Photodynamic therapy as a new treatment modality for inflammatory and infectious conditions

Expert Review of Clinical Immunology

Volumn 11, Issue 5, 2015, Pages 637-657

  Reinhard, Aurélie ^a,b,c   Sandborn, William J ^d   Melhem, Hassan ^a   Bolotine, Lina ^a,b   Chamaillard, Mathias ^e   Peyrin Biroulet, Laurent ^c,f  

^a UNIVERSITÉ DE LORRAINE   (France)

^b CENTRE DE RECHERCHE EN AUTOMATIQUE DE NANCY   (France)

^c INSERM   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e INSERM U1019   (France)

^f CHU NANCY BRABOIS   (France)

Author keywords

Antimicrobial; Immune modulation; Inflammation; Photodynamic therapy; Wound healing

Indexed keywords

CYCLOSPORIN A; INDOMETACIN; INTERLEUKIN 10; INTERLEUKIN 6; TEMOPORFIN;

ACNE VULGARIS; ANTIMICROBIAL ACTIVITY; APOPTOSIS; ARTHRITIS; CHRONIC WOUND; CLINICAL TRIAL (TOPIC); COLORECTAL CANCER; CYTOKINE RELEASE; DENDRITIC CELL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; EXPERIMENTAL COLITIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFECTION; INFLAMMATION; LANGERHANS CELL; NONHUMAN; PERIODONTITIS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHOTODYNAMIC THERAPY; PSORIASIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; THERAPY EFFECT; TISSUE REGENERATION; TOOTH INFECTION; WOUND HEALING; ANIMAL; DISEASE MODEL; MOUSE; PHOTOCHEMOTHERAPY; PROCEDURES; TRENDS;

ANIMALS; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; HUMANS; INFECTION; INFLAMMATION; MICE; PERIODONTITIS; PHOTOCHEMOTHERAPY; PSORIASIS; WOUND HEALING;

EID: 84928179621     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1586/1744666X.2015.1032256     Document Type: Review

References (114)

