The Laryngoscope C 2013 The American Laryngological, V
Rhinological and Otological Society, Inc.
The Effect of Obstructive Sleep Apnea on Olfactory Functions lu, MD; Mustafa Tansel Kendirli, MD; Aytug Altundag , MD; Hakan Tekeli, MD; Murat Salihog € lam, MD; Melih C¸ay€on€ , MD Muzaffer Sag u, MD; Mehmet G€ uney S¸enol, MD; Fatih Ozda g Objectives/Hypothesis: The aim of this study was to investigate the effect of obstructive sleep apnea (OSA) on the parameters of olfactory functions (odor threshold, odor discrimination, and odor identification tests) for orthonasal olfaction, retronasal olfactory testing, and olfactory bulb (OB) volumes. Study Design: Prospective clinical study. Methods: This study was carried out in 78 volunteers between the ages of 20 and 60 years. The mean age of the patients was 46 6 10.1 years. Patients were divided into three groups according to polysomnography results: 1) a control group, 2) a mild to moderate OSA group, and 3) a severe OSA group. Clinical features of the participants were evaluated with the Epworth Sleepiness Scale. Orthonasal and retronasal olfactory testing were performed with Sniffin’ Sticks olfactory testing and retronasal olfactory testing, respectively. Olfactory bulb volumes were measured by planimetric manual contouring on magnetic resonance imaging (MRI). Results: The current investigation produced four major findings: 1) The apnea-hypopnea index had a significant and strong negative correlation with odor threshold scores and odor discrimination scores; 2) The apnea-hypopnea index was significantly negatively correlated with odor identification score and both right and left OB volumes; 3) retronasal olfactory scores were not significantly affected by OSA; and 4) continuous O2 saturation had a significant positive correlation on orthonasal olfactory functions, particularly the odor threshold and discrimination scores. Conclusions: This study demonstrated that OSA had significant negative effects on all orthonasal olfactory tasks, especially on threshold and discrimination. MRI also revealed volumetric shrinkage of OB volumes. Key Words: Obstructive sleep apnea, polysomnography, olfaction disorders, Sniffin’ Sticks, olfactory bulb. Level of Evidence: 3b. Laryngoscope, 00:000–000, 2014
INTRODUCTION It is well known that obstructive sleep apnea (OSA) is characterized by breathing cessation (apnea) or reduction of airflow (hypopnea) during sleep, heavy snoring, and daytime sleepiness.1–3 OSA is a disease affecting about 2% to 4% of the adult population and is becoming more commonly recognized because of its significant negative effects, including increased risks of cardiovascular and cerebrovascular mortality and morbidity.4–6 It is also known that OSA is associated with neurocognitive and psychological problems, such as memory and new learning, attention, executive function, and depression.7–10 The Epworth Sleepiness Scale (ESS) is the
From the Department of Otorhinolaryngology (M.SALIHOGLU) Department of Neurology (M.T.K., H.T., M.G.S., F.O.), GATA Haydarpas¸a Training Hospital; and Department of Radiology (M.S.), GATA Haydarpas¸a Training Hospital; and Division of Otorhinolaryngology (A.A.), Istanbul Surgery Hospital, Istanbul; and Department of Otorhinolaryngology (M.C.), Amasya University Training and Research Hospital, Amasya, Turkey. Editor’s Note: This Manuscript was accepted for publication December 12, 2013. The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Aytu g Altunda g, MD, Istanbul Surgery Hospital, Division of Otorhinolaryngology, Ferah Sok. No: 22 S¸is¸li, Istanbul, P.K.: 34365, Turkey. E-mail: [email protected] DOI: 10.1002/lary.24565
Laryngoscope 00: Month 2014
most widely used self-report questionnaire to assess daytime sleepiness in the clinical setting, particularly in patients with OSA, and polysomnography (PSG) is the gold standard assessment method for OSA.3,11,12 Olfaction is one of the five neurosensory systems, which plays an important role in human daily life, for example, by alerting us against and attracting us toward odorous items, influencing food intake, and affecting interpersonal relations.13 There is strong evidence that cognitive impairment exhibits a significant influence on olfactory function, as well as other major factors affecting the olfactory function: head trauma, upper respiratory tract infections, and sinonasal disorders.14–16 The effect of OSA on olfactory functions has not yet been investigated. The odorants travel to the olfactory receptors by two routes. Sniffing brings odorants through the nostrils into the nasal cavity (orthonasal olfaction), and chewing and swallowing force odorants emitted by foods upward behind the palate into the nasal cavity from the rear of the mouth (retronasal olfaction).17–19 Studies have suggested that the olfactory bulb volume (OB), measured by planimetric manual contouring on magnetic resonance imaging (MRI), is a reliable measure of olfactory function.20,21 Thus, the aim of this study was to investigate the effect of OSA on the parameters of olfactory functions, odor threshold, odor discrimination, and odor identification tests for orthonasal olfaction, retronasal olfactory testing, and OB volumes. lu et al.: OSA and Olfaction Salihog
1
