Journal of Investigative and Clinical Dentistry (2015), 0, 1–12

REVIEW ARTICLE Oral Medicine

Photobiomodulation in oral medicine: a review Padma Pandeshwar1, Mahesh Datta Roa2, Reshma Das1, Shilpa P. Shastry1, Rachna Kaul1 & Mahesh B. Srinivasreddy1 1 Department of Oral Medicine and Radiology, Vydehi Institute of Dental Sciences and Research Centre, Whitefield, Bangalore, India 2 Department of Oral Medicine and Radiology, Dayananda Sagar College of Dental Sciences, Bangalore, India

Keywords burning mouth syndrome, low-level laser therapy, photobiomodulation, recurrent aphthous ulceration, temporomandibular disorder. Correspondence Dr P. Pandeshwar, Department of Oral Medicine and Radiology, Vydehi Institute of Dental Sciences and Research Centre, no. 82, EPIP Area, Whitefield, Bangalore 560066, India. Tel: +91 09845196873 Email: [email protected] Received 12 June 2014; accepted 22 November 2014.

Abstract Photobiomodulation (PBM) or low-level laser therapy (LLLT) in dentistry is an evolving science, with an increasing number of controlled clinical studies exploring its potential as a treatment modality. The present study provides an outline of the biologic mechanism of PBM and summarizes the findings of clinical studies of PBM for specific applications in oral medicine. Controversies and drawbacks associated with PBM, which require further research, are also identified. Current literature reports the potential of PBM in various applications in oral medicine. Furthermore, well-documented research confirms its efficacy in certain conditions, such as oral mucositis, recurrent herpes simplex infection, and burning mouth syndrome. The absence of any reported adverse effects is an advantage over conventional therapeutic modalities. While PBM has proved to be effective for some specific applications, it is not a panacea. The paucity in standardized studies, coupled with ambiguity over the laser parameters, has limited its credibility as a therapeutic modality.

doi: 10.1111/jicd.12148

Introduction Photobiomodulation (PBM), also known as low-level laser therapy (LLLT) or cold laser therapy, was developed in 1967 by Endre Mester, who was the first to describe the “biostimulation” effect of lasers.1 The term “PBM” is generally substituted for “LLLT”, as the therapy does not only stimulate, but can also suppress biologic processes.2 PBM is a drug-free, non-invasive clinical application of red (600–700 nm) and near infrared light (NIR) (700– 950 nm, usually produced by low-to-mid power coherent lasers or non-coherent light-emitting diodes [LED]), with a power density (irradiance) between 1 mW and 5 W/cm2 over injuries or lesions to improve wound and soft tissue healing, reduce inflammation, and give relief for both acute and chronic pain.3,4 PBM has approval from the Food and Drug Administration (FDA), Health Canada, Conformite Europeenne, and numerous other health regulatory agencies from many countries worldwide.4 Unlike other medical laser procedures, PBM is a non-ablative and non-thermal mechanism, with a photochemical ª 2015 Wiley Publishing Asia Pty Ltd

effect comparable to photosynthesis in plants, whereby the light is absorbed and exerts a chemical change.5 The primary effect occurs when light is absorbed in cytochrome c oxidase (CCO), a protein within the mitochondria that increases adenosine triphosphate (ATP) production and reduces oxidative stress.6 PBM is characterized by a biphasic dose response (Arndt-Schultz Law), where a “therapeutic window” within a certain dose range exists; too small a dose gives no effect, and doses over that range are inhibitory (Figure 1).5,7,8 Mechanism of action The precise biochemical mechanism underlying the therapeutic effects of PBM have not yet been well established.7 There is a growing body of evidence that suggests that the primary effect is the stimulation of mitochondrial cytochromes, which in turn initiates secondary cell-signaling pathways. The overall result of PBM is increased energy metabolism and improved cell viability.9–12 Within mammalian tissues, there are three major photoacceptor molecules: hemoglobin, myoglobin, and CCO. 1

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Figure 1. Tissue optical window. (a) Percentage of absorption of light in tissue versus laser wavelength; (b) super-pulsed laser. IRED, infra red emitting diode; LED, light-emitting diodes; Nd:YAG, neodymium: yttrium–aluminum–garnet.

Of these, CCO is the one involved in energy metabolism and production.9,13 This was confirmed when absorption spectra obtained for CCO in different oxidation states were found to be very similar to the action spectra for biologic responses to light.12 In the mitochondria, especially of stressed or hypoxic cells, nitric oxide (NO) binds to CCO by competitively displacing oxygen, inhibiting cellular respiration, and thus decreasing the production of ATP. PBM might work by photodissociating NO from CCO, thereby reversing the mitochondrial inhibition of respiration and the generation of reactive-oxygen species (ROS) (Figure 2).7 This shift in overall cell redox potential, toward greater oxidation10 and increased ROS generation, causes the activation of redox-sensitive transcription factors, such as necrosis factor-Kb, leading to the expression of an array of gene products that prevent apoptosis and cell death, stimulate fibroblast proliferation, migration and

collagen synthesis, modulate the inflammatory and antioxidant response, and stimulate angiogenesis and tissue repair.5,14 In addition to this, NO is photodissociated from other intracellular stores, such as the nitrosylated hemoglobin and nitrosylated myoglobin, causing vasodilation.5 Laser technology in photobiomodulation PBM uses various light sources (e.g. lasers, LED) with different parameters (e.g. wavelength, output power, continuous-wave or pulsed operation modes, pulse parameters). In recent years, longer wavelengths (~800–900 nm) and higher output powers (up to 100 mW) have been preferred in therapeutic devices, especially to allow deeper tissue penetration. The FDA has granted marketing clearances to several devices, although none of those clearances are specifically for dentistry, which are