1. Agostinis P, Berg K, Cengel KA, et al. Photodynamic therapy of cancer: an update. CA Cancer J Clin 2011;61:250-81
2. Ratkay LG, Waterfield JD, Hunt DW. Photodynamic therapy in immune (nononcological) disorders: focus on benzoporphyrin derivatives. BioDrugs 2000;14:127-35
3. Dai T, Huang YY, Hamblin MR. Photodynamic therapy for localized infections-state of the art. Photodiagnosis Photodyn Ther 2009;6:170-88
4. Dougherty TJ, Gomer CJ, Henderson BW, et al. Photodynamic therapy. J Natl Cancer Inst 1998;90:889-905
5. Nowis D, Stoklosa T, Legat M, et al. The influence of photodynamic therapy on the immune response. Photodiagnosis Photodyn Ther 2005;283-98
6. Elmets CA, Bowen KD. Immunological suppression in mice treated with hematoporphyrin derivative photoradiation. Cancer Res 1986;46:1608-11
7. Eming SA, Hammerschmidt M, Krieg T, et al. Interrelation of immunity and tissue repair or regeneration. Semin Cell Dev Biol 2009;20:517-27
8. Eming SA, Krieg T, Davidson JM. Inflammation in wound repair: molecular and cellular mechanisms. J Invest Dermatol 2007;127:514-25
9. Garcia VG, de Lima MA, Okamoto T, et al. Effect of photodynamic therapy on the healing of cutaneous third-degree-burn: histological study in rats. Lasers Med Sci 2010;25:221-8
10. Garrier J, Bezdetnaya L, Barlier C, et al. Foslip(R)-based photodynamic therapy as a means to improve wound healing. Photodiagnosis Photodyn Ther 2011;8: 321-7
11. Hamblin MR, O'Donnell DA, Murthy N, et al. Rapid control of wound infections by targeted photodynamic therapy monitored by in vivo bioluminescence imaging. Photochem Photobiol 2002;75:51-7
12. Hamblin MR, Zahra T, Contag CH, et al. Optical monitoring and treatment of potentially lethal wound infections in vivo. J Infec Dis 2003;187:1717-25
13. Wong TW, Wang YY, Sheu HM, et al. Bactericidal effects of toluidine blue-mediated photodynamic action on Vibrio vulnificus. Antimicrob Agents Chemother 2005;49:895-902
14. Zolfaghari PS, Packer S, Singer M, et al. In vivo killing of Staphylococcus aureus using a light-activated antimicrobial agent. BMC Microbiol 2009;9:27
15. Hansch A, Frey O, Gajda M, et al. Photodynamic treatment as a novel approach in the therapy of arthritic joints. Lasers Surg Med 2008;40:265-72
16. Huang L, Dai T, Hamblin MR. Antimicrobial photodynamic inactivation and photodynamic therapy for infections. Methods Mol Biol 2010;635:155-73
17. Chowdhary RK, Ratkay LG, Neyndorff HC, et al. The use of transcutaneous photodynamic therapy in the prevention of adjuvant-enhanced arthritis in MRL/lpr mice. Clin Immunol Immunopathol 1994;72:255-63
18. Chabannes D, Besnier DP, Esnault VL. Photopheresis affects the course of experimental allergic encephalomyelitis in Lewis rat. Photodermatol Photoimmunol Photomed 2002;18:238-43
19. Leong S, Chan AH, Levy JG, et al. Transcutaneous photodynamic therapy alters the development of an adoptively transferred form of murine experimental autoimmune encephalomyelitis. Photochem Photobiol 1996;64:751-7
20. Favre L, Borle F, Velin D, et al. Low dose endoluminal photodynamic therapy improves murine T cell-mediated colitis. Endoscopy 2011;43:604-16
21. Reinhard A, Bressenot A, Dassonneville R, et al. Photodynamic therapy relieves colitis and prevents colitis-associated carcinogenesis. Inflamm Bowel Dis 2015; In press
22. Morimoto K, Ozawa T, Awazu K, et al. Photodynamic therapy using systemic administration of 5-aminolevulinic acid and a 410-nm wavelength light-emitting diode for methicillin-resistant Staphylococcus aureus-infected ulcers in mice. PLoS One 2014;9:e105173
23. Nafee N, Youssef A, El-Gowelli H, et al. Antibiotic-free nanotherapeutics: hypericin nanoparticles thereof for improved in vitro and in vivo antimicrobial photodynamic therapy and wound healing. Int J Pharm 2013;454:249-58
24. Bissonnette R, Tremblay JF, Juzenas P, et al. Systemic photodynamic therapy with aminolevulinic acid induces apoptosis in lesional T lymphocytes of psoriatic plaques. J Invest Dermatol 2002;119:77-83
25. Fransson J, Ros AM. Clinical and immunohistochemical evaluation of psoriatic plaques treated with topical 5-aminolaevulinic acid photodynamic therapy. Photodermatol Photoimmunol Photomed 2005;21:326-32
