Abstract
Oral biofilm is a primary determinant of oral health, yet our ability to detect, map, and characterize it in vivo remains extremely limited. Moreover, there exists an as yet unmet but pressing need for characterizing its properties and response to prevention and intervention measures. Because clinical mapping of oral biofilm has been primarily restricted to macroscopic plaque staining techniques combined with naked eye visualization, additional means of assessing and quantifying oral biofilm in situ at high levels of resolution are currently under development. This chapter addresses emerging optical imaging modalities for evaluating in vivo oral biofilm noninvasively. Desirable attributes include: informing on variables that translate into clinical decision-making guidance to improve diagnosis, better treatment planning and outcomes, ease and speed of use, appropriate cost for the indicated setting, patient-friendly probes, and reliability. In this chapter, the principles behind optical approaches to imaging and characterizing oral biofilm, as well as their feasibility and applicability for imaging in situ are reviewed.
Keywords
Oral biofilm Dental plaque Salivary pellicle Optical coherence tomography (OCT) Optical coherence microscopy (OCM) Confocal laser scanning microscopy (CLSM) Multiphoton fluorescence microcopy (MPM) Atomic force microscopy Light sheet fluorescence microscopy (LSFM) Ultrasound imaging Digital imagingReferences
- 1.Whittaker C, Ridgway H, Olson BH. Evaluation of cleaning strategies for removal of biofilms from reverse-osmosis membranes. Appl Environ Microbiol. 1984;48(2):395–403.PubMedPubMedCentralGoogle Scholar
- 2.Chandki R, Banthia P, Banthia R. Biofilms: a microbial home. J Indian Soc Periodontol. 2011;15(2):111–4. https://doi.org/10.4103/0972-124X.84377.CrossRefPubMedPubMedCentralGoogle Scholar
- 3.Hannig M, Fiebiger M, Güntzer M, Döbert A, Zimehl R, Nekrasheych Y. Protective effect of the in situ formed short-term salivary pellicle. Arch Oral Biol. 2004;49:903–10.PubMedCrossRefGoogle Scholar
- 4.Nieuw Amerongen AV, Oderkerk CH, Driessen AA. Role of mucins from human whole saliva in the protection of tooth enamel against demineralization in vitro. Caries Res. 1987;21:297–309.PubMedCrossRefGoogle Scholar
- 5.Hannig C, Wasser M, Becker K, Hannig M, Huber K, Attin T. Influence of different restorative materials on lysozyme and amylase activity of the salivary pellicle in situ. J Biomed Mater Res Part A. 2006;78A:755–61.CrossRefGoogle Scholar
- 6.Zahradnik RT, Moreno EC, Burke EJ. Effect of salivary pellicle on enamel subsurface demineralization in vitro. J Dent Res. 1976;55:664–70.PubMedCrossRefGoogle Scholar
- 7.Hannig M, Hess NJ, Hoth-Hannig W, de Vrese M. Influence of salivary pellicle formation time on enamel demineralization-an in situ pilot study. Clin Oral Investig. 2003;7:158–61.PubMedCrossRefGoogle Scholar
- 8.Roberts AP, Mullany P. Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev Anti Infect Ther. 2010;8(12):1441–50.PubMedCrossRefGoogle Scholar
- 9.Ahimou F, Semmens MJ, Novak PJ, Haugstad G. Biofilm cohesiveness measurement using a novel atomic force microscopy methodology. Appl Environ Microbiol. 2007;73(9):2897–904.PubMedPubMedCentralCrossRefGoogle Scholar
