Air Pollution Exposure and Olfactory Health: A Systematic Review

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Systematic Review

Air Pollution Exposure and Olfactory Health: A Systematic Review

https://doi.org/10.21203/rs.3.rs-4329122/v1

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Exposure to air pollution can affect the olfactory system, causing disorders such as anosmia (partial or total loss of smell) and hypogeusia (reduced ability to taste). The objective of this study is to systematically review air pollution exposure and associated olfactory health disorders. The systematic review included air pollutant types, types of exposure, testing methods, and study limitations. Specific keywords related to air pollution and olfactory and/or gustatory functions were employed to search electronic databases (PubMed, Google Scholar, MEDLINE, Highwire, ResearchGate, and the Cochrane Library) for studies and reviews on exposure to air pollution that assess and measure smell and taste and published up to the year 2021. Non-English studies, studies on animals, plants, and exposure to pollutants other than air pollutants were excluded. Out of 1,100 identified studies, only 52 studies met the selection criteria. Forty-nine studies were related to olfactory health (sense of smell) associated with air pollution exposure, and three studies were related to gustatory health (sense of taste). Most studies reviewed had a small sample size and were subject to substantial confounding, making it implausible to determine a significant association between air pollution exposure and olfactory health. The review shows the study limitations and gaps that should be considered in future research related to olfactory/gustatory health and air pollution. To our knowledge, this is the first systematic review of the olfactory health studies related to air pollution exposure.

Cognitive Neuroscience

Toxicology

Epidemiology

Air pollution

Olfactory

Gustatory

Anosmia

Air pollution is a leading risk factor in the global environmental burden of disease. While much of the previous work on air pollution has focused on cardio-respiratory health effects, emerging evidence suggests linkage to neurological impairments and increased risk of dementia [1–3]. Within the neurological system, humans have three sensory systems that can detect chemicals in the environment: namely, the olfactory system for odors (i.e., the nose and the mouth); the gustatory system for taste; and the trigeminal chemosensory system for the sense of irritation in the skin or mucus membranes of the eyes, nose, and mouth [4]. Air pollutants can reach and harm the chemosensory receptors [3] in the nose and mouth through inhalation [5], and the blood through translocation from the lungs or ingestion of contaminated water and food [6]. Although the exact mechanisms underlying the neurological effects of air pollution remain unclear, recent evidence points to common pathways including inflammation and oxidative stress [7]. There has been growing interest in the neurological impact of air pollution through studying the olfactory (smell) and gustation (taste) functions.

Air pollutants may directly harm the olfactory mucosa through cytotoxic effects and DNA damage, often resulting in squamous metaplasia of nasal tissue [8]. Particles that reach the olfactory mucosa may be translocated to the olfactory bulb, where they can cause direct cytotoxicity or provoke inflammation and cellular stress response [8]. As these damages accumulate over time, individuals exposed to air pollution may be at greater risk of developing hyposmia or anosmia (i.e., the partial or total loss of the sense of smell) [8], which has been associated with increased mortality in the elderly [9–11] as well as elevated risks of injuries; for instance, anosmatic individuals cannot detect hazardous smells (e.g., gas leaks) [12, 13]. Furthermore, hyposmia and anosmia are among the earliest signs of major neurological diseases, including Alzheimer’s, Idiopathic Parkinson’s, and Huntington’s diseases [14]. An impaired sense of smell has also been associated with depression and anxiety [15]. An impaired sense of taste can weaken an individual’s appetite and nutritional state [16]. As smell and taste are connected [13, 16], impairment in the sense of smell can also affect the taste, resulting in a preference for more robust flavors, especially salty and fatty food, and thus increasing the risk of obesity [15].

Although existing studies on the impact of air pollution on the sense of smell and taste have adopted a wide range of assessment methods, to our knowledge there has been no comprehensive or systematic review of the olfactory health studies related to air pollution exposure. The heterogeneity of the assessment methods used, compounded by the lack of systematic evaluation across methods, renders direct comparison and synthesis of results from different studies challenging. Therefore, the objective of this study is twofold: (i) to conduct a systematic review of the existing studies on the association between air pollution exposure and olfactory health, and (ii) to critically compare the different methods of olfactory health assessment and facilitate more informed decisions in choosing the appropriate method in future studies.

2.1. Data sources and searches

We searched the electronic databases MEDLINE, PubMed, Google Scholar, ResearchGate, and the Cochrane Library for full-text, peer-reviewed articles published in English up to July 8, 2021, which assessed the associations between air pollution exposure and olfactory health. We performed the searches by combining the pre-specified keywords (“air pollution effect on smell / tests”, “personal / occupational / exposure to air pollution”, “industrial airborne chemicals”, “exposure to ambient air pollution”, “olfactory impairment / dysfunction and air pollution”, “smell / taste / anosmia / hypogeusia / hyposmia / ageusia”) using the “AND” and “OR” Boolean operators. In addition to the database searches, we screened the bibliography of previous reviews and identified further relevant studies.