MATERIALS AND METHODS Volunteers and Study Design We conducted a prospective clinical study at the Neurology and Otorhinolaryngology Department of G€ ulhane Military Medicine Academy (GATA) Haydarpas¸a Training Hospital. All investigations were performed in accordance with the Declaration of Helsinki on biomedical studies involving human subjects, and informed consent was obtained from all participants before the study began. This study was approved by the Clinical Research Ethics Committee of Istanbul Cerrahpasa Medical Faculty (10.05.13-83045809/11280). The participants were selected from patients who presented with a clinical suspicion of OSA and were admitted to the sleep lab of GATA Haydarpas¸a Training Hospital. Prior to the onset of the sleep study, the data were registered for each participant individually, including height and weight, to calculate body mass index (BMI), medical history, tobacco use, and a list of current medications. Nasopharyngeal endoscopy was also performed. Exclusion criteria included patients with a history of upper respiratory infections within the past 3 weeks, taste and smell disorders, sinonasal disorders (nasal polyps, chronic rhinosinusitis, allergic rhinitis), asthma, malignancy, head trauma, neurologic and psychiatric disorders (Alzheimer’s disorder, Parkinson’s disease, epilepsy, schizophrenia), metabolic and endocrine disorders (diabetes mellitus, hypogonadism), or a current history of smoking more than 3 cigarettes per day. In addition, patients who underwent sleep surgery or were currently using continuous positive airway pressure were not included in the study. A validated Turkish version of the ESS questionnaire22 was completed (eight items with a four-point scale [0–3]) as previously decsribed11 for every participant included in the study.
Polysomnographical Evaluation All participants underwent a full-night PSG study with at least 7 hours of recording time (Model AURA PSG Base, Software Grass Database Explorer Version 4.5.3.23; Astro-Med Inc., Grass Technologies, W. Warwick, RI). Sleep staging was scored according to the criteria of the American Academy of Sleep Medicine (AASM) published in 2007.3 Apnea was defined as the cessation of airflow for 10 seconds. Hypopnea was defined as a 30% reduction of airflow lasting 10 seconds and associated with a 4% decrease in oxyhemoglobin saturation. The number of apneas and hypopneas per hour of sleep was calculated to obtain the apnea-hypopnea index (AHI). The participants were classified into three different groups according to the diagnostic criteria for OSA based on the AASM criteria per reported AHI values from the overnight PSG study: 1) the primary snoring group, which was the control group of the study (AHI
Rhinological and Otological Society, Inc.
The Effect of Obstructive Sleep Apnea on Olfactory Functions lu, MD; Mustafa Tansel Kendirli, MD; Aytug Altundag , MD; Hakan Tekeli, MD; Murat Salihog € lam, MD; Melih C¸ay€on€ , MD Muzaffer Sag u, MD; Mehmet G€ uney S¸enol, MD; Fatih Ozda g Objectives/Hypothesis: The aim of this study was to investigate the effect of obstructive sleep apnea (OSA) on the parameters of olfactory functions (odor threshold, odor discrimination, and odor identification tests) for orthonasal olfaction, retronasal olfactory testing, and olfactory bulb (OB) volumes. Study Design: Prospective clinical study. Methods: This study was carried out in 78 volunteers between the ages of 20 and 60 years. The mean age of the patients was 46 6 10.1 years. Patients were divided into three groups according to polysomnography results: 1) a control group, 2) a mild to moderate OSA group, and 3) a severe OSA group. Clinical features of the participants were evaluated with the Epworth Sleepiness Scale. Orthonasal and retronasal olfactory testing were performed with Sniffin’ Sticks olfactory testing and retronasal olfactory testing, respectively. Olfactory bulb volumes were measured by planimetric manual contouring on magnetic resonance imaging (MRI). Results: The current investigation produced four major findings: 1) The apnea-hypopnea index had a significant and strong negative correlation with odor threshold scores and odor discrimination scores; 2) The apnea-hypopnea index was significantly negatively correlated with odor identification score and both right and left OB volumes; 3) retronasal olfactory scores were not significantly affected by OSA; and 4) continuous O2 saturation had a significant positive correlation on orthonasal olfactory functions, particularly the odor threshold and discrimination scores. Conclusions: This study demonstrated that OSA had significant negative effects on all orthonasal olfactory tasks, especially on threshold and discrimination. MRI also revealed volumetric shrinkage of OB volumes. Key Words: Obstructive sleep apnea, polysomnography, olfaction disorders, Sniffin’ Sticks, olfactory bulb. Level of Evidence: 3b. Laryngoscope, 00:000–000, 2014
INTRODUCTION It is well known that obstructive sleep apnea (OSA) is characterized by breathing cessation (apnea) or reduction of airflow (hypopnea) during sleep, heavy snoring, and daytime sleepiness.1–3 OSA is a disease affecting about 2% to 4% of the adult population and is becoming more commonly recognized because of its significant negative effects, including increased risks of cardiovascular and cerebrovascular mortality and morbidity.4–6 It is also known that OSA is associated with neurocognitive and psychological problems, such as memory and new learning, attention, executive function, and depression.7–10 The Epworth Sleepiness Scale (ESS) is the