- 10.Schilling KM, Bowe WH. Glucans synthesized in situ in experimental salivary pellicle function as specific binding sites for streptococcus mutans. Infect Immun. 1992;60:284–95.PubMedPubMedCentralGoogle Scholar
- 11.Gong K, Mailloux L, Herzberg MC. Salivary film express a complex, macromolecular binding site for streptococcus sanguis. J Biol Chem. 2000;275:8970–4.PubMedCrossRefGoogle Scholar
- 12.Dobell C. Antony Van Leewenhoek and his ‘little animals’. The first observations on entozoic protozoa and bacteria. New York: Russell and Russell, Inc.; 1958. p. 236–56.Google Scholar
- 13.Karygianni L, Follo M, Hellwig E, Burghardt D, Wolkewitz M, Anderson A, et al. Microscope-based imaging platform for large-scale analysis of oral biofilms. Appl Environ Microbiol. 2012;78(24):8703–11.PubMedPubMedCentralCrossRefGoogle Scholar
- 14.Zaura-Arite E, van Marle J, ten Cate JM. Conforcal microscopy study of undisturbed and chlorhexidine-treated dental biofilm. J Dent Res. 2016;80(5):1436–40.CrossRefGoogle Scholar
- 15.Wood SR, Kirkham J, Marsh PD, Shore RC, Nattress B, Robinson C. Architecture of intact natural human plaque biofilms studied by confocal laser scanning microscopy. J Dent Res. 2016;79(1):21–7.CrossRefGoogle Scholar
- 16.Dige I, Nilsson H, Kilian M, Nyvad B. In situ identification of streptococci and other bacteria in initial dental biofilm by confocal laser scanning microscopy and fluorescence in situ hybridization. Eur J Oral Sci. 2007;115(6):459–67.PubMedCrossRefGoogle Scholar
- 17.Netuschil L, Reich E, Unteregger G, Schulean A, Brecx M. A pilot study of confocal laser scanning microcopy for the assessment of undisturbed dental plaque vitality and topography. Arch Oral Biol. 1998;43(4):277–85.PubMedCrossRefGoogle Scholar
- 18.Sandison D, Webb W. Background rejection and signal-to-noise optimization in the confocal and alternative fluorescence microscopes. Appl Opt. 1994;33:603–10.PubMedCrossRefGoogle Scholar
- 19.Gratton E, van de Ven MJ. Laser sources for confocal microscopy. In: Pawley JB, editor. Handbook of biological confocal microscopy. New York: Plenum Press; 1995. p. 69–98.CrossRefGoogle Scholar
- 20.Ashkin A, Dziedzic JM, Yamane T. Optical trapping and manipulation of single cells using infrared laser beams. Nature. 1987;330:769–71.PubMedCrossRefGoogle Scholar
- 21.Claxton NS, Fellers TJ, Davidson MW. Laser scanning confocal microscopy. Tallahassee: Department of Optical Microscopy and Digital Imaging, Florida State University; 2006. http://www.olympusconfocal.com/theory/LSCMIntro.pdf.Google Scholar
- 22.Klug B, Rodler C, Koller M, Wimmer G, Kessler H, Grube M, et al. Oral biofilm analysis of palatal expanders by fluorescence in-situ hybridization and confocal laser scanning microscopy. J Vis Exp. 2011;56:2967.Google Scholar
- 23.Gabriela PM. Confocal scanning laser microscopy in the study of biofilm formation in tissues of the upper airway in otolaryngologic disease. Miscosc Sci Technol Appl Educ. 2010;3:590–6.Google Scholar
- 24.Nakano A. Spinning disk confocal microscopy—a cutting-edge tool for imaging of membrane traffic. Cell Struct Funct. 2002;27(5):349–55.PubMedCrossRefGoogle Scholar
- 25.Tomas I, Henderson B, Biz P, Donos N. In vivo oral biofilm analysis by conforcal laser scanning microscopy: methodological approaches. Miscosco Sci Technol Appl Educ. 2010;3:597–606.Google Scholar
