Effects of E-Liquids and Their Aerosols on Biofilm Formation and Growth of Oral Commensal Streptococcal Communities: Effect of Cinnamon and Menthol Flavors
"> Figure 1
<p>Description of E-liquid and apparatus. The E-liquid (<b>A</b>) and apparatus (<b>B</b>) used to expose streptococcal bacteria to E-cigarette-generated aerosol ± flavors are shown. In (<b>B</b>), the (left) shows the Apollo ECIG batteries; the (middle) shows the Apollo blank cartridges; the (right) shows the peristaltic pump, Traceable<sup>TM</sup> controller, and exposure chamber. Note the Tygon S3<sup>®</sup> tubing running from the E-cigarette to the pump and finally to the exposure chamber.</p> "> Figure 2
<p>E-liquid treatments and live/dead stain. Viability of biofilm biomass exposed to BHI media alone (control) or BHI and 5% E-liquids ± 25% flavors. The medium is a 1:1 <span class="html-italic">v</span>/<span class="html-italic">v</span> mixture of BHI and distilled water. Representative confocal micrographs at 630× total magnification (XY); the white horizontal bars on the xy graphs indicate 20 µm. The Z-axis measures 8 to 10 µm in biofilm height (<b>A</b>). Quantification of percent live/dead biofilm biomass (<b>B</b>). Each bar represents the mean ± SEM (<span class="html-italic">n</span> = 4 to 6). Significance was determined using one-way ANOVA followed by a Bonferroni multiple comparison test. Green *** = <span class="html-italic">p</span> < 0.001 from live control and red *** = <span class="html-italic">p</span> < 0.001 from dead control.</p> "> Figure 3
<p>E-liquid treatments and hydrophobicity assay. Hydrophobicity, tested with n-hexane, after exposure of oral commensal streptococci to PG, VG, stock menthol, stock cinnamon flavors, E-liquid + 25% cinnamon, and E-liquid + 25% menthol. The control indicates baseline hydrophobicity for each of the bacterial species. Hydrophobicity is indexed by the reciprocal value of absorbance (595 nm) of the aqueous fraction, where an increase of 1/absorbance equates to an increase in hydrophobicity. Each bar represents the mean ± SEM (<span class="html-italic">n</span> = 6). Significance from the control was determined using one-way ANOVA followed by a Bonferroni multiple comparison test. * = <span class="html-italic">p</span> < 0.05, ** = <span class="html-italic">p</span> < 0.01, and *** = <span class="html-italic">p</span> < 0.001.</p> "> Figure 4
<p>Baseline single-species biofilm biomass. Average baseline (control) of crystal violet absorbance for single-species biofilms. Each bar represents the mean ± SEM (3 replicate experiments, <span class="html-italic">n</span> = 4 per replicate, total = 12).</p> "> Figure 5
<p>Aerosol-treated single-species biofilm biomass. Left-side graphs give a quantification of the oral commensal streptococcal biofilm biomass, as indexed by absorbance (595 nm) of crystal violet, after exposure to air or E-cigarette-generated aerosol ± flavors (menthol or cinnamon). Each point is the mean ± SEM (<span class="html-italic">n</span> = 11 to 12). Statistical significance was determined by two-way ANOVA with Bonferroni post hoc analysis comparing exposures of air to E-liquid ± flavors after 0, 15, 30, or 45 puffs. ** = <span class="html-italic">p</span> < 0.01, *** = <span class="html-italic">p</span> < 0.001. The right-side graphs display trend lines (slope) of the same data displayed in the left-side graphs.</p> "> Figure 6
