Effects of COVID-19 on Sense of Smell: Human Factors/Ergonomics Considerations

Objective We review the effects of COVID-19 on the human sense of smell (olfaction) and discuss implications for human-system interactions. We emphasize how critical smell is and how the widespread loss of smell due to COVID-19 will impact human-system interaction. Background COVID-19 reduces the sense of smell in people who contract the disease. Thus far, olfaction has received relatively little attention from human factors/ergonomics professionals. While smell is not a primary means of human-system communication, humans rely on smell in many important ways related to both quality of life and safety. Method We briefly review and synthesize the rapidly expanding literature through September 2020 on the topic of smell loss caused by COVID-19. We interpret findings in terms of their relevance to human factors/ergonomics researchers and practitioners. Results Since March 2020 dozens of articles have been published that report smell loss in COVID-19 patients. The prevalence and duration of COVID-19-related smell loss is still under investigation, but the available data suggest that it may leave many people with long-term deficits and distortions in sense of smell. Conclusion We suggest that the human factors/ergonomics community could become more aware of the importance of the sense of smell and focus on accommodating the increasing number of people with reduced olfactory performance. Application We present examples of how olfaction can augment human-system communication and how human factors/ergonomics professionals might accommodate people with olfactory dysfunction. While seemingly at odds, both of these goals can be achieved.

Attempts to answer the question of how human factors/ergonomics professionals can help with the ongoing COVID-19 pandemic have focused primarily on clinical environments (see Gurses et al., 2020). In this artipatients after recovery from the most severe reduction in, or loss of, sense of smell (olfaction). We demonstrate the importance of olfaction in human perception and performance, and encourage the human factors/ergonomics community to become more aware of the importance of human olfaction and consider taking action in two disparate ways: integrate olfaction into systems design as another means of human-system communication and accommodate the increasing number of people with reduced smell function.
While these two goals may seem contradictory, we feel both are achievable and important. Olfaction can be used as another form of redundant sensory coding, just as we use multiple forms of visual, auditory, and tactile coding in human-system communication.

COVID-19 AND SENSE OF SMELL
At the time of submission of this review, dozens of studies had been published regarding smell loss in COVID-19 patients, with the earliest appearing in late March  indicating that smell loss could be an early marker of the disease. Most of the data reported thus far come from self-report (e.g., Bagheri et al., 2020;Giacomelli et al., 2020;Lechien et al., 2020;Parma et al., 2020;Qiu et al., 2020;Speth et al., 2020;Yan et al., 2020), which is well known not to correlate with objective measures of smell function (Landis et al., 2003;Soter et al., 2008;Wehling et al., 2011). Microsmia-a subtle smell loss-often goes undetected, and even anosmia-complete smell loss-can go undetected. Thus, the extent of smell loss from COVID-19 may be underestimated (e.g., Tong et al., 2020). Indeed, one study that measured smell loss objectively found that 98% of COVID-19 patients had some smell loss although only 35% reported any smell dysfunction when asked (Moein, Hashemian, Mansourafshar, et al., 2020).
Although prevalence estimates have varied considerably, it is clear that many or even most COVID-19 patients have demonstrable smell loss. By mid-April 2020, the Center for Disease or smell" as a symptom of COVID-19 (https:// www. cdc. gov/ coronavirus/ 2019-ncov/ symptoms-testing/ symptoms. html).
The duration of smell loss in COVID-19 patients is still under investigation, but available data suggest that recovery typically occurs, if not completely, within days or weeks Lee et al., 2020;. Given the duration of the pandemic, no studies have yet been able 19 on smell loss. Anecdotal evidence suggests that for some people, smell loss may be longlasting (see, for example, posts at: https://www. facebook. com/ groups/ AbScentCovid19/). Even when recovery of function occurs, a later postrecovery parosmia-distortion of the perception of odors-has also been reported (Burges Watson et al., 2020).
mon colds") are one of the primary triggers for permanent smell loss (Hawkes & Doty, 2009). Given that smell loss is a symptom of COVID-estimate the extent of the issue, the scale of the pandemic means that at any given time, many sense of smell. Furthermore, even if persistent centage of COVID-19 survivors, there may be a substantial number left with long-term smell Soler et al., 2020).