- 26.Baek JH, Krasieva T, Tang S, Ahn Y, Kim C, Vu D, Chen Z, Wilder-Smith P. Optical approach to the salivary pellicle. J Biomed Opt. 2009;14(4):044001.PubMedPubMedCentralCrossRefGoogle Scholar
- 27.Wood SR, Kirkham J, Marsh PD, Shore RC, Nattress B, Robinson C. Architecture of intact natural human plaque biofilms studied by confocal laser scanning microscopy. J Dent Res. 2000;79:21–7.PubMedCrossRefGoogle Scholar
- 28.Wecke J, Kersten T, Madela K, Moter A, Göbel UB, Friedmann A, Bernimoulin J. A novel technique for monitoring the development of bacterial biofilms in human periodontal pockets. FEMS Microbiol Lett. 2000;191:95–101.PubMedCrossRefGoogle Scholar
- 29.Auschill TM, Hellwig E, Sculean A, Hein N, Arweiller NB. Impact of the intraoral location on the rate of biofilm growth. Clin Oral Investig. 2004;8:97–101.PubMedCrossRefGoogle Scholar
- 30.Watson PS, Pontefract HA, Devine DA, Shore RC, Nattres BR, Kirkham J, Robinson C. Penetration of fluoride into natural plaque biofilms. J Dent Res. 2005;84:451–5.PubMedCrossRefGoogle Scholar
- 31.Neu TR, Kuhlicke U, Lawrence JR. Assessment of fluorochromes for two-photon laser scanning microscopy of biofilms. Appl Environ Microbiol. 2002;68(2):901–9.PubMedPubMedCentralCrossRefGoogle Scholar
- 32.Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science. 248:73–6.PubMedCrossRefGoogle Scholar
- 33.Zipfel WR, Williams RM, Webb WW. Nonlinear magic: multiphoton microscopy in the biosciences. Nat Biotechnol. 2003;21:1369–77.PubMedCrossRefGoogle Scholar
- 34.Maeda K, Tribble GD, Tucker CM, Anaya C, Shizukuishi S, Lewis JP, Demuth DR, Lamont RJ. A porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes. Mol Microbiol. 2008;69(5):1153–64.PubMedPubMedCentralCrossRefGoogle Scholar
- 35.Tung OH, Lee SY, Lai YL, Chen HF. Characteristics of subgingival calculus detection by multiphoton fluorescence microscopy. J Biomed Opt. 2011;16(6):066017.PubMedCrossRefGoogle Scholar
- 36.König K. Multiphoton microscopy in life sciences. J Microsc. 2000;200(2):83–104.PubMedCrossRefGoogle Scholar
- 37.Bode J, Kruwel T, Tews B. Light sheet fluorescence microscopy combined with optical clearing methods as a novel imaging tool in biomedical research. Eur Med J. 2017;1:67–74.Google Scholar
- 38.Binnig G, Quate CF, Gerber C. Atomic force microscope. Phys Rev Lett. 1986;56:930–3.PubMedCrossRefGoogle Scholar
- 39.Dickinson ME, Mann AB. Nanomechanics and morphology of salivary pellicle. J Mater Res. 2006;21(8):1996–2002.CrossRefGoogle Scholar
- 40.Howland R, Benatar L, Park scientific instruments. A practical guide to scanning probe microscopy. Park scientific instruments; 1996.Google Scholar
- 41.Germano F, Bramanti E, Arcuri C, Cecchetti F, Cicciu M. Atomic force microcopy of bacteria from periodontal subgingival biofilm: preliminary study results. Eur J Dent. 2013;7(2):152–8.PubMedPubMedCentralCrossRefGoogle Scholar
- 42.Sharma S, Lavender S, Guo L, Gimzewski JK. Nasoscale characterization of effect of L-arginine on S. mutans biofilm adhesion by atomic force microscopy. Microbiology. 2014;160:1466–73.PubMedCrossRefGoogle Scholar
- 43.Dickinson ME, Mann AB. Nanoscale characterisation of salivary pellicle. MRS Proc. 844. https://doi.org/10.1557/PROC-844-Y2.3/R2.3.