Figure 2. Proposed mechanism of low-level laser therapy. AP-1, activator protein 1; ATP, adenosine triphosphate; cAMP, cyclic adenosine monophosphate; Fos, Finkel–Biskis–Jinkins murine osteogenic sarcoma virus; IKb, I kappa b; Jun; NF-Kb, necrosis factor-Kb; NO, nitric oxide; PKD, protein kinase D; ROS, reactive-oxygen species. (Adapted from: Ying-Ying Huang, Michael Hamblin, and Aaron C.-H. Chen. Low-level laser therapy: an emerging clinical paradigm. 9 July 2009, SPIE Newsroom. DOI: 10.1117/2.1200906.1669)

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Table 1. Lasers used in photobiomodulation HeNe or InGaAlP Wavelength Pulsed or continuous Penetration depth Ideal treatment applications Benefits

GaAlA Wavelength Pulsed or continuous Penetration depth Ideal treatment applications GaA Wavelength Pulsed or continuous Penetration depth Ideal treatment applications

633–660 nm Generally continuous, but can be mechanically pulsed Shallow, ~1–2 cm Wound healing, shallow muscles Beneficial effect on mucous membrane and skin Minimal risk of injury to the eyes (visible light will elicit a blink reflex) 780–870 nm Continuous, but can be mechanically pulsed ~2–3 cm Wound healing, muscle attachments, muscles, oral applications 904 nm Always pulsed ~3–4 cm (although dependent on dose, power, and application mechanism) Deep muscle and inflammation treatments

GaAIA, gallium–aluminum–arsenide; GaA, gallium–arsenide; HeNe, helium neon, InGaAIP, indium–gallium–aluminum–phosphide.

considered as “off-label” uses.2 In 2002, MicroLight (Missouri City, TX, USA) received 510K FDA clearance for the ML 830 nm diode laser to treat carpal tunnel syndrome.15 Lasers in general are classified based on different properties (i.e. coherence of the beam, depth of penetration, wavelength), as well as the period of the “on time” when pulsed, and their effect on the eye. Lasers used in PBM belong to class 3 or class 3B, based on the optical hazards that they pose to patients and staff.16 The class 3 infrared wavelengths A and B refer to NIF or short wavelengths (A) and far infrared or long wavelengths (B). Classes 1, 2, and 3 (A and B) lasers do not harm tissue, but protective eyewear is necessary for the therapist and the patient.17 PBM lasers are also considered to have the best balance of power output ( placebo (PI on palpation) LLLT = placebo (ME) LLLT = placebo

6.2 J/cm2 1 J/cm2 80 J/cm2

17.3 mW 1.8 mW 40 mW

360 sec 600 sec 16 sec

48 (24 + 24)

AsGaAl 780 nm

2 sessions/week for 4 weeks

25 J/cm2 60 J/cm2

50 mW 60 mW

2

17 mW

20 sec 40 sec

LLLT > placebo LLLT > placebo LLLT = placebo

AsGa, arsenium-gallium; HeNe, helium–neon; InGaAlP, aluminium gallium indium phosphide; LLLT, low-level laser therapy; LM, lateral movements; ME, masticatory efficiency; MO, mouth opening; TP, tender points; PI, pain intensity; TMJ, temporomandibular joint.

recommended as a predictable and reliable treatment modality for TMD.73 Effect of LLLT on tumor cells Despite the favorable nature of PBM-induced cellular proliferation, there is negative speculation on its effect on tumor growth in neoplastic diseases. Previous studies of PBM irradiation of tumor cells in vitro have generated conflicting research data across a range of cultivated tumor cell lines and irradiation parameters, but there have been relatively few in vivo studies published. In vivo studies are essential for the study of disease development and are the main tool for studying the behavior of tumor cells. The effects of PBM on tumor cells in vitro reveal that such abnormal cells can be stimulated to grow. In vivo, however, small malignant and benign tumors in rats treated with PBM receded and completely disappeared. In Frigo et al.’s study, discrepancies between the in vitro and in vivo experiments’ results were noted.88 They advised caution in generalizing in vitro results, as cell– matrix interactions and cell behavior in the complex environment of tissues might produce unexpected reactions. They also found differences in the tumor behavior when the tumor cells were irradiated with different PBM parameters. Thus, more studies are needed to elucidate ª 2015 Wiley Publishing Asia Pty Ltd

the main factors that are responsible for the different behaviors of tumor cells in response to PBM, and to determine laser irradiance and energy thresholds for the stimulation of abnormal tumor cell behavior.88,89 Discretion should be employed in the use of PBM over primary or secondary tumors, and PBM needs to be used cautiously in potentially-malignant lesions, such as erosive lichen planus. Conclusion PBM is steadily moving into mainstream medicine. There have been a substantial number of reports on the clinical benefits of PBM, which also includes dentistry, although the quality of these studies is yet to be subjected to detailed assessment through randomized, clinical trials. Furthermore, the science of PBM is complicated with the requirement for a combined knowledge of laser physics, medicine, and clinical procedures.90 In the present review, a selection of the applications of PBM in oral medicine was mentioned, as only some of these indications have enough qualified studies to back them up as evidence-based therapies, such as PBM for the treatment of oral mucositis. In most other applications, the material available is insufficient for any definite conclusions. These drawbacks have limited the credibility 9

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of PBM as a therapeutic modality. Nonetheless, with advantages of being non-invasive and a lack of reported adverse effects, PBM has an edge over other treatment

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Photobiomodulation in oral medicine: a review.

Photobiomodulation (PBM) or low-level laser therapy (LLLT) in dentistry is an evolving science, with an increasing number of controlled clinical studi...
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