<p>Aerosol-treated multispecies biofilm biomass. Quantitation of multispecies streptococcal biofilm biomass exposed to 45 puffs of air or E-cigarette-generated aerosol ± flavors (menthol or cinnamon), as indexed by absorbance of crystal violet before (<b>A</b>) and after (<b>B</b>) 24 h incubation. Each bar represents the mean ± SEM (3 replicate experiments, <span class="html-italic">n</span> = 5 per replicate, total <span class="html-italic">n</span> = 15). Statistical significance was determined by one-way ANOVA with Bonferroni post hoc analysis, where * = <span class="html-italic">p</span> < 0.05 and *** = <span class="html-italic">p</span> < 0.001 as compared to 0-puff control. The red line represents the average baseline absorbance reading for the 0-puff control.</p> "> Figure 7
<p>Aerosol-treated single-species biofilm microscopy and quantitation. Depiction of oral commensal single-species streptococcal biofilms using the DNA stain, SYTO 59 Red. (<b>A</b>) Representative biofilms are shown comparing 0-puff control for <span class="html-italic">S. gordonii</span>, <span class="html-italic">S. intermedius</span>, <span class="html-italic">S. mitis,</span> and <span class="html-italic">S. oralis</span> with 45 puffs of air, or E-cigarette-generated aerosol ± flavors. Each micrograph was photographed at 1000× total magnification (1920 × 1080 resolution) using a fluorescent microscope and converted to 8-bit black and white images (not shown). (<b>B</b>) The percentage of the biofilm biomass was calculated on the black and white images using ImageJ and is shown as % area of micrograph. Each bar represents the mean ± SEM (at least four random micrographs). The red line represents the average biofilm percentage of the 0-puff control.</p> "> Figure 8
<p>Aerosol-treated multispecies biofilm microscopy and quantitation. Depiction of oral multispecies (<span class="html-italic">S. gordonii</span>, <span class="html-italic">S. intermedius</span>, <span class="html-italic">S. mitis,</span> and <span class="html-italic">S. oralis</span>) streptococcal biofilms using the DNA stain, SYTO 59 Red. (<b>A</b>) Representative biofilms are shown comparing 0-puff control with 45 puffs of air, or E-cigarette-generated aerosol ± flavors. Each micrograph was photographed at 1000× total magnification (1920 × 1080 resolution) using a fluorescence microscope and converted to an 8-bit black and white image. (<b>B</b>) The percentage of the biofilm biomass (white area in A) was calculated using ImageJ. Each bar represents the mean ± SEM (<span class="html-italic">n</span> = 4). The red line represents the average biofilm percentage of the 0-puff control. RBG refers to red, blue, and green color images and B&W refers to black and white images.</p> "> Figure 9
<p>Aerosol-treated live/dead stain on multispecies biofilms. Percent viability of multispecies streptococcal biofilms exposed to 45 puffs of air or E-cigarette-generated aerosol ± flavors (menthol or cinnamon) before (<b>A</b>) and after (<b>B</b>) 24 h incubation. Each bar is the mean ± SEM (3 replicate experiments, <span class="html-italic">n</span> = 10 per replicate, total <span class="html-italic">n</span> = 30). Statistical significance was determined by one-way ANOVA with Bonferroni post hoc analysis where * = <span class="html-italic">p</span> < 0.05, ** = <span class="html-italic">p</span> < 0.01, and *** = <span class="html-italic">p</span> < 0.001 (comparing exposures of air to peroxide and E-cigarette-generated aerosols ± flavors). The red line represents the average baseline absorbance reading for the 0-puff control.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Reagents and Supplies
2.2. Bacterial Strains
2.3. Stock E-Liquids
2.4. Saliva Preparation
2.5. Streptococcal Biofilm Exposure to E-Liquids
