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Abstract

Background

Variation in alternative tobacco product (ATP) constituents, heating potential, and consumer behaviors have made it difficult to characterize their health risks. To date, most toxicity studies of ATPs have used established cigarette endpoints to inform study design. Furthermore, to assess where ATPs fall on the tobacco harm continuum, with cigarettes representing maximum potential risk, studies have tended to compare the relative biological responses to ATPs against those due to cigarettes.

Objectives

1) To characterize the exhalation profiles of two popular ATPs: electronic cigarettes (e-cigarettes) and hookah waterpipes (hookah) and 2) to determine if ATP exhalation patterns were representative of cigarette exhalation patterns.

Methods

Exhalation patterns were recorded (mouth only, nose only, or both mouth and nose) among individuals observed in the New York City tri-state area using a recognizable tobacco product (cigarette, e-cigarette, or hookah). Cigarette smokers and e-cigarette vapers were observed on city streets; water-pipe smokers were observed inside Manhattan hookah bars.

Results

E-cigarette vapers practiced exclusive nasal exhalation at far higher rates than did cigarette smokers (19.5% vs 4.9%). Among vapers, e-cigarette device type was also significantly associated with exhalation profile. Overall, cigarette smokers exhaled from their nose approximately half to one-third as often as ATP users (hookah and e-cigarettes, respectively).

Conclusions

Nasal exhalation of tobacco emissions appears to be a shared characteristic across several types of ATPs. It is therefore plausible that ATP-specific consumer behaviors may foster unique upper respiratory health consequences that have not been observed in smokers. Thus, product-specific behaviors should inform the prioritization of biological endpoints used in studies evaluating ATP toxicity and health effects.

Keywords

alternative tobacco products electronic cigarettes hookah vaping

Introduction

Since the introduction of electronic cigarettes (e-cigarettes) to the US market 15 years ago, vaping rates have surged exponentially,^1,2 with current usage rates among US adults exceeding 1 in 20.³ Separately, waterpipe hookah tobacco (hookah) use continues to gain popularity in the U.S.,⁴ with year-over-year ever use increasing by as much as 40%.⁵ The toxicological research needed to characterize the potential health risks associated with alternative tobacco products (ATPs), including e-cigarettes and hookah, has not kept pace with their growing popularity and use.^6–8 Not only do ATP constituents and toxicity profiles tend to differ from those of combustible tobacco cigarettes,^9–11 but consumer demographics and puff topographies also can vary by tobacco product.^12–15 Importantly, product-specific behaviors can affect health risk: Inhalation depth (a measure of how deeply into the lungs tobacco smoke is inhaled) is greater among cigarette smokers than persons who smoke other combustible tobacco products.^16–18 In fact, physicians have attributed increased incidence of chronic bronchitis in cigarette smokers to this cigarette-specific behavior for more than a century.^19,20

Several studies have implicated tobacco-smoke inhalation depth as an independent risk factor for lung and laryngeal cancers, independent of pack-years.^21–24 Separately, among combustible tobacco products, epidemiology studies have identified the strongest association between cigarettes and lung-cancer diagnoses.^16,25-27 Cigarette smokers who do not inhale tobacco smoke into their lungs, however, face a lower risk of lung cancer.^21,28 Hence, cigarette smoke inhaled more deeply may foster lung-cancer risk by increasing pulmonary exposure to—and deposition of—harmful tobacco-smoke toxicants.^29-31

Further differences in product-specific puff topographies (e.g., puff duration, volume, and velocity) have been shown to affect the resultant tobacco emissions and potentially influence associated health risks.^32,33 However, despite the fact that most ATPs, including e-cigarettes and hookah, contain chemicals that have been added to enhance odor/flavor,³⁴ little is known about how ATP-specific features, such as flavor, might impact their use and subsequent health risks. Research shows that taste is strongly influenced by retronasal olfaction,³⁵ which has been found to improve odorant identification and strengthen perceived flavor intensity.³⁶ Furthermore, several internet forums and news outlets have ascribed “retrohaling”—the practice of intentionally exhaling tobacco emissions from the nose to increase flavor intensity—as a feature common among various ATP users including cigar and hookah smokers and e-cigarette vapers.^37,38 Separately, the lungs have been posited to serve as a “sink” for odorants that could reinforce retrohaling of inhaled tobacco product emissions.³⁹ Together, these data suggest that ATP-specific breathing patterns could differentially affect respiratory exposures and any health risks associated with these products.

