**4. The Human Perception of Malodors**

Perception of a malodor occurs when a molecule activates receptor cells linked to one of several cranial nerves associated with chemoreception. The olfactory nerves of the nasal epithelium are the most significant in odor perception and transmit information from the nasal cavity to the olfactory bulb, which in turn transmits olfactory information to other areas of the brain. In addition, the trigeminal nerve transmits information about pungency from the mouth and eyes as well as the nose. The chorda tympani nerve, glossopharyngeal nerve or vagus nerve may additionally be activated if the compound enters via the mouth [27].

Pungency and odor perception have been determined to be separate chemical senses, as anosmics, who lack the ability to smell, can still sense chemicals through their pungency effects in the nose, mouth and elsewhere [28]. While unpleasant olfactory sensations define malodors, at sufficiently high concentrations these sensations can be further accompanied by unpleasant pungency sensations.

The chemical senses of odor and pungency perception vary in several significant ways. For one, the threshold detection for pungency is generally several orders of magnitude higher in concentration than what is required to perceive the odor; people most often perceive a smell before it becomes so strong as to sting their eyes [29]. Though people may adapt to a constant odor in a matter of minutes or hours, adaptation to the perception of pungency occurs over longer periods [30].

Detection thresholds for malodors vary dramatically depending on the specific chemical in question, with thresholds generally declining with the carbon chain length of the compound [28,29]. Humans can detect common indoor malodors like hexyl acetate at concentrations as low as 2.9 parts per billion [30]. Malodors from sulfur compounds like isoamyl mercaptan can be detected at concentrations as low as 0.77 parts per trillion (ppt) [31], and MVOC can be detected as low as 0.2 ppt (i.e., from 2-Isopropyl-3-methoxy-pyrazine) [15]. From an evolutionary point of view, this ability to detect extremely low concentrations of chemical compounds in the air affords identification of various sources of danger, such as spoiled food or harmful chemicals.

Like all senses, olfaction is a product of biological evolution whose features are linked to survival and adaptation [32]. To this end, major connections have been identified between the olfactory system and cognitive processes, such as associative learning [33] and emotional memory [34–36], as well as "fight or flight" response [37]. "Top-down" cognitive functions, such as risk and danger perception, can also influence "bottom-up" information from the odor stimulus by allocating greater attentional resources to malodors, thus increasing their negative impact [38].

While the perception of malodors across individuals follows the same physiological pathways, the intensity of and response to the perception can vary. Although there can be differences across individuals in their sensitivity to specific malodors, the more important drivers of an individual's hedonic response may be due to their expectations, past experiences and the context in which an odor is experienced. For instance, the smell of smoke around a campfire can evoke a positive scent experience. However, the smell of smoke within a home will evoke an entirely different response, as the smoke is a signal of danger in this context.

### **5. The Negative E**ff**ects of Malodors**

Utilizing the search term "malodor harm" or variations thereof (e.g., synonyms of "malodor" and "harm") via publicly available databases such as ScienceDirect (https://www.sciencedirect.com/) revealed scientific research across an array of disciplines documenting various negative effects associated with malodors. These negative effects were observed to cluster into six categories as identified by the authors of this review (Figure 1).

**Figure 1.** Reported negative effects associated with exposure to malodors.

Studies evaluating the negative effects of malodors have been conducted in both the field (observational) and the laboratory (experimental) employing a variety of dependent measures (Table 1).


**Table 1.** Measurement of malodor effects conducted in the field via observations and in the laboratory (Lab) via experimental methods.

Several studies have reported the negative effect of malodors on mood. Self-reported feelings of depression [39,40], fatigue [39,40], confusion [39,41], aggression [40,60,61], and tension [39,40] have all been positively correlated with malodor exposure, whereas subjective well-being [40] has been negatively correlated with such exposures. Even when no malodor is present, expectations of malodor exposure may cause negative effects on mood [43].