2.6. Viability of Streptococcal Biofilm/Biomass after E-Liquid Exposure
2.7. Hydrophobicity of Streptococcal Bacteria
2.8. Streptococcal Biofilm/Biomass Exposure to E-Cigarette-Generated Aerosols
2.9. Crystal Violet Quantification of Streptococcal Biofilm Biomass after Aerosol Exposure
2.10. Fluorescent Microscopy of Streptococcal Biofilm/Biomass after Aerosol Exposure
2.11. Crystal Violet Quantification of Multispecies Streptococcal Biofilm Biomass Exposed to Aerosol before and after 24 h Incubation
2.12. Viability of Multispecies Streptococcal Biofilms Exposed to Aerosol before and after 24 h Incubation
2.13. Statistical Analysis
3. Results
3.1. Biofilm Biomass Viability after E-Liquid Exposure
3.2. Hydrophobicity Assay
3.3. Crystal Violet Quantification after Aerosol Exposure
3.4. Fluorescent Microscopy Analysis after Aerosol Exposure
3.5. Live–Dead Stain after Aerosol Exposure
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Glantz, S.A.; Bareham, D.W. E-Cigarettes: Use, Effects on Smoking, Risks, and Policy Implications. Annu. Rev. Public Health 2018, 39, 215–235. [Google Scholar] [CrossRef]
- Selekman, J. Vaping: It’s All a Smokescreen. Pediatr. Nurs. 2019, 45, 56. [Google Scholar] [CrossRef]
- Palazzolo, D. Electronic Cigarettes and Vaping: A New Challenge in Clinical Medicine and Public Health. A Literature Review. Front. Public Health 2013, 1, 56. [Google Scholar] [CrossRef] [PubMed]
- Famiglietti, A.; Memoli, J.W.; Khaitan, P.G. Are Electronic Cigarettes and Vaping Effective Tools for Smoking Cessation? Limited Evidence on Surgical Outcomes: A Narrative Review. J. Thorac. Dis. 2021, 13, 384–395. [Google Scholar] [CrossRef] [PubMed]
- Eaton, D.L.; Kwan, L.Y.; Stratton, K.; National Academies of Sciences, Engineering, and Medicine. E-Cigarette Devices, Uses, and Exposures. In Public Health Consequences of E-Cigarettes; National Academies Press: Washington, DC, USA, 2018. [Google Scholar]
- Krüsemann, E.J.Z.; Boesveldt, S.; de Graaf, K.; Talhout, R. An E-Liquid Flavor Wheel: A Shared Vocabulary Based on Systematically Reviewing E-Liquid Flavor Classifications in Literature. Nicotine Tob. Res. 2019, 21, 1310–1319. [Google Scholar] [CrossRef] [PubMed]
- Hajek, P.; Etter, J.-F.; Benowitz, N.; Eissenberg, T.; McRobbie, H. Electronic Cigarettes: Review of Use, Content, Safety, Effects on Smokers and Potential for Harm and Benefit: Electronic Cigarettes: A Review. Addiction 2014, 109, 1801–1810. [Google Scholar] [CrossRef] [PubMed]
- Farzal, Z.; Perry, M.F.; Yarbrough, W.G.; Kimple, A.J. The Adolescent Vaping Epidemic in the United States—How It Happened and Where We Go From Here. JAMA Otolaryngol. Head Neck Surg. 2019, 145, 885–886. [Google Scholar] [CrossRef] [PubMed]
- Ali, F.R.M.; Seidenberg, A.; Crane, E.; Seaman, E.; Tynan, M.A.; Marynak, K. E-Cigarette Unit Sales by Product and Flavor Type, and Top-Selling Brands, United States, 2020–2022. MMWR Morb. Mortal. Wkly. Rep. 2023, 72, 672–677. [Google Scholar] [CrossRef] [PubMed]
- Surgeon General’s Advisory on E-Cigarette Use Among Youth|Smoking & Tobacco Use|CDC. Available online: https://www.cdc.gov/tobacco/basic_information/e-cigarettes/surgeon-general-advisory/index.html (accessed on 16 September 2023).
- National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health. Introduction, Conclusions, and Historical Background Relative to E-Cigarettes. In E-Cigarette Use Among Youth and Young Adults: A Report of the Surgeon General; Centers for Disease Control and Prevention: Atlanta, GA, USA, 2016. [Google Scholar]
