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Smell Distortions: Prevalence, Longevity and Impact of Parosmia in a Population-Based, Longitudinal Study Spanning 10 Years

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Smell Distortions: Prevalence, Longevity and Impact of Parosmia in a Population-Based, Longitudinal Study Spanning 10 Years Smell distortions: Prevalence, longevity and impact of parosmia in a population-based, longitudinal study spanning 10 years Jonas K. Olofsson*1, Fredrik Ekesten1, & Steven Nordin2 1Department of Psychology, Stockholm University, Stockholm, Sweden 2Department of Psychology, Umeå University, Umeå, Sweden *Corresponding author: [email protected] Abstract. Parosmia, experiences of distorted smell sensations, is a common consequence of covid-19. The phenomenon is not well understood in terms of its impact and long-term outcomes. We examined parosmia in a population-based sample from the Betula study that was conducted in Umeå in northern Sweden (baseline data collected in 1998-2000). We used a baseline sample of 2168 individuals aged 35-90 years and with no cognitive impairment at baseline. We investigated the prevalence of parosmia and, using regression analyses, its relationship to other olfactory and cognitive variables and quality of life. Benefitting from the longitudinal study design, we also assessed the persistence of parosmia over 5 and 10 years prospectively. Parosmia was prevalent in 5% of the population (n=104) and was often co- occurring with phantosmia (“olfactory hallucinations”), but was not associated with lower self-rated overall quality of life or poor performance on olfactory or cognitive tests. For some individuals, parosmia was retained 5 years (17%) or even 10 years later (10%). Thus, parosmia is relative common in the population, and can be persistent for some individuals. This work provides rare insights into the expected impact of, and recovery from parosmia, with implications for those suffering from qualitative olfactory dysfunction following covid-19. 2 Introduction Parosmia is an olfactory disorder (OD) where odor perception is distorted and different stimuli trigger unpleasant odor sensations previously not associated with the stimuli (i.e. smelling freshly brewed coffee, but experiencing a rotten smell). Parosmia is, together with Phantosmia (experiencing an odor without the presence of a triggering source), referred to as qualitative ODs (Nordin et al., 1996; Nordin, Brämerson, Millqvist and Bende, 2007; Croy et al., 2014). Qualitative OD is less well understood than quantitative OD, such as hyposmia, reduced olfactory ability; and anosmia, complete loss of smell (Frasnelli and Hummel, 2005; Landis, Frasnelli, Croy and Hummel, 2010; Reden, Maroldt, Fritz, Zahnert, and Hummel, 2006). Olfactory disorders are common in the general population, especially in the older age- groups, but are often not diagnosed (Desiato et al., 2020). The overall prevalence of OD in the general population was estimated to 28.8% with objective measurements, and about 9.5% with subjective assessments (Desiato et al., 2020). A Swedish population-based study yielded an estimated parosmia prevalence of 4.0% in the adult population (Nordin et al., 2007). The olfactory experiences in parosmia are unpleasant; rotten, burnt and sewage are examples of sensations reported by parosmics, and tobacco, coffee, perfume and citrus fruits are some of the most common triggers (Bonfils et al., 2005). The covid-19 pandemic has led to an increased awareness of, and interest in parosmia. Although patients with parosmia tend to describe their olfactory experience as being the smell of for example sewage, it seems that the actual sensation is novel (AbScent Anosmia Support, 2021). Patients resort to illustrating their parosmic sensation with names of odors that are common and unpleasant, to communicate the level of disgust experienced (AbScent Anosmia Support, 2021). Olfactory deficits are more common in men than in women (Desiato et al., 2020). Phantosmia on the other hand may be more common in women (Sjölund, Larsson, Olofsson, Seubert and Laukka, 2017). Parosmia is thought to similarly affect men and women (Croy, Yarina and Hummel, 2013; Landis et al., 2010; Nordin et al., 2007). Some studies found no association between parosmia and age (Cory et al., 2013; Landis et al., 2010), whereas others report higher prevalence in young adults (Nordin et al., 2007). Parosmia often co-occurs with a quantitative OD (Bonfils, Avan, Faulcon and Malinvaud, 2005; Croy et al., 2013; Frasnelli and Hummel, 2005; Landis et al., 2010; Reden et al., 2006). Between 10% and 60% of the OD patient-group suffer from parosmia (Croy et al., 2014; Landis et al., 2010; Reden et al., 2006). Between 83% and 100% are thought to have also a quantitative OD (Bonfils et al., 2005; Frasnelli and Hummel, 2005; Landis et al., 2010), where hyposmia appears most commonly observed (Bonfils et al., 2005; Frasnelli and