26. Smits T, Kleinpenning MM, van Erp PE, et al. A placebo-controlled randomized study on the clinical effectiveness, immunohistochemical changes and protoporphyrin IX accumulation in fractionated 5-aminolaevulinic acidphotodynamic therapy in patients with psoriasis. Br J Dermatol 2006;155:429-36
27. Morley S, Griffiths J, Philips G, et al. Phase IIa randomized, placebo-controlled study of antimicrobial photodynamic therapy in bacterially colonized, chronic leg ulcers and diabetic foot ulcers: a new approach to antimicrobial therapy. Br J Dermatol 2013;168:617-24
28. Brown EM, Sadarangani M, Finlay BB. The role of the immune system in governing host-microbe interactions in the intestine. Nat Immunol 2013;14:660-7
29. Itoh Y, Ninomiya Y, Tajima S, et al. Photodynamic therapy of acne vulgaris with topical delta-aminolaevulinic acid and incoherent light in Japanese patients. Br J Dermatol 2001;144:575-9
30. Hongcharu W, Taylor CR, Chang Y, et al. Topical ALA-photodynamic therapy for the treatment of acne vulgaris. J Invest Dermatol 2000;115:183-92
31. Pollock B, Turner D, Stringer MR, et al. Topical aminolaevulinic acid-photodynamic therapy for the treatment of acne vulgaris: a study of clinical efficacy and mechanism of action. Br J Dermatol 2004;151:616-22
32. Alwaeli HA, Al-Khateeb SN, Al-Sadi A. Long-term clinical effect of adjunctive antimicrobial photodynamic therapy in periodontal treatment: a randomized clinical trial. Lasers Med Sci 2015;30(2):801-7
33. Campos GN, Pimentel SP, Ribeiro FV, et al. The adjunctive effect of photodynamic therapy for residual pockets in single-rooted teeth: a randomized controlled clinical trial. Lasers Med Sci 2013;28:317-24
34. Chondros P, Nikolidakis D, Christodoulides N, et al. Photodynamic therapy as adjunct to non-surgical periodontal treatment in patients on periodontal maintenance: a randomized controlled clinical trial. Lasers Med Sci 2009;24:681-8
35. Christodoulides N, Nikolidakis D, Chondros P, et al. Photodynamic therapy as an adjunct to non-surgical periodontal treatment: a randomized, controlled clinical trial. J Periodontol 2008;79:1638-44
36. Hamblin MR. Antimicrobial photodynamic therapy and photodynamic inactivation, or killing bugs with dyes and light-a symposium-in-print. Photochem Photobiol 2012. 88:496-8
37. Hunt DW, Levy JG. Immunomodulatory aspects of photodynamic therapy. Expert Opin Invest Drugs 1998;7:57-64
38. Korbelik M. Induction of tumor immunity by photodynamic therapy. J Clin Laser Med Surg 1996;14:329-34
39. Castano AP, Mroz P, Hamblin MR. Photodynamic therapy and anti-tumour immunity. Nat Rev Cancer 2006;6:535-45
40. Agostinis P, Buytaert E, Breyssens H, et al. Regulatory pathways in photodynamic therapy induced apoptosis. Photochem Photobiol Sci 2004;3:721-9
41. Granville DJ, Carthy CM, Jiang H, et al. Rapid cytochrome c release, activation of caspases 3, 6, 7 and 8 followed by Bap31 cleavage in HeLa cells treated with photodynamic therapy. FEBS Lett 1998;437:5-10
42. Granville DJ, Jiang H, McManus BM, et al. Fas ligand and TRAIL augment the effect of photodynamic therapy on the induction of apoptosis in JURKAT cells. Int Immunopharmacol 2001;1:1831-40
43. Granville DJ, Levy JG, Hunt DW. Photodynamic therapy induces caspase-3 activation in HL-60 cells. Cell Death Differ 1997;4:623-8
44. Granville DJ, Levy JG, Hunt DW. Photodynamic treatment with benzoporphyrin derivative monoacid ring A produces protein tyrosine phosphorylation events and DNA fragmentation in murine P815 cells. Photochem Photobiol 1998;67: 358-62
45. Allison BA, Pritchard PH, Levy JG. Evidence for low-density lipoprotein receptor-mediated uptake of benzoporphyrin derivative. Br J Cancer 1994;69:833-9
46. Hunt DW, Jiang H, Granville DJ, et al. Consequences of the photodynamic treatment of resting and activated peripheral T lymphocytes. Immunopharmacology 1999;41:31-44
47. Jiang H, Granville DJ, North JR, et al. Selective action of the photosensitizer QLT0074 on activated human T lymphocytes. Photochem Photobiol 2002;76:224-31