- Kelsh, S.; Ottney, A.; Young, M.; Kelly, M.; Larson, R.; Sohn, M. Young Adults’ Electronic Cigarette Use and Perceptions of Risk. Tob. Use Insights 2023, 16, 1179173X231161313. [Google Scholar] [CrossRef]
- Talhout, R.; Schulz, T.; Florek, E.; Van Benthem, J.; Wester, P.; Opperhuizen, A. Hazardous Compounds in Tobacco Smoke. Int. J. Environ. Res. Public Health 2011, 8, 613–628. [Google Scholar] [CrossRef]
- Polosa, R.; Caponnetto, P.; Morjaria, J.B.; Papale, G.; Campagna, D.; Russo, C. Effect of an Electronic Nicotine Delivery Device (e-Cigarette) on Smoking Reduction and Cessation: A Prospective 6-Month Pilot Study. BMC Public Health 2011, 11, 786. [Google Scholar] [CrossRef] [PubMed]
- Yu, V.; Rahimy, M.; Korrapati, A.; Xuan, Y.; Zou, A.E.; Krishnan, A.R.; Tsui, T.; Aguilera, J.A.; Advani, S.; Crotty Alexander, L.E.; et al. Electronic Cigarettes Induce DNA Strand Breaks and Cell Death Independently of Nicotine in Cell Lines. Oral. Oncol. 2016, 52, 58–65. [Google Scholar] [CrossRef] [PubMed]
- Holliday, R.; Kist, R.; Bauld, L. E-Cigarette Vapour Is Not Inert and Exposure Can Lead to Cell Damage. Evid. Based Dent. 2016, 17, 2–3. [Google Scholar] [CrossRef] [PubMed]
- Song, Y.; Li, X.; Li, C.; Xu, S.; Liu, Y.; Wu, X. What Are the Effects of Electronic Cigarettes on Lung Function Compared to Non-Electronic Cigarettes? A Systematic Analysis. Int. J. Public Health 2022, 67, 1604989. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.B.; Olgin, J.E.; Nah, G.; Vittinghoff, E.; Cataldo, J.K.; Pletcher, M.J.; Marcus, G.M. Cigarette and E-Cigarette Dual Use and Risk of Cardiopulmonary Symptoms in the Health eHeart Study. PLOS ONE 2018, 13, e0198681. [Google Scholar] [CrossRef] [PubMed]
- Chaumont, M.; van de Borne, P.; Bernard, A.; Van Muylem, A.; Deprez, G.; Ullmo, J.; Starczewska, E.; Briki, R.; de Hemptinne, Q.; Zaher, W.; et al. Fourth Generation E-Cigarette Vaping Induces Transient Lung Inflammation and Gas Exchange Disturbances: Results from Two Randomized Clinical Trials. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2019, 316, L705–L719. [Google Scholar] [CrossRef] [PubMed]
- Palamidas, A.; Gennimata, S.A.; Kaltsakas, G.; Tsikrika, S.; Vakali, S.; Gratziou, C.; Koulouris, N. Acute Effect of an E-Cigarette with and without Nicotine on Lung Function. Tob. Induc. Dis. 2014, 12, A34. [Google Scholar] [CrossRef]
- Clapp, P.W.; Pawlak, E.A.; Lackey, J.T.; Keating, J.E.; Reeber, S.L.; Glish, G.L.; Jaspers, I. Flavored E-Cigarette Liquids and Cinnamaldehyde Impair Respiratory Innate Immune Cell Function. Am. J. Physiol.-Lung Cell. Mol. Physiol. 2017, 313, L278–L292. [Google Scholar] [CrossRef] [PubMed]
- Muthumalage, T.; Prinz, M.; Ansah, K.O.; Gerloff, J.; Sundar, I.K.; Rahman, I. Inflammatory and Oxidative Responses Induced by Exposure to Commonly Used E-Cigarette Flavoring Chemicals and Flavored e-Liquids without Nicotine. Front. Physiol. 2018, 8, 1130. [Google Scholar] [CrossRef]
- Aas, J.A.; Paster, B.J.; Stokes, L.N.; Olsen, I.; Dewhirst, F.E. Defining the Normal Bacterial Flora of the Oral Cavity. J. Clin. Microbiol. 2005, 43, 5721–5732. [Google Scholar] [CrossRef]
- Jia, G.; Zhi, A.; Lai, P.F.H.; Wang, G.; Xia, Y.; Xiong, Z.; Zhang, H.; Che, N.; Ai, L. The Oral Microbiota—A Mechanistic Role for Systemic Diseases. Br. Dent. J. 2018, 224, 447–455. [Google Scholar] [CrossRef]
- Kolenbrander, P.E.; Andersen, R.N.; Blehert, D.S.; Egland, P.G.; Foster, J.S.; Palmer, R.J. Communication among Oral Bacteria. Microbiol. Mol. Biol. Rev. 2002, 66, 486–505. [Google Scholar] [CrossRef]
- Jenkinson, H.F.; Lamont, R.J. Oral Microbial Communities in Sickness and in Health. Trends Microbiol. 2005, 13, 589–595. [Google Scholar] [CrossRef] [PubMed]