FUNCTIONS OF SMELL
Widespread loss of smell due to COVID-19 has increased awareness of how critical the chemical senses are to human behavior. Personal responses to such losses range from minor annoyance to major devastation; consider the end of a career for a chef.
Because humans rely so heavily on vision and audition, a majority of perceptual research over the past 100 years has focused on these senses. Similarly, both research and applied human factors/ergonomics work has focused on visual and auditory displays to engage these primary senses and facilitate humansystem interaction. Human factors/ergonomics practitioners also exploit other sensory modalities such as vibro-tactile sense, kinesthesia, proprioception, and vestibular senses, but in less overt ways. For example, a driver may rely on kinesthesia and proprioception to learn the locations of controls in a car and rely on tactile sensation to discriminate between On the other hand, olfaction has generally received less attention from human factors/ ergonomics professionals, aside from a mention in introductory textbooks of the addition of methyl mercaptan to natural gas, which is odorless and almost impossible to detect by itself. The important functions that olfaction plays in basic human behavior are often less obvious than those of vision and audition and therefore less appreciated. We rely on smell in important ways that relate to both quality of life and safety. Stevenson (2010) identirelated to ingestion (e.g., enjoyment of food, eating a well-balanced diet, avoiding unsafe foods), avoiding environmental hazards (e.g., (e.g., recognizing kin). Furthermore, familwhereas novel, unexpected odors detected in well-known environments, make us uneasy (Köster et al., 2014). Although rarely acknowledged, olfactory problems are associated with a variety of negative outcomes (Erskine & Philpott, 2020;Miwa et al., 2001). why many elderly persons complain that food die in accidental gas poisonings. These cheincreased risk related to hazards such as food hazardous chemical exposure (Santos et al., 2004 for a review, see ). The sense of smell interacts with other sensory systems (see De Luca & Botelho, 2019 for a review). For example, the combination of smell food. Indeed, it is common for people to believe they have a taste loss when they are actually experiencing smell loss (Hawkes & Doty, 2009). Odors can be used to increase attentiveness and performance on a visual task requiring sustained attention (vigilance) without increasing stress (Dember et al., 1995;Warm et al., 1991). Though not a contributing factor to motion sickness, unpleasant smells, are perceived as even more unpleasant; and pleasant smells, more pleasant after motioninduced sickness (Paillard et al., 2014). Smell also plays an important role in emotional state (Herz, 2002;Hofer et al., 2020). The multi-billion-dollar fragrance and perfume industry speaks to the

OLFACTION IN SYSTEM DESIGN
Now that COVID-19 has awakened us to the fragility of our sense of smell, and given the important functions that olfaction serves, here we consider some possible ways in which human factors/ergonomics professionals could be thinking about olfaction. First, we address ways in which olfaction can be further harnessed as a means of human-system interaction and second, we address ways to accommodate people's olfactory dysfuncwe feel that both are achievable.

Smell: An Additional Channel of Human-System Communication
Since about 2010 there has been a small but steady increase in applied research on media" (see, for example, Ghinea et al., 2014;Kannan & Andres, 2010). Mulsemedia systems involve at least three senses (Ghinea et al., 2014)-increasingly including smell-ically integrate just audio and visual displays.
There is a long, but intermittent history of using smell as a means of communication between systems and human users, starting with the scent of roses delivered to audiences 1906 (Logino, 1999 as cited in Kaye, 2001). The consideration of smell as an additional channel of human-system interaction is on the rise for both entertainment and productivity (e.g., Maggioni et al., 2018). For a review of the technology associated with olfactory interfaces and related human factors issues see Yanagida (2008).
Here we present some possible ways to integrate smell as an additional channel of communication in system design. and can be used in stressful environments, such as emergency department waiting rooms. For example, pleasant, familiar odors reduce perceived stress and peripheral nervous system activity (Calvi et al., 2020;Glass & Heuberger, 2016; Joussain et al., 2014 on learned associations (e.g., Schachtman, 2016 people to perceive dental treatment as more painful when they smell the typical eugenol (clove) odor in a dental clinic (Robin et al., 1999). Using other odors to mask this odor might reduce anxiety and pain of dental visits.
in scent marketing. Car dealerships exploit the scents, and many fashion shops use fragrances Teerling et al. (1992) found that some odors, added to the ventilation systems of clothing stores in low concentrations, resulted in longer customer visits and Holland et al. (2005) found that people exposed to a citrus-scented cleaning product demonstrated both increased mental access to the concept of cleaning and increased cleaning behavior. Although beyond the scope of this review, some behavior even when presented at a level below conscious awareness (De Luca & Botelho, 2019;Li et al., 2007). Smells could be used to guide people with dementia around a memory care institution in which they live. Visual signage, which relies on reading and visual and semantic memory, might not work well for these people. Smells could be corridors by using characteristic smells for each corridor. This technique could also be used to guide blind people to a corridor or room.
tasks for groups of mentally disabled people. For example, food odors from the kitchen can be used to help prepare people for mealtime by setting up expectations and generating the appetite and cephalic responses that prepare the digestive system. Chlorine odor has been used in a Dutch residential facility to set the stage for changing into a swimsuit before a trip to the swimming pool (E.P. Köster, personal communication, June 25, 2020).
for human factors applications.