Given that product-specific behaviors (e.g., puff topographies) are well documented among consumers of combustible tobacco, we sought to determine whether product-specific retrohaling behaviors could be identified. We evaluated real-world product-specific behaviors of subjects in their naturalistic environment using tobacco products of choice at their discretion ad libitum (i.e., without being prompted). Of particular interest were retronasal exhalation patterns associated with two of the most popular, and commonly flavored, ATPs: e-cigarettes and hookahs.^40,41

Methods

From March 2018 through February 2019, researchers observed people using tobacco products. Exhalation patterns of cigarette smokers (n = 122) and e-cigarette vapers (n = 124) were observed on New York City streets. Water-pipe smoker (n = 96) exhalation patterns were observed inside Manhattan hookah bars. Binary categorization of e-cigarette devices as either pod-like or modular-tank formats (e.g., cig-a-like, vape-pen and clear-o-mizers vs box-mod, and sub-ohm atomizers, respectively) was assigned using commonly cited size and shape criteria.^42,43

To characterize consumer behaviors associated with distinct tobacco products, a disguised naturalistic observational approach was used. These data were collected by a team of tobacco-product researchers with prior experience identifying unique tobacco products and exhalation patterns discretely and accurately. Additionally, avoiding direct interaction with the subjects offered several experimental advantages: This methodology qualifies for IRB exemption, subject anonymity is maintained,⁴⁴ and observations would not bias subject behaviors.⁴⁵

Observations were limited to circumstances where product type and exhalation pattern could be visually confirmed; subjects were excluded from analysis when the facial source of exhaled smoke/aerosol was unclear or product type could not be verified. To limit risk of researchers being noticed or confronted, observation windows were limited to no more than 1 minute or 5 individual puffs; subjects commuting on foot were not followed for more than 1 block. To maintain discretion, researchers recorded observations on their phone; individual subject details were submitted to a centralized email for blinded quantification. The observational nature of this study precluded verification of a subject’s age.

Tobacco-exhalation profiles were characterized by exclusive exhalation (mouth or nose only) or dual exhalation (both mouth and nose). Dual exhalation was defined as either combined oral and nasal exhalation during the same puff or exclusive exhalation from the mouth and nose during different puffs (but in the same individual). Relative product-specific exhalation patterns were determined by calculating the percentage of individuals observed exhaling exclusively from either their mouth or nose, vs exhaling from both their mouth and nose. Visual confirmation of e-cigarette device type was used to further dichotomize vapers into modular-tank users (n = 60) or pod-like users (n = 64).

Pearson’s chi-squared tests⁴⁶ were run in STATA (StataCorp LLC, College Station, TX) to determine if overall exhalation patterns differed by gender (i.e., male vs female), tobacco product (i.e., cigarettes vs hookah vs e-cigarettes) or e-cigarette devices (i.e., modular vs pod-like). Significance was set at P ≤ .05. To identify which tobacco products were associated with different exhalation patterns (e.g., mouth only, nose only, or both mouth and nose), a two-tailed Z-test for two proportions was run, where cigarettes were the reference group for tobacco-product pairwise comparisons and modular tanks were the reference group for pairwise e-cigarette device comparisons (P ≤ .05). Analyses were conducted using the infrrr Difference in Proportions Hypothesis Test Calculator (https://www.infrrr.com/).

Results

A total of 341 people were observed using tobacco products: 122 cigarette smokers, 96 hookah smokers, and 123 e-cigarette vapers (Table 1). Subjects that outwardly presented as male accounted for at least two-thirds of all observed individuals, regardless of product used. Within e-cigarette users, roughly half used pod-like devices (52%). Irrespective of device style, females accounted for fewer than 25% of vapers.

Table 1.

Sex-specific exhalation patterns by product type (cigarette, hookah, and e-cigarette).