- Hanel, A.N.; Herzog, H.M.; James, M.G.; Cuadra, G.A. Effects of Oral Commensal Streptococci on Porphyromonas Gingivalis Invasion into Oral Epithelial Cells. Dent. J. 2020, 8, 39. [Google Scholar] [CrossRef]
- Ganesan, S.M.; Dabdoub, S.M.; Nagaraja, H.N.; Scott, M.L.; Pamulapati, S.; Berman, M.L.; Shields, P.G.; Wewers, M.E.; Kumar, P.S. Adverse Effects of Electronic Cigarettes on the Disease-Naive Oral Microbiome. Sci. Adv. 2020, 6, eaaz0108. [Google Scholar] [CrossRef] [PubMed]
- Maki, K.A.; Ganesan, S.M.; Meeks, B.; Farmer, N.; Kazmi, N.; Barb, J.J.; Joseph, P.V.; Wallen, G.R. The Role of the Oral Microbiome in Smoking-Related Cardiovascular Risk: A Review of the Literature Exploring Mechanisms and Pathways. J. Transl. Med. 2022, 20, 584. [Google Scholar] [CrossRef]
- Patangia, D.V.; Anthony Ryan, C.; Dempsey, E.; Paul Ross, R.; Stanton, C. Impact of Antibiotics on the Human Microbiome and Consequences for Host Health. Microbiologyopen 2022, 11, e1260. [Google Scholar] [CrossRef] [PubMed]
- Hajishengallis, G. Periodontitis: From Microbial Immune Subversion to Systemic Inflammation. Nat. Rev. Immunol. 2015, 15, 30–44. [Google Scholar] [CrossRef]
- Mealey, B.L. Influence of Periodontal Infections on Systemic Health. Periodontology 2000 1999, 21, 197–209. [Google Scholar] [CrossRef]
- Cichońska, D.; Kusiak, A.; Piechowicz, L.; Świetlik, D. A Pilot Investigation into the Influence of Electronic Cigarettes on Oral Bacteria. Adv. Dermatol. Allergol. 2022, 38, 1092–1098. [Google Scholar] [CrossRef]
- Cuadra, G.A.; Smith, M.T.; Nelson, J.M.; Loh, E.K.; Palazzolo, D.L. A Comparison of Flavorless Electronic Cigarette-Generated Aerosol and Conventional Cigarette Smoke on the Survival and Growth of Common Oral Commensal Streptococci. Int. J. Environ. Res. Public Health 2019, 16, 1669. [Google Scholar] [CrossRef] [PubMed]
- Nelson, J.M.; Cuadra, G.A.; Palazzolo, D.L. A Comparison of Flavorless Electronic Cigarette-Generated Aerosol and Conventional Cigarette Smoke on the Planktonic Growth of Common Oral Commensal Streptococci. Int. J. Environ. Res. Public Health 2019, 16, 5004. [Google Scholar] [CrossRef] [PubMed]
- Fischman, J.S.; Sista, S.; Lee, D.; Cuadra, G.A.; Palazzolo, D.L. Flavorless vs. Flavored Electronic Cigarette-Generated Aerosol and E-Liquid on the Growth of Common Oral Commensal Streptococci. Front. Physiol. 2020, 11, 585416. [Google Scholar]
- Xu, C.P.; Palazzolo, D.L.; Cuadra, G.A. Mechanistic Effects of E-Liquids on Biofilm Formation and Growth of Oral Commensal Streptococcal Communities: Effect of Flavoring Agents. Dent. J. 2022, 10, 85. [Google Scholar] [CrossRef] [PubMed]
- Socransky, S.S.; Haffajee, A.D.; Cugini, M.A.; Smith, C.; Kent, R.L., Jr. Microbial Complexes in Subgingival Plaque. J. Clin. Periodontol. 1998, 25, 134–144. [Google Scholar] [CrossRef]
- Nyvad, B.; Kilian, M. Microbiology of the Early Colonization of Human Enamel and Root Surfaces in Vivo. Eur. J. Oral Sci. 1987, 95, 369–380. [Google Scholar] [CrossRef] [PubMed]
- Garnier, F.; Gerbaud, G.; Courvalin, P.; Galimand, M. Identification of Clinically Relevant Viridans Group Streptococci to the Species Level by PCR. J. Clin. Microbiol. 1997, 35, 2337–2341. [Google Scholar] [CrossRef]
- Cuadra-Saenz, G.; Rao, D.L.; Underwood, A.J.; Belapure, S.A.; Campagna, S.R.; Sun, Z.; Tammariello, S.; Rickard, A.H. Autoinducer-2 Influences Interactions amongst Pioneer Colonizing Streptococci in Oral Biofilms. Microbiology 2012, 158, 1783–1795. [Google Scholar] [CrossRef]
- Material Safety Data Sheet—Menthol. Available online: https://fscimage.fishersci.com/msds/23818.htm (accessed on 29 January 2024).