2.2. Study selection and inclusion/exclusion criteria

Titles and abstracts of potentially eligible studies were screened, followed by a full-text review of each article. The exclusion criteria were: (i) non-English paper, (ii) not related to air pollution, (iii) not related to smell/taste function, and (iv) in-vivo or in-vitro studies.

2.3. Data extraction and quality assessment of studies

Information was extracted from the publications using a standard data extraction form, which recorded the first author, year of publication, study design, location, sample size, characteristics of participants, and the test methods used.

A total of 1,100 studies were identified. After removing 341 duplicates, the titles, and abstracts of 759 studies were screened. Following a full-text review of 241 studies, 189 studies were excluded (Fig. 1). Ultimately, 52 articles were found to have used standardized tests to measure olfactory and/or gustatory functions. However, only three of these related to taste (two of which measured both smell and taste) (Fig. 1).

3.1. Air pollution and associated olfactory health

We identified a total of 52 air pollution studies associated with olfactory/gustatory health, of which 49 studies were related to olfactory, and only three were related to gustatory. The systematic review studies were arranged by the testing methods (Table 1). Broadly speaking, there are three main approaches that assess the olfactory health: a) odor threshold, which is a non-semantic smell test [17] measuring the lowest concentration of odor that can be sensed; b) odor identification, in which the subject names a specific odor based on their knowledge and semantic memory [18]; and c) odor discrimination, which is another non-semantic smell test [17] that assesses the ability to distinguish and detect the differences between different odor molecules [17, 19] when exposed to complex mixtures of more than two odorants [17].

3.1.1. Odor threshold tests

There were a total of twenty-seven studies that used the odor threshold method. There were a large number of test types of odor thresholds. Most studies (81%) found impaired olfactory function using the odor threshold method, but five failed to find any statistically significant differences in olfactory function between the exposed subjects and the controls [20–24]. Nineteen studies measured the changes in olfactory function due to occupational exposure to air pollution (e.g., metals and volatile organic compounds VOCs), among which 16 assessed the long-term exposure. Twelve studies used both the odor threshold test and the odor identification test [24–33], and three studies found no decline in the olfactory function measured by either test type (25%) [22–24]. Many studies assessed participants’ exposure to volatile organic compounds (VOCs) (e.g., phenyl-ethyl alcohol, n-butanol, styrene, and formaldehyde), and these tests tend to have good reliability and validity. Other studies assessed long-term exposure to heavy metal fumes (cadmium, manganese, chromium).

3.1.2. Odor identification tests

There were thirty-six studies that used the odor identification test method, making it the most popular olfactory test method. Twenty-six studies reported decreased olfactory function (74%), whereas nine studies found no effect [24, 34–41]. Twenty studies assessed the olfactory effects of occupational exposure (18 out of 20 long-term effects), and the remaining assessed the effect of non-occupational exposure [29–31, 38, 40–50].

3.1.3. Odor discrimination tests

Only three olfactory-related air pollution studies used the odor discrimination olfactory test method [29–30, 33]. These three studies assessed air pollution and associated olfactory health using all three testing methods (odor threshold, odor discrimination, odor identification). Two of these studies evaluated the olfactory effects of non-occupational exposure to ambient air [29, 30]. In contrast, the remaining study evaluated the long-term occupational exposure for acid, metal, and solvent pollutants [33]. Two studies were based on the Sniffin’ stick test type [30, 33].

In total, fifty-two studies were conducted to determine the association between air pollution exposure and olfactory health. The testing methods were as follows: 27 odor threshold, 36 odor identification, and three odor discrimination (some studies used more than one method) [17, 51]. Other olfactory tests that are not mentioned in Table 1 can be used effectively to measure the sense of smell including the snap and sniff threshold test [11, 52–53], olfactory event-related potentials (OERPs), and positron emission tomography (PET) [13].

3.2. Air pollution and associated gustatory health

There are only three studies that assessed air pollution association with gustatory health using three testing methods: a) the Börstein gustometry method, b) a tongue tip test (using quinine and sodium chloride), and c) brain-computer interface electroencephalography. Two of these studies assessed non-occupational exposure, and one study assessed occupational long-term exposure. All the three studies had a small sample size and did not adequately address the confounding factors (Table 1).