- 44.Meller K, Theiss C. Atomic force microscopy and confocal laser scanning microscopy on the cytoskeleton of permeabilized and embedded cells. Ultramicroscopy. 2005;106:320–5.PubMedCrossRefGoogle Scholar
- 45.Kumar S, Hoh JH. Probing the machinery of intracelluer trafficking with the atomic force microscope. Traffic. 2001;2(11):746–56.PubMedCrossRefGoogle Scholar
- 46.Siedentopf H. Visualization and size measurement of ultramicroscopic particles, with special application to gold-colored ruby glass. Ann Phys. 1903;10:1–39.Google Scholar
- 47.Santi PA. Light sheet fluorescence microscopy. J Histochem Cytochem. 2011;59(2):129–38.PubMedPubMedCentralCrossRefGoogle Scholar
- 48.Cavalcanti IM, Ricomini FAP, Lucena-Ferreira SC, da Silva WJ, Paes Leme AF, Senna PM, Del Bel Cury AA. Salivary pellicle composition and multispecies biofilm developed on titanium nitrided by cold plasma. Arch Oral Biol. 2014;59(7):695–7.PubMedCrossRefGoogle Scholar
- 49.Kolenbrander PE, Anderson RN, Palmar RJ Jr, et al. Communication among oral bacteria. Microbiol Mol Biol Rev. 2002;66(3):486–505.PubMedPubMedCentralCrossRefGoogle Scholar
- 50.Vokes DE, Jackson R, Guo S, Perez A, Su J, Ridgway M, Armstrong WB, Chen Z, Wong BJ. Optical coherence tomography-enhanced microlaryngoscopy: preliminary report of a noncontact optical coherence tomography system integrated with a surgical microscope. Ann Otol Rhinol Laryngol. 2008;117(7):538–47.PubMedPubMedCentralCrossRefGoogle Scholar
- 51.Chelliyil RG, Ralston TS, Marks DL, Boppart SA. High speed processing architecture for spectral-domain optical coherence microscopy. J Biomed Opt. 2008;13(4):44013.CrossRefGoogle Scholar
- 52.Sumen C, Mempel TR, Mazo IB, von Andrian UH. Intravital microscopy: visualizing immunity in context. Immunity. 2004;21(3):315–29.PubMedGoogle Scholar
- 53.Huang R, Li M, Gregory RL. Bacterial interactions in dental biofilm. Virulence. 2011;2:435–44.PubMedPubMedCentralCrossRefGoogle Scholar
- 54.Corbin A, Pitts B, Parker A, Stewart PS. Antimicrobial penetration and efficancy in an in vitro oral biofilm model. Antimicrob Agents Chemother. 2011;55(7):3338–44.PubMedPubMedCentralCrossRefGoogle Scholar
- 55.Baker PJ, Pintar AL, Lin-Gibson S, Lin NJ, Lopez-Perez D. Evaluating the activity of an anti-biofilm agent via imaging. BioImaging Informatics Conference. 2015.Google Scholar
- 56.March PD. Dental plaque as a microbial biofilm. Caries Res. 2004;38(3):204–11.CrossRefGoogle Scholar
- 57.Ajdaharian J, Dadkhah M, Sabokpey S, Biren-Fetz J, Chung NE, Wink C, Wilder-Smith P. Multimodality imaging of the effects of a novel dentifrice on oral biofilm. Lasers Surg Med. 2014;46(7):546–52.PubMedPubMedCentralCrossRefGoogle Scholar
- 58.Quintas V, Prada-López I, Prados-Frutos JC, Tomás I. In situ antimicrobial activity on oral biofilm: essential oils vs. 0.2% chlorhexidine. Clin Oral Investig. 2015;19(1):97–107.PubMedCrossRefGoogle Scholar
- 59.McNamara PM, Dsouza R, O’Riordan C, Collins S, O’Brien P, Wilson C, Hogan J, Leahy MJ. Development of a first-generation miniature multiple reference optical coherence tomography imaging device. J Biomed Opt. 2016;21(12):126020.PubMedCrossRefGoogle Scholar