Hummel, 2005; Reden et al., 2006). The most common etiologies for parosmia are upper respiratory tract infection (URTI) (Bitter et al., 2011), head trauma (Iannilli, Leopold, Hornung and Hummel, 2019), sinonasal disease (Landis et al., 2010; Reden et al., 2006), neurological deficits, exposure to toxic chemicals, psychiatric connections and nasal operations (Bonfils et al., 2005). Covid-19 is a type of URTI (Sayin, Yaşar, and Yazici, 2020). In a recent comparison between covid-19-positive patients and patients with a different type of URTI, results showed that both parosmia and hyposmia were more frequent in the covid-19-positive group (Sayin et al., 2020). Hence, parosmia and quantitative ODs appear strongly associated, and the covid-19 pandemic has emphasized the need for understanding their long-term impact. Research conducted before the covid-19 pandemic indicated that 57.1% of parosmia cases develop either simultaneously with, or within a few months following the onset of a quantitative OD (Bonfils et al., 2005). The longitudinal prognosis of parosmia is uncertain, 3 since there is little known about how persistent parosmia is over time. There are records of patients reportedly having had parosmia between three months to 22 years, though these are based on retrospective self-evaluations (Bonfils et al., 2005). Parosmia is associated with a lower volume of olfactory cortical regions, as well as behavioral deficits in odor discrimination and memory (Bitter et al., 2011). This morphological difference might help explain the distorted olfactory qualities (Bitter et al., 2011). In a study examining brain activation, patients with parosmia and hyposmia had a higher activation in areas associated with attention directing (in relation to smells), the processing of odor valence, and the perception of contempt and disgust (Iannilli et al., 2019). Generally, unpleasant odors result in a stronger brain activation since they are more important to identify than pleasant ones, due to their higher biological significance (Iannilli et al., 2019). Parosmia may thus either cause, or be a consequence of, a combination of atrophy and disrupted brain activation paths. It is critical to understand the persistence of parosmia, since it could be a chronic disease for some individuals. Olfactory disorders have been associated with depression and a reduced quality of life (QoL). Patients with depression often perform worse than healthy controls on olfactory tests (Kohli et al., 2016). Patients with more severe depression are more likely to report parosmia and/or phantosmia (Croy et al., 2013). Between one fourth to one third of individuals with ODs exhibited symptoms of depression, whilst about a third experienced a lowered QoL (Croy, Nordin and Hummel, 2014). Furthermore, about one third of individuals with qualitative ODs reported high depression scores on Beck's Depression Inventory (BDI) (Croy et al, 2014). Severe self-rated qualitative OD is associated with more severe self-rated depression (Croy et al., 2013). About half of parosmic patients reported their quality of life as being severely affected due to their OD (Bonfils et al., 2005). Patients with parosmia and an olfactory deficit have difficulty coping with their olfactory dysfunction, compared to patients with only an olfactory deficit (Frasnelli and Hummel, 2005). Mild depression was significantly more frequent in the parosmic group, compared to a control group with only quantitative ODs (Frasnelli and Hummel, 2005). Patients may adapt to their OD over time, resulting in reduced depressive symptoms at follow-up (Croy et al. 2014). Thus, patients with ODs, and especially parosmia, more often experience a lowered quality of life due to their disorder, and are at higher risk of having depression. It is unclear to what extent an OD results in more depressive symptoms or if depression might also be affecting olfactory recovery. While olfactory loss may result in reduced food consumtion, but also compensatory overeating (Croy et al., 2014), parosmia has negative effects on appetite, mood, or interpersonal relationships (Temmel et al., 2002). Food flavor is distorted in parosmia, and appetite is diminished (Bonfils et al., 2005; Temmel et al., 2002). There is a lack of large-scale, prospective studies on parosmia in the general population. Given the current circumstances of the covid-19-pandemic, it is critical to estimate the persistence and impact of parosmia. We used population-based data from the longitudinal Betula study to investigate the prevalence of parosmia in a large sample of adults, and its development over 5 and 10 years. Additionally, we investigated associations between parosmia and demographic (sex, age, education), olfactory (self-rated ability to perceive weak odors, phantosmia, current disease in nose, performance on the Scandinavian Odor Identification Test, SOIT), cognitive ability (vocabulary and
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