Accommodating People With Smell Dysfunction
Human factors/ergonomics professionals strive to consider all potential users of systems that we help design. We are trained to accommodate people with a wide range of anthropometric dimensions and physical, visual, auditory, and cognitive abilities. Given the smell loss that many people will experience as a result of COVID-19, and the risk of harm that comes with this loss, we are now called upon to consider how the human factors/ergonomics community might help. function and the implications it has for safety and quality of life. Many people are unaware just being made aware or reminded of olfacsome avenues for exploration in which we may be able to help people cope more directly Increase reminders both within the devices themselves and in public service announcements to check batteries in smoke detectors to make up for decreases in sensitivity to smelling smoke. Increase size and contrast of expiration dates or provide other salient, visual indications when food is spoiled. Increase prominence of nutrition labels (see Goldberg et al., 1999) and awareness of nutrient intake to compensate for nutritional inadequacies associated with the loss of smell. Recruit people with olfactory dysfunction when conducting usability studies on systems where smell is used as a means of human-system communication.
Use objective measures of olfactory function when employees are recovering from smell loss to determine when they are able to return to work where sense of smell is critical for task performance (e.g., gas line maintenance, food production/quality control). Provide other indicators (e.g., visual) as reminders to launder soiled clothes and change diapers. Provide visual or auditory indicators that a mechanical device is overheating or malfunctioning in other ways that might normally be detected by smell. Provide visual indicators that chemicals such as chlorine are reaching unhealthy levels (either too high or too low) in a swimming pool or water treatment system. Improve surgical devices by providing visual and auditory feedback to surgeons who no longer can smell burning tissue or other relevant smells. Provide more salient visual indicators on gas stoves to indicate when they are on and releasing gas, make gas stove valves less susceptible to accidental activation (Pollack, 2019), and encourage people to use electronic gas detectors (Wogalter & Laughery, 2011). Develop a gauge to measure spiciness of food. This is not intended as an exhaustive list. Rather we encourage readers to consider these and other ways that human factors/ergonomics professionals can help guide user interface design to accommodate COVID-19 patients who have lost their sense of smell.

MEASURING SENSE OF SMELL
There are many reasons that human factors/ergonomics professionals may need to assess a person's sense of smell. Here are some examples: Screening participants for usability testing of a medication delivery system in which smell indicates a leak. an underground environment in which an odor is added to ventilation air to signal emergency evacuation. Testing to determine the appropriate strength of new system design.
There are a number of commercially available, objective tests to assess sense of smell, but by far the most commonly used tests are the Test, UPSIT (Doty et al., 1984) from Sensonics ( www. sensonics. com) and the Screening 12 Test kit from Burghart (https:// smelltest. eu/ en/ burghart-sniffin-sticks-burghart-smelltests/). We encourage use of objective measures of smell function whenever possible, given that self-report is unreliable.

CONCLUSION
In conclusion, the COVID-19 pandemic is ple. The scale of the pandemic means that at any ciencies in their sense of smell, and some may experience permanent dysfunction. We encourage the human factors/ergonomics professional community to (1) be aware of the importance of the sense of smell for human behavior and of the of products and systems that we help develop, (3) consider ways to accommodate people with such sensory disabilities, and (4) consider new ways of using smell as an additional channel of human-system communication.

KEY POINTS
COVID-19 is known to reduce the olfactory sense (smell) in people who contract the disease.
The duration of the loss is not well characterized at this time, but some may experience permanent dysfunction in the sense of smell. Human factors/ergonomics professionals should be aware of the increased number of people with olfactory dysfunction and consider ways to accommodate them. While the sense of smell is not commonly thought of as a primary means of human-system communication, we rely on smell in many important ways that relate to both quality of life and safety. Olfaction has received relatively little attention from human factors/ergonomics professionals. Product research and development teams have just begun to tap into the sense of smell to augment human system communication.