This paper summarized air pollution exposure studies and associated olfactory and gustatory health. Olfactory health studies were grouped into three main categories: odor threshold, odor identification, and odor discrimination. The most common olfactory testing method is odor identification, specifically the University of Pennsylvania Smell Identification Test (UPSIT) and Sniffin’ Sticks test. UPSIT is the most commonly used test in the United States, and it has 32 versions and can produce a reliable, validated, and culturally appropriate olfactory test [54]. The Sniffin’ Sticks Test is commonly used in Europe and is cheaper to use and has been properly validated [55]. To assess olfactory health in response to air pollution effectively, it is advisable to use the three olfactory test methods. It is also essential to develop a more robust and universal test to assess olfactory functions for the clinical management of olfactory dysfunction; for instance, an effective biomarker to predict different neurodegenerative diseases (i.e., Alzheimer's and Parkinson's diseases).

There are only three studies that associated air pollution exposure with gustatory health. The three studies used dripping solutions on the tongue and self-applied tests with taste strips. These taste tests are widely used in the paper-impregnated form and are easy to use by impregnating paper tapes with the taste solutions at appropriate concentrations [56].

Gustatory health deficit (loss of taste) can be masked by olfactory health dysfunction (loss of smell) [13,16]. Breathing mostly through the nose can be a greater risk to the olfactory system (R). Findings should be interpreted with caution when subjects have pre-existing health conditions that can affect the senses (i.e., vitamin D deficiency [57,58] or brain injury [59]).

Some air pollutants have different chemical toxicities in the olfactory/gustatory system. For instance, formaldehyde is a pungent irritating gas and very soluble in water and irritates the mucous membranes in the nose and the upper respiratory tract. Selenium and tellurium are present in metal oxide fumes and are associated with "garlic breath." Hydrogen sulfide causes olfactory nerve paralysis at higher concentrations. The late effects of nickel inhalation can cause nasal sinuses. Heavy exposure to vanadium metal dust can result in green discoloration of the tongue. Cadmium is a metal of significant health concern and common in electroplating use; cadmium fumes were shown to irritate the respiratory tract and cause delayed anosmia.

The systematic-review studies present confounding factors associated with olfactory health in response to air pollution exposure. Genetic factors have an essential effect on the ability to detect odors [60]. Responses to air pollutants are likely to be affected by genetic variations [61,62]. There are also gender differences associated with olfactory response to air pollution. Women tend to discriminate odor differences better than men [11,63-64]. Age can also substantially influence on odor response to air pollution, especially for age groups 65 and above. Age-related olfactory sensory loss may confound or mask the impact of air pollution [65]. Cigarette smoking can impair olfactory function, even in those who have quit smoking [66]. Studies showed that alcohol, certain medications, hunger, and hormonal effects can impact the olfactory function [13]. Environmental and occupational exposure to harmful chemicals, as well as residential characteristics (e.g., moldy homes), may also affect the olfactory function [26,35,46,49,67].

This study identified 1,100 studies related to olfactory health, of which 52 studies were systematically reviewed using various criteria, including olfactory health testing method, test type, exposure type, pollutant type, and confounding effects. Most studies assessed long-term occupational exposure to various pollutants. The systematically reviewed studies had a small sample size and confounding limitations and therefore provide inconclusive evidence of the association between air pollution exposure and olfactory health.

Author contribution statement

Maryam Shehab and Xi Xia conducted the review and prepared the tables and figures. Maryam Shehab, Olga-Ioanna Kalantzi, Olga S. Arvaniti, Xi Xia, Ka Hung Chan, and Hakan Tekeli wrote the first draft of the manuscript. Maryam Shehab, Ka Hung Chan, Ali Al-Hemoud, Kin Bong Hubert Lam, Janvier Gasana, Hakan Tekeli, Olga-Ioanna Kalantzi, and Olga S. Arvaniti reviewed and edited the manuscript.

Declaration of interest’s statement

The authors declare no conflict of interest.

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Table 1 is available in the Supplementary Files section

The authors declare no competing interests.

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Table 1. Studies of air pollution exposure and associated olfactory-gustatory health (1961 – 2021).

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Air Pollution Exposure and Olfactory Health: A Systematic Review

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Abstract

Figures

1. Introduction

2. Methodology

2.1. Data sources and searches

2.2. Study selection and inclusion/exclusion criteria

2.3. Data extraction and quality assessment of studies

3. Results

3.1. Air pollution and associated olfactory health

3.1.1. Odor threshold tests

3.1.2. Odor identification tests

3.1.3. Odor discrimination tests

3.2. Air pollution and associated gustatory health

4. Discussion

Conclusions

Declaration

References

Table

Additional Declarations

Supplementary Files

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