- Battery for Challenger Kit Extreme Kit (Compatible with V2 Cartridges). Available online: https://apolloecigs.com/products/battery-for-challenger-kit-extreme-kit-compatible-with-v2-cartridges-1-piece (accessed on 14 March 2024).
- Routine Analytical Machine for E-Cigarette Aerosol Generation and Collection—Definitions and Standard Conditions|CORESTA. Available online: https://www.coresta.org/routine-analytical-machine-e-cigarette-aerosol-generation-and-collection-definitions-and-standard (accessed on 14 March 2024).
- Asally, M.; Kittisopikul, M.; Rué, P.; Du, Y.; Hu, Z.; Çağatay, T.; Robinson, A.B.; Lu, H.; Garcia-Ojalvo, J.; Süel, G.M. Localized Cell Death Focuses Mechanical Forces during 3D Patterning in a Biofilm. Proc. Natl. Acad. Sci. USA 2012, 109, 18891–18896. [Google Scholar] [CrossRef]
- Ingendoh-Tsakmakidis, A.; Mikolai, C.; Winkel, A.; Szafrański, S.P.; Falk, C.S.; Rossi, A.; Walles, H.; Stiesch, M. Commensal and Pathogenic Biofilms Differently Modulate Peri-implant Oral Mucosa in an Organotypic Model. Cell. Microbiol. 2019, 21, e13078. [Google Scholar] [CrossRef]
- Mikolai, C.; Kommerein, N.; Ingendoh-Tsakmakidis, A.; Winkel, A.; Falk, C.S.; Stiesch, M. Early Host–Microbe Interaction in a Peri-Implant Oral Mucosa-Biofilm Model. Cell. Microbiol. 2020, 22, e13209. [Google Scholar] [CrossRef] [PubMed]
- Vijayakumar, A.; Sarveswari, H.B.; Vasudevan, S.; Shanmugam, K.; Solomon, A.P.; Neelakantan, P. Baicalein Inhibits Streptococcus Mutans Biofilms and Dental Caries-Related Virulence Phenotypes. Antibiotics 2021, 10, 215. [Google Scholar] [CrossRef] [PubMed]
- Shen, S.; Zhang, T.; Yuan, Y.; Lin, S.; Xu, J.; Ye, H. Effects of Cinnamaldehyde on Escherichia Coli and Staphylococcus Aureus Membrane. Food Control. 2015, 47, 196–202. [Google Scholar] [CrossRef]
- Balasubramanian, A.R.; Vasudevan, S.; Shanmugam, K.; Lévesque, C.M.; Solomon, A.P.; Neelakantan, P. Combinatorial Effects of Trans-cinnamaldehyde with Fluoride and Chlorhexidine on Streptococcus Mutans. J. Appl. Microbiol. 2021, 130, 382–393. [Google Scholar] [CrossRef] [PubMed]
- He, Z.; Huang, Z.; Jiang, W.; Zhou, W. Antimicrobial Activity of Cinnamaldehyde on Streptococcus Mutans Biofilms. Front. Microbiol. 2019, 10, e13078. [Google Scholar] [CrossRef] [PubMed]
- Golestannejad, Z.; Gavanji, S.; Mohammadi, E.; Bahrani, M.; Rezaei, F.; Larki, B.; Mojiri, A.; Bakhtari, A. Comparison of Antibacterial Activity of Essential Oils of Foeniculum Vulgare Mill, Mentha Arvensis and Mentha Piperita against Streptococcus Mutans. Future Nat. Products 2018, 4, 3–13. [Google Scholar]
- Chung, J.Y.; Choo, J.H.; Lee, M.H.; Hwang, J.K. Anticariogenic Activity of Macelignan Isolated from Myristica Fragrans (Nutmeg) against Streptococcus Mutans. Phytomedicine 2006, 13, 261–266. [Google Scholar] [CrossRef] [PubMed]
- Ribeiro, B.D.; Florindo, C.; Iff, L.C.; Coelho, M.A.Z.; Marrucho, I.M. Menthol-Based Eutectic Mixtures: Hydrophobic Low Viscosity Solvents. ACS Sustain. Chem. Eng. 2015, 3, 2469–2477. [Google Scholar] [CrossRef]