Malodors may cause individuals to feel a lack of control over their environment, adversely affecting stress levels. Indoor household malodors of external origin that are consistent and uncontrollable may produce feelings of helplessness [39,62]. Perceived control has also been shown to affect tolerance of a given malodor [44]. Individual coping style, however, may also affect odor annoyance and symptom

prevalence. Studies have suggested that those who have "palliative" or avoidance coping styles generally report less annoyance and symptoms than those with "instrumental" or problem-oriented coping styles [52]. Stress about the perceived toxicological effects of malodors may further allow odors to act as a trigger for other symptoms and behaviors [48–50].

Malodors have been shown to have detrimental effects on cognition. Rotton [44] has shown that exposure to malodor does not affect simple cognitive tasks, but that it has a detrimental effect on more complex tasks, such as proofreading. Cognitive deficits resulting from malodor exposure may be due to their negative effect on focus [45].

Malodors have been shown to elicit somatic symptoms. Somatic symptoms that have been reported with malodor exposure include vomiting, nausea, dizziness, headache, loss of appetite, sleep disorders and irritation of eyes, throat and nose [2,63]. Malodors can also cause somatic symptoms via "odor-worry" and stress [46]. Asthmatics, for example, may experience exacerbation of symptoms from non-irritating odors that are perceived as harmful [51]. Others may experience the stress effects of malodors because of "environmental worry" [46], an association with the odor as socially taboo or by perceiving possible property devaluation resulting from the odor [39]. Exposure to certain malodors has also been shown to affect the immune system, an effect probably mediated by perceived stress [47].

Social relations are also threatened by indoor malodors. Habituation to the odors of one's background can make people acutely aware of intrusive malodors, which may cause a variety of problems in social settings. Subjective ratings of odor unpleasantness have been shown to correlate with perception of socially undesirable traits [54]. Odor perception may also integrate with higher-order visual processes, such as facial perception. Unpleasant facial expressions paired with malodors have been shown to increase people's ratings of odor intensity and decrease their respiratory amplitude [53]. Judgments of interpersonal attraction are also influenced by the presence of malodor [64]. Indoor malodors can also reduce social interactions by causing inhabitants to experience shame or embarrassment about the malodor, even when they are external in origin [55]. It is reasonable to assume that this occurs with household odors as well.

Malodors can have economic effects. Unlike other "less visible" forms of pollution, malodors are readily identified and capitalized into property values [56]. Some industries, such as tanneries, paint factories, pulp mills and livestock operations, are regulated by legislated minimum "setback distances" that facilities must maintain from surrounding properties. Setbacks are used to minimize the economic effects of pollution, including malodors. Not only do properties surrounding these facilities decrease in value, but if the facilities' setback distance from surrounding properties is either unenforced or inaccurately determined [4,57], then malodors emitted from the facility can result in net economic loss, despite efficiency gains made by the offending firm [58]. Business and home owners alike can also suffer economic consequences. Malodors can affect car sales [59], worker productivity at call centers [9] and consumer satisfaction within the hospitality industry [65].

It is important to note that these negative effects are not necessarily independent measures and that individual effects can often act to compound economic ones. Levy and Yagil [66], for example, suggest that low Air Quality Index scores within stock exchanges may affect mood and risk aversion, thus resulting in lower stock returns. Fist, Black and Brunner [10] note that improvements to indoor environmental quality has a strong effect on workplace productivity and health, estimating a potential annual gain of \$20 billion from improvements in office buildings in the United States.

#### **6. Contemporary Approaches and Benefits of Mitigating Malodors**

Efforts to protect the public from the adverse effects of outdoor malodors take the form of regulations in many jurisdictions. Regulations include concentration or exposure limits if the odors are produced by specific target pollutants, nuisance or annoyance laws and property setbacks. The odor impact criteria established by such regulations are most commonly based on field olfactometry-based concentration measurements, although instrumental concentration measurements or air dispersion models are also used [67].

In order to comply with odor regulations and to promote good relations with neighboring households, some facilities may install technology to control odors at the source. Control strategies include oxidation, adsorption, chemical reaction, chemical scrubbing, biofiltration/bioremediation and other methods [68].