From the Department of Otorhinolaryngology (M.SALIHOGLU) Department of Neurology (M.T.K., H.T., M.G.S., F.O.), GATA Haydarpas¸a Training Hospital; and Department of Radiology (M.S.), GATA Haydarpas¸a Training Hospital; and Division of Otorhinolaryngology (A.A.), Istanbul Surgery Hospital, Istanbul; and Department of Otorhinolaryngology (M.C.), Amasya University Training and Research Hospital, Amasya, Turkey. Editor’s Note: This Manuscript was accepted for publication December 12, 2013. The authors have no funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Aytu g Altunda g, MD, Istanbul Surgery Hospital, Division of Otorhinolaryngology, Ferah Sok. No: 22 S¸is¸li, Istanbul, P.K.: 34365, Turkey. E-mail: [email protected] DOI: 10.1002/lary.24565
Laryngoscope 00: Month 2014
most widely used self-report questionnaire to assess daytime sleepiness in the clinical setting, particularly in patients with OSA, and polysomnography (PSG) is the gold standard assessment method for OSA.3,11,12 Olfaction is one of the five neurosensory systems, which plays an important role in human daily life, for example, by alerting us against and attracting us toward odorous items, influencing food intake, and affecting interpersonal relations.13 There is strong evidence that cognitive impairment exhibits a significant influence on olfactory function, as well as other major factors affecting the olfactory function: head trauma, upper respiratory tract infections, and sinonasal disorders.14–16 The effect of OSA on olfactory functions has not yet been investigated. The odorants travel to the olfactory receptors by two routes. Sniffing brings odorants through the nostrils into the nasal cavity (orthonasal olfaction), and chewing and swallowing force odorants emitted by foods upward behind the palate into the nasal cavity from the rear of the mouth (retronasal olfaction).17–19 Studies have suggested that the olfactory bulb volume (OB), measured by planimetric manual contouring on magnetic resonance imaging (MRI), is a reliable measure of olfactory function.20,21 Thus, the aim of this study was to investigate the effect of OSA on the parameters of olfactory functions, odor threshold, odor discrimination, and odor identification tests for orthonasal olfaction, retronasal olfactory testing, and OB volumes. lu et al.: OSA and Olfaction Salihog
1
MATERIALS AND METHODS Volunteers and Study Design We conducted a prospective clinical study at the Neurology and Otorhinolaryngology Department of G€ ulhane Military Medicine Academy (GATA) Haydarpas¸a Training Hospital. All investigations were performed in accordance with the Declaration of Helsinki on biomedical studies involving human subjects, and informed consent was obtained from all participants before the study began. This study was approved by the Clinical Research Ethics Committee of Istanbul Cerrahpasa Medical Faculty (10.05.13-83045809/11280). The participants were selected from patients who presented with a clinical suspicion of OSA and were admitted to the sleep lab of GATA Haydarpas¸a Training Hospital. Prior to the onset of the sleep study, the data were registered for each participant individually, including height and weight, to calculate body mass index (BMI), medical history, tobacco use, and a list of current medications. Nasopharyngeal endoscopy was also performed. Exclusion criteria included patients with a history of upper respiratory infections within the past 3 weeks, taste and smell disorders, sinonasal disorders (nasal polyps, chronic rhinosinusitis, allergic rhinitis), asthma, malignancy, head trauma, neurologic and psychiatric disorders (Alzheimer’s disorder, Parkinson’s disease, epilepsy, schizophrenia), metabolic and endocrine disorders (diabetes mellitus, hypogonadism), or a current history of smoking more than 3 cigarettes per day. In addition, patients who underwent sleep surgery or were currently using continuous positive airway pressure were not included in the study. A validated Turkish version of the ESS questionnaire22 was completed (eight items with a four-point scale [0–3]) as previously decsribed11 for every participant included in the study.
Polysomnographical Evaluation All participants underwent a full-night PSG study with at least 7 hours of recording time (Model AURA PSG Base, Software Grass Database Explorer Version 4.5.3.23; Astro-Med Inc., Grass Technologies, W. Warwick, RI). Sleep staging was scored according to the criteria of the American Academy of Sleep Medicine (AASM) published in 2007.3 Apnea was defined as the cessation of airflow for 10 seconds. Hypopnea was defined as a 30% reduction of airflow lasting 10 seconds and associated with a 4% decrease in oxyhemoglobin saturation. The number of apneas and hypopneas per hour of sleep was calculated to obtain the apnea-hypopnea index (AHI). The participants were classified into three different groups according to the diagnostic criteria for OSA based on the AASM criteria per reported AHI values from the overnight PSG study: 1) the primary snoring group, which was the control group of the study (AHI