- Whitmore, S.E.; Lamont, R.J. The Pathogenic Persona of Community-Associated Oral Streptococci. Mol. Microbiol. 2011, 81, 305–314. [Google Scholar] [CrossRef]
- Courtney, H.S.; Ofek, I.; Penfound, T.; Nizet, V.; Pence, M.A.; Kreikemeyer, B.; Podbielbski, A.; Hasty, D.L.; Dale, J.B. Relationship between Expression of the Family of M Proteins and Lipoteichoic Acid to Hydrophobicity and Biofilm Formation in Streptococcus Pyogenes. PLoS ONE 2009, 4, e4166. [Google Scholar] [CrossRef]
- Nesbitt, W.E.; Doyle, R.J.; Taylor, K.G. Hydrophobic Interactions and the Adherence of Streptococcus Sanguis to Hydroxylapatite. Infect. Immun. 1982, 38, 637–644. [Google Scholar] [PubMed]
- Mirani, Z.A.; Fatima, A.; Urooj, S.; Aziz, M.; Khan, M.N.; Abbas, T. Relationship of Cell Surface Hydrophobicity with Biofilm Formation and Growth Rate: A Study on Pseudomonas Aeruginosa, Staphylococcus Aureus, and Escherichia Coli. Iran. J. Basic Med. Sci. 2018, 21, 760–769. [Google Scholar] [CrossRef] [PubMed]
- Koga, T.; Okahashi, N.; Takahashi, I.; Kanamoto, T.; Asakawa, H.; Iwaki, M. Surface Hydrophobicity, Adherence, and Aggregation of Cell Surface Protein Antigen Mutants of Streptococcus Mutans Serotype c. Infect. Immun. 1990, 58, 289–296. [Google Scholar] [CrossRef] [PubMed]
- Cowan, M.M.; Van Der Mei, H.C.; Rouxhet, P.G.; Busscher, H.J. Physico-Chemical and Structural Properties of the Surfaces of Peptostreptococcus Micros and Streptococcus Mitis as Compared to Those of Mutans Streptococci, Streptococcus Sanguis and Streptococcus Salivarius. Microbiology 1992, 138, 2707–2714. [Google Scholar] [CrossRef] [PubMed]
- Grivet, M.; Morrier, J.J.; Benay, G.; Barsotti, O. Effect of Hydrophobicity on in Vitro Streptococcal Adhesion to Dental Alloys. J. Mater. Sci. Mater. Med. 2000, 11, 637–642. [Google Scholar] [CrossRef] [PubMed]
- Bos, R.; van der Mei, H.C.; Busscher, H.J. Influence of Temperature on the Co-Adhesion of Oral Microbial Pairs in Saliva. Eur. J. Oral Sci. 1996, 104, 372–377. [Google Scholar] [CrossRef] [PubMed]
- Petersen, F.C.; Pasco, S.; Ogier, J.; Klein, J.P.; Assev, S.; Scheie, A.A. Expression and Functional Properties of the Streptococcus Intermedius Surface Protein Antigen I/II. Infect. Immun. 2001, 69, 4647–4653. [Google Scholar] [CrossRef] [PubMed]
- Gibbons, R.J.; Etherden, I. Comparative Hydrophobicities of Oral Bacteria and Their Adherence to Salivary Pellicles. Infect. Immun. 1983, 41, 1190–1196. [Google Scholar] [CrossRef] [PubMed]
- Wood, P.L.; Le, A.; Palazzolo, D.L. Comparative Lipidomics of Oral Commensal and Opportunistic Bacteria. Metabolites 2024, 14, 240. [Google Scholar] [CrossRef]
- Catala-Valentin, A.; Bernard, J.N.; Caldwell, M.; Maxson, J.; Moore, S.D.; Andl, C.D. E-Cigarette Aerosol Exposure Favors the Growth and Colonization of Oral Streptococcus Mutans Compared to Commensal Streptococci. Microbiol. Spectr. 2022, 10, e02421-21. [Google Scholar] [CrossRef]