48. Hunt DW, Chan AH. Influence of photodynamic therapy on immunological aspects of disease-an update. Expert Opin Investig Drugs 2000;9:807-17
49. King DE, Jiang H, Simkin GO, et al. Photodynamic alteration of the surface receptor expression pattern of murine splenic dendritic cells. Scand J Immunol 1999;49:184-92
50. Obochi MO, Ratkay LG, Levy JG. Prolonged skin allograft survival after photodynamic therapy associated with modification of donor skin antigenicity. Transplantation 1997;63:810-17
51. Evangelou G, Farrar MD, Cotterell L, et al. Topical photodynamic therapy significantly reduces epidermal Langerhans cells during clinical treatment of basal cell carcinoma. Br J Dermatol 2012;166:1112-15
52. Evangelou G, Farrar MD, White RD, et al. Topical aminolaevulinic acid-photodynamic therapy produces an inflammatory infiltrate but reduces Langerhans cells in healthy human skin in vivo. Br J Dermatol 2011;165:513-19
53. Ramaswamy P, Powers JG, Bhawan J, et al. Effective blue light photodynamic therapy does not affect cutaneous langerhans cell number or oxidatively damage DNA. Dermatol Surg 2014;40:979-87
54. Matthews YJ, Damian DL. Topical photodynamic therapy is immunosuppressive in humans. Br J Dermatol 2010;162:637-41
55. Castano AP DT, Hamblin MR. Mechanisms in photodynamic therapy : part two-cellular signaling, cell metabolism and modes of cell death. Photodiagnosis Photodyn Ther 2005;2:23
56. Larisch P, Verwanger T, Linecker M, et al. The Interrelation Between a Pro-inflammatory Milieu and Fluorescence Diagnosis or Photodynamic Therapy of Human Skin Cell Lines. Photodiagnosis Photodyn Ther 2014;11(2):91-103
57. Gollnick SO, Liu X, Owczarczak B, et al. Altered expression of interleukin 6 and interleukin 10 as a result of photodynamic therapy in vivo. Cancer Res 1997;57:3904-9
58. Simkin GO, Tao JS, Levy JG, et al. IL-10 contributes to the inhibition of contact hypersensitivity in mice treated with photodynamic therapy. J Immunol 2000;164:2457-62
59. de Waal Malefyt R, Haanen J, Spits H, et al. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med 1991;174:915-24
60. D'Andrea A, Aste-Amezaga M, Valiante NM, et al. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 1993;178: 1041-8
61. Koch F, Stanzl U, Jennewein P, et al. High level IL-12 production by murine dendritic cells: upregulation via MHC class II and CD40 molecules and downregulation by IL-4 and IL-10. J Exp Med 1996;184:741-6
62. Gollnick SO, Musser DA, Oseroff AR, et al. IL-10 does not play a role in cutaneous Photofrin photodynamic therapy-induced suppression of the contact hypersensitivity response. Photochem Photobiol 2001;74:811-16
63. Werner S, Grose R. Regulation of wound healing by growth factors and cytokines. Physiol Rev 2003;83:835-70
64. Hubner G, Hu Q, Smola H, et al. Strong induction of activin expression after injury suggests an important role of activin in wound repair. Dev Biol 1996;173:490-8
65. Liechty KW, Kim HB, Adzick NS, et al. Fetal wound repair results in scar formation in interleukin-10-deficient mice in a syngeneic murine model of scarless fetal wound repair. J Pediatr Surg 2000;35: 866-72; discussion 72-3
66. Jayasree RS, Gupta AK, Rathinam K, et al. The influence of photodynamic therapy on the wound healing process in rats. J Biomat Appl 2001;15:176-86
67. Silva JC, Lacava ZG, Kuckelhaus S, et al. Evaluation of the use of low level laser and photosensitizer drugs in healing. Lasers Surg Med 2004;34:451-7
68. Stachon T, Wang J, Langenbucher A, et al. IL-1alpha, IL-1beta, IL-6, and IL-8 secretion of human keratocytes following photodynamic inactivation (PDI) in vitro. Graefes Arch Clin Exp Ophthalmol 2013;251:2585-90
69. Stachon T, Wang J, Eppig T, et al. KGF, FGFb, VEGF, HGF and TGFbeta1 secretion of human keratocytes following photodynamic inactivation (PDI) in vitro. Graefes Arch Clin Exp Ophthalmol 2013;251:1987-93
70. Garrier J, Reshetov V, Zorin V, et al. Contrasting Facets of nanoparticules-based phototherapy: photo-damage and photo-regeneration. Nova Science Publishers, Inc; 2008