To help households control indoor odors, product manufacturers often employ some of the same technical strategies used industrially to control odors. These include air filters and filter media, oxidizers, absorbents/adsorbents, surface and air sprays, and a variety of volatile ingredient diffusers. Air filtration to remove odors may be achieved with filters attached to heating, ventilation and air conditioning (HVAC) units or stand-alone filtering units. Such filters may utilize activated carbon or zeolite adsorbents, photocatalytic oxidants such as metal oxides (for example, patents US 8911670, US 8038935), or odor-reactive chemistry such as metallic salts or amine polymers (for example, patent US 4892719).

Household consumer goods products designed to eliminate household and automobile odors include air fresheners, pump and spray aerosols and diffusers. Such products may contain technologies designed to: capture or alter the molecular structure of VOC responsible for the underlying malodor; prevent perception of the malodorous VOC (MOVOC) by the olfactory system; and/or mask MOVOC via fragranced ingredients. Technologies used in air freshening sprays and diffusers that are designed to capture or alter specific types of malodor molecules are summarized in (Table 2). Spray products may utilize one or a variety of such technologies to eliminate the molecular source(s) and/or perception of MOVOC.


**Table 2.** Malodor classification and patented technologies that can be used in air fresheners to mitigate common indoor malodors.

One such technology approach to mitigate indoor malodors is the use of cyclodextrin (CD) or cyclodextrin derivatives to trap MOVOC by complexation. Cyclodextrin has a macro-ring structure consisting of glucopyranose units. It is produced naturally by bacteria including *Bacillus macerana* and *Bacillus circulans*, and is made industrially in bioreactors utilizing engineered glucosyl transferase enzymes [81]. The cavity of the cyclodextrin ring is apolar, so that less polar MOVOC readily displace water and become "trapped" upon interaction with aqueous cyclodextrin. Once complexed, the volatility of the MOVOC is significantly reduced and the malodors remain trapped in the CD cavity as long as the complex stays dry [69,82]. Patent documents indicate that consumer product companies make use of cyclodextrin technology in spray air freshening and other consumer products (for example, patents US 5760475, US 6077318, US 6248135 and US 6451065).

Spray air freshening products may also utilize pH buffers to neutralize acid or basic odors and convert them to non-volatile salts. Acidic odors include short chain fatty acids such as isovaleric acid, heptanoic acid and basic odors include amines such as ammonia, butyl amine, and trimethyl amine. Both types of neutralizable MOVOC are constituents of household odors such as food waste odors, and human odors [16]. Buffer systems used in spray air freshening products to neutralize odors may include for example, citrate or carbonate buffers. Neutralization of acid and amine odors to pH in the range of 5–8 by pH buffering converts these MOVOC to non-volatile salts, reducing or eliminating the odor [83].

Enzyme inhibitors may be used in consumer products, including air freshening products, to prevent production of odorous metabolites (patent US 9200269). For example, urease inhibitors and β-glucuronidase inhibitors have been described to prevent the formation MOVOC from urine by microorganisms on fibrous consumer products [84].

Unsaturated aldehydes are MOVOC components of household odors that are derived from the oxidation of skin oils or from oxidation of lipids during cooking [16,85,86]. Amine-functional polymers are known to bind with and capture aldehydes (including formaldehyde) through the formation of imine bonds [87,88], and have been used in air freshening products to bind with odors (patent US 9273427).

Additional technologies used in air freshening sprays include anti-microbial agents such as quaternary ammonium compounds to eliminate odor-causing microbes, which use salts of transition metals, particularly zinc and copper to complex with odors (for example, patents US 5783544, US 6503413), and oxidizing agents such as chloramine (patent US 6743420) that eliminate MOVOC through both antimicrobial and oxidative mechanisms.

Diffusion-type products, like heated or unheated fragrance diffusers, may typically contain reactive materials such as carbonyl compounds designed to react with nucleophilic or electrophilic malodorous molecules such as amines (for example, patents US 8992889, US 5795566, US 7998403) to form covalently bonded, non-odorous products.

