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Analytical and Toxicological Evaluation of Flavor Chemicals in Electronic www.nature.com/scientificreports OPEN Analytical and toxicological evaluation of favor chemicals in electronic cigarette refll fuids Received: 26 February 2018 Rachel Z. Behar1,2,3, Wentai Luo4, Kevin J. McWhirter4, James F. Pankow4 & Prue Talbot2,3 Accepted: 19 April 2018 Thousands of electronic cigarette refll fuids are commercially available. The concentrations of nicotine Published: xx xx xxxx and the solvents, but not the favor chemicals, are often disclosed on product labels. The purpose of this study was to identify and quantify favor chemicals in 39 commercial refll fuids that were previously evaluated for toxicity. Twelve favor chemicals were identifed with concentrations ≥1 mg/ml: cinnamaldehyde, menthol, benzyl alcohol, vanillin, eugenol, p-anisaldehyde, ethyl cinnamate, maltol, ethyl maltol, triacetin, benzaldehyde, and menthone. Transfer of these favor chemicals into aerosols made at 3V and 5V was efcient (mean transfer = 98%). We produced lab-made refll fuids containing authentic standards of each favor chemical and analyzed the toxicity of their aerosols produced at 3V and 5V using a tank Box Mod device. Over 50% of the refll fuids in our sample contained high concentrations of favor chemicals that transferred efciently to aerosols at concentrations that produce cytotoxicity. When tested with two types of human lung cells, the aerosols made at 5V were generally more toxic than those made at 3V. These data will be valuable for consumers, physicians, public health ofcials, and regulatory agencies when discussing potential health concerns relating to favor chemicals in electronic cigarette products. In 2014, more than 7,000 electronic cigarette (EC) refll fuid products with unique favor names were commer- cially available online and from local shops, and the number of products continues to grow1. In a study of 30 refll fuids, total favor chemical concentrations ranged from 10–40 mg/ml2. Even though many of these favor chemicals are generally regarded as safe (GRAS) for ingestion, the Flavors & Extract Manufacturers Association (FEMA) has cautioned that their GRAS designation does not extend to inhalation3. It is important to gain a better understanding of which favor chemicals are predominant ingredients in refll fuids, their concentrations, and the potential health efects that EC consumers may experience when inhaling high concentrations of favor chemicals. As an initial step to identify refll fuids that may have adverse health efects, our laboratory evaluated the cytotoxicity of a library of refll fuids with a broad range of favors which included buttery/creamy, minty, sweet/ candy, fruit, tobacco and cinnamon/spiced4. About a third of these products were highly cytotoxic to human pulmonary fbroblasts (hPF) and two types of stem cells. However, a cinnamon-favored refll fuid was the most potent across all cell types. Cinnamaldehyde was subsequently identifed as the dominant favor chemical in a small library of commercial cinnamon-favored refll fuids, and its concentration was directly correlated with its cytotoxicity in the MTT assay5. Te cytotoxicity of the refll fuids and aerosols made from the products in our original screen4 was then compared across brands6. 74% of the refll fuid cytotoxicity data accurately predicted the toxicity of the corre- sponding aerosols. Te “creamy/buttery”-favored refll fuids led to more cytotoxic aerosols than did fuids in other favor classes, again suggesting that favor chemicals are diferentially important in determining cytotoxicity of EC products. Te above studies have demonstrated a need for further identifcation and characterization of the potency of favor chemicals in EC refll fuids. Te current study evaluated the favor chemicals and their cytotoxicity using the two refll fuid libraries from our previous studies4,5, which included 39 commercial refll fuids and 1Cell Molecular and Developmental Biology Graduate Program, University of California, Riverside, CA, 92521, United States. 2UCR Stem Cell Center, University of California, Riverside, CA, 92521, United States. 3Department of Molecular, Cell and Systems Biology, University of California, Riverside, CA, 92521, United States. 4Department of Civil and Environmental Engineering, Portland State University, PO Box 751, Portland, OR, 97207-0751, United States. Correspondence and requests for materials should be addressed to P.T. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:8288 | DOI:10.1038/s41598-018-25575-6 1 www.nature.com/scientificreports/ Figure 1. Heat map of favor chemicals identifed and quantifed in 45 commercial refll fuids. Chemicals (y- axis) are classifed by toxicity and ordered within each toxicity bracket from highest to lowest lethal dose based on rat oral toxicity data. Refll fuids (x-axis) are represented by their inventory number and ranked with the lef having the highest concentration of total favor chemicals and the right having the lowest. Te color gradient provides information on the concentration of each chemical. Red asterisks represent the 12 favor chemicals that were ≥1 mg/ml in at least one product. six duplicate bottles (45 products total). We specifcally: (1) identifed the favor chemicals in each product, (2) produced “lab-made” refll fuids with authentic standards of those favor chemicals present in concentrations ≥1 mg/ml, (3) determined how much of each favor chemical is transferred from the lab-made refll fuids into aerosols made at high and low voltages, (4) examined the cytotoxicity of these aerosols using human lung cells, and (5) identifed reaction products formed due to the aerosolization process. Results Identifcation of favor chemicals in 39 refll fuids and selected duplicates. Fify-two of the 92 favor chemicals on the GC/MS target analyte list used were identifed and quantifed in the combined library of 45 refll fuids (Fig. 1)4,5. Te total concentration of the favor chemicals in these products ranged from 0.141 to 179 mg/ml. Te chemicals in Fig. 1 are arranged on the y-axis based on IC50 (highest to lowest) from rat oral toxicity values found in online compilations7. Products on the x-axis are identifed by our laboratory inventory number (Supplemental Table 1) and are arranged from highest (lef) to lowest total favor chemical concentra- tion. Tirteen chemicals were identifed as dominant favor chemicals, being found at concentrations ≥1 mg/ml in at least one of the products and are identifed in Fig. 1 with a red asterisk. Te 13th dominant favor chemical, benzaldehyde PG (propylene glycol) acetal (13.8 mg/ml) was not available commercially for use as an authentic standard and was not examined in this work. When arranged by toxicity classifcation according to rat oral data7 (y-axis of Fig. 1), eight of these 12 favor chemicals were in the harmful bracket, three were in the irritant bracket, and one was not classifed according to oral rat toxicity data7 (Fig. 1). Tese dominant favor chemicals include mainly minty, sweet, fruity, and creamy favors (Table 1). Te highest concentrations for the 12 dominant favor chemicals found in the refll fuids were: cinnamal- dehyde (155 mg/ml), menthol (84 mg/ml), benzyl alcohol (39 mg/ml), vanillin (31 mg/ml), eugenol (12 mg/ml), p-anisaldehyde (9.0 mg/ml), ethyl cinnamate (8.5 mg/ml), maltol (4.9 mg/ml), ethyl maltol (4.2 mg/ml), triacetin (2.8 mg/ml), benzaldehyde (2.5 mg/ml), and menthone (1.4 mg/ml). Frequency of occurrence of the 12 dominant chemicals. Te frequency of occurrence and the con- centration of each dominant favor chemical from the GC/MS commercial refll fuid screen is shown in Figs 2 and 3. Duplicate bottles were not incorporated into the frequency calculation, but were included in the graphs to determine whether duplicate products were similar to each other. Six of the 12 dominant favor chemicals were present less frequently (5–12 products) (Fig. 2). Tis included ethyl cinnamate in four products (10%), triacetin in fve products (13%), eugenol in six products (15%), benzyl alcohol in seven products (18%), maltol in seven products (18%), and benzaldehyde in 12 products (31%). Te other six dominant favor chemicals were found more frequently (16–31 products) (Fig. 3). Figure 3 shows menthone in 16 products (41%), p-anisaldehyde in 17 products (44%), menthol in 17 products (44%), cinnamaldehyde in 20 products (51%), vanillin in 22 products (56%), and ethyl maltol in 31 products (80%). Generally, for Figs 2 and 3, the concentrations of favor chemicals were similar in the duplicate bottles. Flavor chemical aerosolization transfer efciency. Aerosols that were captured in liquids and used for analytical chemistry or cytotoxicity experiments will be referred to as “aerosols”. GC/MS was used to identify and quantify favor chemicals in aerosols produced at 3V (volts)/4.3 watts or 5V/11.9 watts from lab-made refll fuids that contained 80% propylene glycol and one of the 12 dominant favor chemicals. For these analyses, the GC/MS target list included 178 favor chemicals. Generally, for aerosols produced at 3V and 5V, the refll fuid to aerosol SCIENTIFIC REPORTS | (2018) 8:8288 | DOI:10.1038/s41598-018-25575-6 2 www.nature.com/scientificreports/ A549 <70% of CN hPF <70% of CN Identifed Chemical Name CAS # Flavor Category Conc. (mg/ml) 3V 5V 3V 5V Cinnamaldehyde 14371-10-9 Cinnamon/Spicy 155 Yes Yes Yes Yes Menthol 2216-51-5 Minty/Cooling/Fresh 84 No Yes Yes Yes Benzyl Alcohol 100-51-6 Fruity 39 Yes Yes Yes Yes Vanillin 121-33-5 Vanilla/Sweet/Creamy 31 No Yes Yes Yes Eugenol 97-53-0 Sweet/Warm Spiced 12 No Yes Yes Yes p-Anisaldehyde 123-11-5 Creamy/Powdery/Vanilla 9.0 No Yes No Yes Ethyl Cinnamate 103-36-6 Balsamic/Fruity/Berry 8.5 No Yes Yes Yes Maltol 118-71-8 Sweet/Cotton Candy/Caramellic 4.9 No Yes Yes Yes Ethyl Maltol 4940-11-8 Sweet/Cotton Candy/Caramellic 4.2 No Yes Yes Yes Triacetin 102-76-1 Creamy 2.8 No Yes No Yes Benzaldehyde 100-52-7 Sweet/Cherry/Almond 2.5 No Yes No Yes Menthone 14073-97-3 Minty/Cooling/Fresh 1.4 No Yes No No Propylene Glycol 57-55-6 Sweet — No Yes No Yes Table 1.
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