- Burmølle, M.; Ren, D.; Bjarnsholt, T.; Sørensen, S.J. Interactions in Multispecies Biofilms: Do They Actually Matter? Trends Microbiol. 2014, 22, 84–91. [Google Scholar] [CrossRef] [PubMed]
- Qiu, Y.; Zhou, Y.; Chang, Y.; Liang, X.; Zhang, H.; Lin, X.; Qing, K.; Zhou, X.; Luo, Z. The Effects of Ventilation, Humidity, and Temperature on Bacterial Growth and Bacterial Genera Distribution. Int. J. Environ. Res Public Health 2022, 19, 15345. [Google Scholar] [CrossRef] [PubMed]
- Kreth, J.; Merritt, J.; Qi, F. Bacterial and Host Interactions of Oral Streptococci. DNA Cell Biol. 2009, 28, 397–403. [Google Scholar] [CrossRef] [PubMed]
- Kreth, J.; Zhang, Y.; Herzberg, M.C. Streptococcal Antagonism in Oral Biofilms: Streptococcus Sanguinis and Streptococcus Gordonii Interference with Streptococcus Mutans. J. Bacteriol. 2008, 190, 4632–4640. [Google Scholar] [CrossRef]
- Aherrera, A.; Aravindakshan, A.; Jarmul, S.; Olmedo, P.; Chen, R.; Cohen, J.E.; Navas-Acien, A.; Rule, A.M. E-Cigarette Use Behaviors and Device Characteristics of Daily Exclusive e-Cigarette Users in Maryland: Implications for Product Toxicity. Tob. Induc. Dis. 2020, 18, 93. [Google Scholar] [CrossRef]
Slope Value | p-Value * | R2 | |
---|---|---|---|
S. gordonii | |||
Air | 0.03777 ± 0.1523 | - | 0.001336 |
Flavorless | −0.1644 ± 0.1569 | NS | 0.02379 |
Menthol | 0.1688 ± 0.1438 | NS | 0.03106 |
Cinnamon | −0.7238 ± 0.2758 | p < 0.01 | 0.1381 |
S. intermedius | |||
Air | 0.4536 ± 0.05000 | - | 0.9763 |
Flavorless | −0.9701 ± 0.3070 | p < 0.01 | 0.8331 |
Menthol | −0.6302 ± 0.2753 | p < 0.01 | 0.7239 |
Cinnamon | −0.6302 ± 0.2753 | p < 0.01 | 0.6158 |
S. mitis | |||
Air | 1.150 ± 0.3194 | - | 0.2198 |
Flavorless | 0.3234 ± 0.1490 | p < 0.01 | 0.09665 |
Menthol | 0.2252 ± 0.2133 | p < 0.01 | 0.02527 |
Cinnamon | −0.02657 ± 0.2913 | p < 0.01 | 0.0001808 |
S. oralis | |||
Air | 0.6079 ± 0.1536 | - | 0.2583 |
Flavorless | −0.08662 ± 0.2611 | p < 0.01 | 0.002554 |
Menthol | −0.1619 ± 0.1222 | p < 0.01 | 0.03837 |
Cinnamon | 0.4826 ± 0.1911 | NS | 0.1292 |
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Christian, N.; Burden, D.; Emam, A.; Brenk, A.; Sperber, S.; Kalu, M.; Cuadra, G.; Palazzolo, D. Effects of E-Liquids and Their Aerosols on Biofilm Formation and Growth of Oral Commensal Streptococcal Communities: Effect of Cinnamon and Menthol Flavors. Dent. J. 2024, 12, 232. https://doi.org/10.3390/dj12080232
Christian N, Burden D, Emam A, Brenk A, Sperber S, Kalu M, Cuadra G, Palazzolo D. Effects of E-Liquids and Their Aerosols on Biofilm Formation and Growth of Oral Commensal Streptococcal Communities: Effect of Cinnamon and Menthol Flavors. Dentistry Journal. 2024; 12(8):232. https://doi.org/10.3390/dj12080232
Chicago/Turabian StyleChristian, Nicole, Daniel Burden, Alexander Emam, Alvin Brenk, Sarah Sperber, Michael Kalu, Giancarlo Cuadra, and Dominic Palazzolo. 2024. "Effects of E-Liquids and Their Aerosols on Biofilm Formation and Growth of Oral Commensal Streptococcal Communities: Effect of Cinnamon and Menthol Flavors" Dentistry Journal 12, no. 8: 232. https://doi.org/10.3390/dj12080232