Technologies designed to prevent the olfactory perception of malodors based on mechanisms such as olfactory receptor antagonism have also been explored by consumer product companies (for example, patents EP 2812316, US 9526680, US 9254248). Such approaches target specific olfactory receptors known to be activated by malodorous agonists with antagonistic agents to block activation of these receptors by the malodor.

Consumer products designed to control malodor often, but not always, contain fragrance in addition to the technologies described above, or may contain fragrance without additional technology. Fragrance can mitigate malodors by masking their smell. The mechanism by which fragrances mask malodors is not well understood and may be achieved through a combination of signal interference (such as by receptor antagonism as discussed above) and through top-down processing effects (e.g., blending malodor with other odors to create perception of a new, non-malodorous aroma). Additionally, as noted above, some fragrances may contain reactive materials, such as carbonyl compounds designed to react with nucleophilic or electrophilic malodorous molecules. Pleasant fragrances have also been shown to have beneficial effects by increasing positive emotions, decreasing negative mood states and reducing indices of stress [89,90]. It is postulated that fragrances exert these effects through emotional learning, conscious perception and belief/expectation [91].

While seeking solutions to mitigate malodors, consumers and regulators must balance the economic, environmental and health costs of indoor malodors against the benefits delivered by the odor mitigating approaches. Companies that manufacture odor control technologies that emit fragrance or odor mitigating molecules into the air follow safety assessment paradigms that are widely recognized to ensure consumer safety when used according to label instructions. These assessments are aligned with the process outlined by EU Scientific Committee on Consumer Safety and are based on an understanding of both the inherent hazards of any materials in a product formulation as well as the level of exposure to those materials based on usage scenarios including extreme consumer usage [76,92]. In addition, the Research Institute for Fragrance Materials (RIFM) has published extensive industry guidance for conducting safety assessments of fragrance ingredients [93]. A 2007 US Environmental Protection Agency (EPA) review found that 0.23% of reported air freshener exposures involved an adverse reaction and that the number of reported exposure incidents for air fresheners was relatively small when compared to the reported exposure incidents for other product categories [94].

Household consumer products designed to eliminate odors are widely used by consumers in the United States, with 75.9% of US households purchasing an air care product as of March 2019, according to Nielsen HomeScan panel data [95]. Air care products are broadly available at retail outlets at relatively low cost. Buying rates of air care products are highest in households with annual incomes less than \$20,000 [96]. This may be due in part because lower-income households are disproportionately affected by environmental odors, odors arising from crowded conditions, and by economic limitations on their ability to deal with odor sources, such as those associated with sub-standard housing.

Despite the potential negative effects of malodors and the widespread use of consumer products designed to eliminate odors, the health and quality-of-life benefits of the use of such consumer products has not been widely studied. A review of published literature on the health impacts of using air cleaning devices was recently completed by Kelly and Fussell [97]. The studies reviewed focused mostly on indoor air cleaning devices that reduced particle and VOC concentrations by using filters, adsorbents, oxidative technologies or combinations thereof. The studies generally showed no or low levels of improvement in the health outcomes measured for households with good ambient air quality and modest improvements for households with very poor ambient air quality. However, none of these studies, and few other published studies, have specifically examined the impact of indoor malodor reduction on health outcomes such as cognition, mood, and stress levels, among others.

It may be inferred that eliminating the perception of malodor can reduce psychological effects of malodors, such as the feeling of a lack of control [41,44,47]. While studies have shown that people with problem-oriented coping strategies experience more stress and stress-related symptoms due to malodor exposure [52], air care and cleaning technologies offer a solution that allows people with problem-oriented coping styles to directly address the problems caused by malodors. Air care products designed to eliminate malodors can provide a more widely affordable solution compared to more costly alternatives such as home filtration systems, especially for low-income households who are economically unable to purchase such systems, replace malodorous household structures or items, or relocate away from substandard housing or industrial sources of malodor.