Tobacco Product/Subject Details			Exhalation Pattern
Product (N)	Subject Gender^a	N (%)	Dual^b N (%)	Oral^c N (%)	Nasal^c N (%)
Cigarette^d (122)	M	80 (65.6)	17 (21.2)	59 (73.8)	4 (5.0)
Cigarette^d (122)	F	42 (34.4)	4 (9.5)	36 (85.7)	2 (4.8)
Hookah^e (96)	M	65 (67.7)	34 (52.3)	31 (47.7)	0 (.0)
Hookah^e (96)	F	31 (32.3)	14 (45.2)	17 (54.8)	0 (.0)
E-cigarette^d,f (124)	M	97 (78.2)	40 (41.3)	35 (36.1)	22 (22.6)
E-cigarette^d,f (124)	F	27 (21.8)	13 (48.1)	12 (44.4)	2 (7.4)
Modular-Tank (60)	M	46 (76.7)	29 (63.0)	11 (24.0)	6 (13.0)
Modular-Tank (60)	F	14 (23.3)	8 (57.1)	5 (35.7)	1 (7.1)
Pod-like (64)	M	51 (79.7)	12 (23.5)	23 (45.1)	16 (31.4)
Pod-like (64)	F	13 (20.3)	5 (38.5)	7 (53.8)	1 (7.7)

^aDetermined by researcher (not verified by subject). M = male//F = female.

^bIndividual was observed exhaling from two facial orifices (oral and nasal).

^cIndividual was observed exhaling from a single orifice (oral or nasal).

^dObservations took place in public spaces (outdoors).

^eObservations took place in multiple hookah bars (indoors).

^fE-cigarettes include both modular-tank and pod-like devices.

Chi-squared analyses revealed that exhalation patterns did not differ significantly by gender (Table 1, statistics not shown). Regardless of tobacco product, exclusive mouth exhalation was more common than exclusive nose exhalation. However, proportion tests revealed that ATP users (both hookah and e-cigarette) practiced exclusive oral exhalation significantly less often than did cigarette smokers (Table 2, P < .001). Surprisingly, people vaping e-cigarettes practiced exclusive nasal exhalation at almost 4 times the rate of cigarette smokers (19.5% vs 4.9%, respectively, Figure 1). Interestingly, hookah smokers were never observed exclusively exhaling from their nose, although 50% did practice dual exhalation.

Table 2.

Two-sample exhalation proportion Z-scores by tobacco product type and e-cigarette device type.

Exhalation Pattern	vs. Cigarette Smoking
Hookah Smoking	Z-Score	P-value
Mouth only	4.42	.001
Nose only	2.51	.012
Dual (mouth + nose)	−5.38	<.001
Ever nose (dual + nose only)	−4.42	.001
E-Cigarette Vaping	Z-Score	P-value
Mouth only	7.15	<.001
Nose only	−3.50	.005
Dual (mouth + nose)	−4.82	<.001
Ever nose (dual + nose only)	−6.96	<.001
E-Cigarette Modular-Tank Device	vs. E-Cigarette pod-like device
	Z-Score	P-value
Mouth only	−2.91	.004
Nose Only^a	---	---
Dual (mouth + nose)	4.41	.001
Ever nose (dual + nose only)	2.74	<.001

P-values are bold when z-score was determined to be statistically different.

^ainsufficient sample size for test to run.

Figure 1.

Product-specific exhalation patterns. Venn diagrams of exhalation patterns of smokers (cigarette, n = 122, and hookah, n = 96) and vapers (e-cigarette, n = 123) observed in New York City. E-cigarette users were further stratified by device type: Modular-tank (mod, n = 59) or pod-like (pod, n = 64). Red boxes include individuals who had ever exhaled from their nose (e.g., mouth and nose + nose only), and these cumulative nasal exhalation percentages are shown in red. Chi-squared analyses revealed statistically significant differences between all tobacco products and between e-cig devices (*P ≤ .05).

Within e-cigarette users, device type was significantly associated with nasal exhalation patterns: Pod-like users were more than twice as likely to exclusively exhale from their nose as compared to individuals vaping modular-tank devices (26.6% vs 11.9%, respectively). However, approximately 40% more modular device users (Figure 1) were seen ever exhaling from their nose (cumulative proportion of dual and exclusive nasal exhalation, Table 2, P<.001). Notably, cigarette smokers exhaled out of their nose significantly less often than did either hookah smokers or e-cigarette vapers (22% compared to 50% and 62.6%, respectively, Figure 1).