71. Lu Z, Dai T, Huang L, et al. Photodynamic therapy with a cationic functionalized fullerene rescues mice from fatal wound infections. Nanomedicine (Lond) 2010;5:1525-33
72. Huang YY, Tanaka M, Vecchio D, et al. Photodynamic therapy induces an immune response against a bacterial pathogen. Expert Rev Clin Immunol 2012;8:479-94
73. Sharma SK, Mroz P, Dai T, et al. Photodynamic Therapy for Cancer and for Infections: what Is the Difference? Isr J Chem 2012;52:691-705
74. Jori G, Fabris C, Soncin M, et al. Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications. Lasers Surg Med 2006;38:468-81
75. Morton CA, Szeimies RM, Sidoroff A, et al. European guidelines for topical photodynamic therapy part 1: treatment delivery and current indications-actinic keratoses, Bowen's disease, basal cell carcinoma. J Eur Acad Dermatol Venereol 2013;27:536-44
76. Morton CA, Szeimies RM, Sidoroff A, et al. European guidelines for topical photodynamic therapy part 2: emerging indications-field cancerization, photorejuvenation and inflammatory/ infective dermatoses. J Eur Acad Dermatol Venereol 2013;27:672-9
77. Hopper C. Photodynamic therapy: a clinical reality in the treatment of cancer. Lancet Oncol 2000;1:212-19
78. Barathan M, Mariappan V, Shankar EM, et al. Hypericin-photodynamic therapy leads to interleukin-6 secretion by HepG2 cells and their apoptosis via recruitment of BH3 interacting-domain death agonist and caspases. Cell Death Dis 2013;4:e697
79. Dai T, Tegos GP, Lu Z, et al. Photodynamic therapy for Acinetobacter baumannii burn infections in mice. Antimicrob Agents Chemother 2009;53: 3929-34
80. Gad F, Zahra T, Francis KP, et al. Targeted photodynamic therapy of established soft-tissue infections in mice. Photochem Photobiol Sci 2004;3:451-8
81. Tanaka M, Kinoshita M, Yoshihara Y, et al. Photodynamic therapy using intra-articular Photofrin for murine MRSA arthritis: biphasic light dose response for neutrophil-mediated antibacterial effect. Lasers Surg Med 2011;43:221-9
82. Tanaka M, Kinoshita M, Yoshihara Y, et al. Influence of intra-articular neutrophils on the effects of photodynamic therapy for murine MRSA arthritis. Photochem Photobiol 2010;86:403-9
83. Tanaka M, Mroz P, Dai T, et al. Photodynamic therapy can induce a protective innate immune response against murine bacterial arthritis via neutrophil accumulation. PLoS One 2012;7:e39823
84. Tanaka M, Mroz P, Dai T, et al. Linezolid and vancomycin decrease the therapeutic effect of methylene blue-photodynamic therapy in a mouse model of MRSA bacterial arthritis. Photochem Photobiol 2013;89:679-82
85. Ratkay LG, Chowdhary RK, Iamaroon A, et al. Amelioration of antigen-induced arthritis in rabbits by induction of apoptosis of inflammatory cells with local application of transdermal photodynamic therapy. Arthritis Rheum 1998;41:525-34
86. Ratkay LG, Chowdhary RK, Neyndorff HC, et al. Photodynamic therapy; a comparison with other immunomodulatory treatments of adjuvant-enhanced arthritis in MRL-lpr mice. Clin Exp Immunol 1994;95:373-7
87. Lebwohl M, Ali S. Treatment of psoriasis. Part 2. Systemic therapies. J Am Acad Dermatol 2001;45:649-61; quiz 62-4
88. Granstein RD, Matsui MS. UV radiation-induced immunosuppression and skin cancer. Cutis 2004;74:4-9
89. Boehncke WH, Konig K, Kaufmann R, et al. Photodynamic therapy in psoriasis: suppression of cytokine production in vitro and recording of fluorescence modification during treatment in vivo. Arch Dermatol Res 1994;286:300-3
90. Kleinpenning MM, Smits T, Ewalds E, et al. Heterogeneity of fluorescence in psoriasis after application of 5-aminolaevulinic acid: an immunohistochemical study. Br J Dermatol 2006;155:539-45
91. Kim JY, Kang HY, Lee ES, et al. Topical 5-aminolaevulinic acid photodynamic therapy for intractable palmoplantar psoriasis. J Dermatol 2007;34:37-40
92. Schleyer V, Radakovic-Fijan S, Karrer S, et al. Disappointing results and low tolerability of photodynamic therapy with topical 5-aminolaevulinic acid in psoriasis. A randomized, double-blind phase I/II study. J Eur Acad Dermatoly Venereol 2006;20:823-8
93. Tandon YK, Yang MF, Baron ED. Role of photodynamic therapy in psoriasis: a brief review. Photodermatol Photoimmunol Photomed 2008;24:222-30
