwise, this study population appears to be representative, since the study patients and the nonparticipating group did not differ significantly from each other. However, a limitation of the cohort size is that it does not allow for reliable comparison of the olfactory capacity between men and women or for comparison between those who received olfactory rehabilitation shortly after laryngectomy and those receiving it years later.
In conclusion, olfactory impairment is common in patients who have undergone laryngectomy. The NAIM rehabilitation method is easy to learn and rapidly improves the capacity to smell and taste. A single intervention session is sometimes sufficient, but many patients benefit from repeated training. We recommend that olfactory and gustatory rehabilitation be incorporated into routine rehabilitation program for patients with laryngectomy.
Correspondence: Caterina Finizia, MD, PhD, Department of Otolaryngology, Sahlgrenska University Hospital Mölndal, SE-431 80 Mölndal, Sweden (email@example.com).
Submitted for Publication: March 21, 2005; final revision received August 25, 2005; accepted November 9, 2005.
Financial Disclosure: None.
Funding/Support: This study was supported by the Assar Gabrielsson Foundation, Göteborg, Sweden, the Laryng Foundation, Stockholm, Sweden, the Research and Development Council (FoU), Västra Götaland County, Sweden, and the Medical Faculty of Göteborg University. ENTpro AB Medical Company, Stockholm, Sweden, provided the silicon nose adapters for the manometers used in the study.
Acknowledgment: We are indebted to the following speech language pathologists in Västra Götaland and Halland counties, Sweden: Inga Eliasson, SPL, Claes Österlind, SPL, Ulla-Britt Tengstrand, SPL, Kerstin Hofling, SPL, Ann-Christin Ohlsson, SPL, and Ingrid Fridén, SPL, for their excellent assistance with examination of the patients, and Carina Åberg, RN, for assistance with collection of data at Sahlgrenska University Hospital. We also thank Frans Hilgers, MD, PhD, and Corina van Aas, SPL, PhD, for teaching us all there is to know about the NAIM technique.