Discussion

Here, we present the first evidence of ATP-specific aerosol exhalation patterns in which vapers and hookah users retronasally exhale ATP emissions more often than do cigarette smokers. ATP products associated with increased rates of retrohaling could increase the direct exposure of the upper respiratory tract (nose and sinuses) to ATP emissions, which may lead to unique health consequences in these tissues. For example, a recent study found increased levels of inflammatory cytokines in the nose of e-cigarette users and hookah smokers—a phenotype that was not present in the nose of cigarette smokers.⁴⁷ Therefore, these findings may have important implications for ATP toxicity and risk evaluations, as these behavioral differences could lead to--and potentially explain--novel product-specific health risks.

Additionally, e-cigarette device type appeared to influence consumer exhalation patterns, with modular-tank users practicing dual exhalation (i.e., both nose and mouth) 40% more frequently than individuals vaping pod-like devices. In fact, persons vaping modular-tank devices had the highest rates of dual exhalation of any group. This dual exhalation may relate to the fact that modular-tank e-cigarettes can generate larger aerosol volumes than pod-like devices,⁴⁸ so modular-tank vapers may need both their nose and mouth to facilitate exhalation of larger volumes of inhaled aerosols.⁴⁹ Importantly, the reduced coil resistance and higher wattages needed to generate those larger emissions has been found to enhance the toxicity of the resultant aerosol.^50-52 Thus, modular-tank users may be enhancing risks through more frequent nasal exposures to potentially larger volumes of more harmful chemicals.

The abundance of available ATP flavors found in vaping e-liquids and hookah shisha may partly explain the apparent preferential nasal exhalation among their users.⁵³ Another biological basis for the observed exhalation patterns could be the complex integration of olfactory and taste sensory networks.⁵⁴ Theoretically, nasal exhalation of flavored emissions should enhance how ATP consumers sense a product’s “flavor,” which in turn may enhance their overall product experience and potentially reinforce this behavior. Intriguingly, chewing tobacco has been shown to attenuate taste perception,⁵⁵ whereas individuals who smoke cigarettes consistently demonstrate impairments in olfaction, but not taste.^56,57 Taken together, these data suggest that the reduced olfaction commonly observed among cigarette smokers might explain why we observed so few practicing nasal exhalation.^57,58

Limitations

While exhalation of tobacco product emissions is not a routine metric, it did permit for the comparison of product-specific breathing patterns that could be observed visually and unbeknownst to research subjects—a vast improvement from classical inhalation research, which has relied heavily on self-reported product behaviors. Unfortunately, the observational nature of this study precluded our knowing the exact constituents of the ATPs used. Despite this experimental limitation, the novel ATP-specific exhalation profiles we observed suggest that the products themselves may be a significant predictor of consumer behavior, rather than intra-product differences (i.e., flavors, brands, or devices), as some have suggested.⁵⁹ If so, this would be consistent with the product-specific breathing patterns that have been observed between smokers of different types of combustible tobacco.^17,18

Final Remarks

Perhaps because of ATP’s potential to reduce tobacco harm, most ATP research has evaluated the health risks of ATPs against those of cigarettes.^60-63 However, as has been found with tobacco-smoke inhalation depth, differences in how tobacco products are used can confer different respiratory risks.^16,18 Limiting the scope of studies to established cigarette health endpoints may risk missing ATP-specific behaviors that might foster unique harms. Thus, we recommend that future toxicological of ATP respiratory risk consider the potential for retrohaling to disproportionately—and uniquely—impact upper-respiratory tissues. Designing studies that better reflect potential real-world exposures by honing experimental considerations and biological endpoints will improve our understanding of any health impacts from new and emerging ATPs and better inform clinical recommendations.

Footnotes

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study is supported by NIH/NHLBI (R01 HL139239-03) and NIH/NIEHS (R21 ES026996-02; T32ES007324).

ORCID iDs

Emma Karey, PhD

Kayla Farrell, MPH

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Exhalation of alternative tobacco product aerosols differs from cigarette smoke—and may lead to alternative health risks

Abstract

Background

Objectives

Methods

Results

Conclusions

Keywords

Introduction

Methods

Results

Discussion

Limitations

Final Remarks

Footnotes

Declaration of conflicting interests

Funding

ORCID iDs

References