94. Robinson DJ, Collins P, Stringer MR, et al. Improved response of plaque psoriasis after multiple treatments with topical 5-aminolaevulinic acid photodynamic therapy. Acta Derm Venereol 1999;79: 451-5
95. Choi YM, Adelzadeh L, Wu JJ. Photodynamic therapy for psoriasis. J Dermatolog Treat 2014;1-6. [Epub ahead of print]
96. Rook AH, Wood GS, Duvic M, et al. A phase II placebo-controlled study of photodynamic therapy with topical hypericin and visible light irradiation in the treatment of cutaneous T-cell lymphoma and psoriasis. J Am Acad Dermatol 2010;63:984-90
97. Brown S. Clinical antimicrobial photodynamic therapy: phase II studies in chronic wounds. J Natl Compr Canc Netw 2012;10(Suppl 2):S80-3
98. Borelli C, Merk K, Schaller M, et al. In vivo porphyrin production by P. acnes in untreated acne patients and its modulation by acne treatment. Acta Derm Venereol 2006;86:316-19
99. Ashkenazi H, Malik Z, Harth Y, et al. Eradication of Propionibacterium acnes by its endogenic porphyrins after illumination with high intensity blue light. FEMS Immunol Med Microbiol 2003;35:17-24
100. Kawada A, Aragane Y, Kameyama H, et al. Acne phototherapy with a high-intensity, enhanced, narrow-band, blue light source: an open study and in vitro investigation. J Dermatol Sci 2002;30:129-35
101. Yang GL, Zhao M, Wang JM, et al. Short-term clinical effects of photodynamic therapy with topical 5-aminolevulinic acid for facial acne conglobata: an open, prospective, parallel-arm trial. Photodermatolo Photoimmunol Photomed 2013;29:233-8
102. Yin R, Lin L, Xiao Y, et al.Combination ALA-PDT and ablative fractional Er:YAG laser (2,940 nm) on the treatment of severe acne. Lasers Surg Med 2014;46:165-72
103. Wiegell SR, Wulf HC. Photodynamic therapy of acne vulgaris using 5-aminolevulinic acid versus methyl aminolevulinate. J Am Acad Dermatol 2006;54:647-51
104. Wiegell SR, Wulf HC. Photodynamic therapy of acne vulgaris using methyl aminolaevulinate: a blinded, randomized, controlled trial. Br J Dermatol 2006;154: 969-76
105. Komerik N, Nakanishi H, MacRobert AJ, et al. In vivo killing of Porphyromonas gingivalis by toluidine blue-mediated photosensitization in an animal model. Antimicrob Agents Chemother 2003;47: 932-40
106. Qin YL, Luan XL, Bi LJ, et al. Comparison of toluidine blue-mediated photodynamic therapy and conventional scaling treatment for periodontitis in rats. J Periodontal Res 2008;43:162-7
107. Arweiler NB, Pietruska M, Skurska A, et al. Nonsurgical treatment of aggressive periodontitis with photodynamic therapy or systemic antibiotics. Three-month results of a randomized, prospective, controlled clinical study. Schweiz Monatsschr Zahnmed 2013;123:532-44
108. Mongardini C, Di Tanna GL, Pilloni A. Light-activated disinfection using a light-emitting diode lamp in the red spectrum: clinical and microbiological short-term findings on periodontitis patients in maintenance. A randomized controlled split-mouth clinical trial. Lasers Med Sci 2014;29:1-8
109. Ruhling A, Fanghanel J, Houshmand M, et al. Photodynamic therapy of persistent pockets in maintenance patients-a clinical study. Clin Oral Investig 2010;14:637-44
110. Gupta A, Avci P, Sadasivam M, et al. Shining light on nanotechnology to help repair and regeneration. Biotechnol Adv 2013;31:607-31
111. Ramalho KM, Luiz AC, de Paula Eduardo C, et al. Use of laser phototherapy on a delayed wound healing of oral mucosa previously submitted to radiotherapy: case report. Int Wound J 2011;8:413-18
112. Kaviani A, Djavid GE, Ataie-Fashtami L, et al. A randomized clinical trial on the effect of low-level laser therapy on chronic diabetic foot wound healing: a preliminary report. Photomed Laser Surg 2011;29: 109-14
113. Aykol G, Baser U, Maden I, et al. The effect of low-level laser therapy as an adjunct to non-surgical periodontal treatment. J Periodontol 2011;82:481-8
114. Moneib H, Tawfik AA, Youssef SS, et al. Randomized split-face controlled study to evaluate 1550-nm fractionated erbium glass laser for treatment of acne vulgaris-an image analysis evaluation. Dermatol Surg 2014;40:1191-200