Research progress of photodynamic therapy for osteomyelitis

doi:10.3969/j.issn.1000-1565.2022.02.014

Abstract

Abstract: Osteomyelitis is an infectious inflammation of deep tissues caused by bacterial infection. Persistent infection will lead to dissolution and necrosis of bone tissues. At present, it is difficult to cure osteomyelitis completely by surgical treatment and antibiotic treatment, and long-term use of antibiotics will make bacteria resistant, which makes it more difficult to treat osteomyelitis. Photodynamic antibacterial chemotherapy(PACT)is a new method of anti-infection treatment. Infection caused by drug-resistant bacteria has a good curative effect. This paper introduces the causes of refractory osteomyelitis, the advantages of PACT in the treatment of osteomyelitis and the recent experimental research progress. With the in-depth study of PACT for osteomyelitis, PACT is expected to become a new method to completely cure osteomyelitis.

Key words: photodynamic antibacterial chemotherapy(PACT), osteomyelitis, photosensitizer, multi-drug resistant bacteria

CLC Number:

ZHAO Jianxi, YIN Xiujuan, FANG Ziyuan, DU Zishuo, ZHU Lin, ZHAO Zhanjuan. Research progress of photodynamic therapy for osteomyelitis[J]. Journal of Hebei University(Natural Science Edition), 2022, 42(2): 199-207.

References

[1] XU C P, CHEN Y, SUN H T, et al. Efficacy of NEMO-binding domain peptide used to treat experimental osteomyelitis caused by methicillin-resistant Staphylococcus aureus: an in-vivo study[J]. Antimicrob Resist Infect Control, 2019, 8: 182. DOI:10.1186/s13756-019-0627-y.
[2] SURDU-BOB C C, COMAN C, BARBUCEANU F, et al. The influence of foreign body surface area on the outcome of chronic osteomyelitis[J]. Med Eng Phys, 2016,38(9): 870-876. DOI:10.1016/j.medengphy.2016.04.0 27.
[3] JENNISON T, MCNALLY M, PANDIT H. Prevention of infection in external fixator pin sites[J]. Acta Biomater, 2014, 10(2): 595-603. DOI:10.1016/j.actbio.2013.09.019.
[4] OBRIEN C L, MENON M, JOMHA N M. Controversies in the management of open fractures[J]. Open Orthop J, 2014, 8(1): 178-184. DOI:10.2174/1874325001408010178.
[5] MALIZOS K N, GOUGOULIAS N E, DAILIANA Z H, et al. Ankle and foot osteomyelitis: treatment protocol and clinical results[J]. Injury, 2010, 41(3): 285-293. DOI:10.1016/j.injury.2009.09.010.
[6] TSCHUDIN-SUTTER S, FREI R, DANGEL M, et al. Validation of a treatment algorithm for orthopaedic implant-related infections with device-retention-results from a prospective observational cohort study[J]. Clin Microbiol Infect, 2016, 22(5): 457.e1-457.e9. DOI:10.1016/j.cmi.2016.01.004.
[7] TAVARES A, CARVALHO C M, FAUSTINO M A, et al. Antimicrobial photodynamic therapy: study of bacterial recovery viability and potential development of resistance after treatment[J]. Mar Drugs, 2010, 8(1): 91-105. DOI:10.3390/md8010091.
[8] THORPE K E, JOSKI P, JOHNSTON K J. Antibiotic-resistant infection treatment costs have doubled since 2002, now exceeding $2 billion annually[J]. Health Aff(Millwood), 2018, 37(4): 662-669. DOI:10.1377/hlthaff.2017.1153.
[9] ZHANG X, LU Q, LIU T, et al. Bacterial resistance trends among intraoperative bone culture of chronic osteomyelitis in an affiliated hospital of South China for twelve years[J]. BMC Infect Dis, 2019, 19(1): 823. DOI:10.1186/s12879-019-4460-y.
[10] SHIPITSYNA I V, OSIPOVA E V, ASTASHOVA O A, et al. Monitoring of the leading causative agents of osteomyelitis and their antibiotic resistance[J]. Klin Lab Diagn, 2020, 65(9): 562-566. DOI:10.18821/0869-2084-2020-65-9-562-566.
[11] ANAGNOSTAKOS K, WILMES P, SCHMITT E, et al. Elution of gentamicin and vancomycin from polymethylmethacrylate beads and hip spacers in vivo[J]. Acta Orthop, 2009, 80(2): 193-197. DOI:10.3109/17453670902884700.
[12] BARRETT R J, SANDQUIST L, RICHARDS B F, et al. Antibiotic-impregnated polymethylmethacrylate as an anterior biomechanical device for the treatment of cervical discitis and vertebral osteomyelitis: technical report of two cases[J]. Turkish Neurosurg, 2014, 24(4): 613-617. DOI:10.5137/1019-5149.jtn.9380-13.0.
[13] JEVONS M P. “Celbenin”-resistant staphylococci[J]. BMJ, 1961, 1(5219): 124-125. DOI:10.1136/bmj.1.5219.12 4-a.
[14] HEROLD B C, IMMERGLUCK L C, MARANAN M C, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk[J]. Jama, 1998, 279(8): 593-598. DOI:10.1001/jama.279.8.593.
[15] DAGHER M, RUFFIN F, MARSHALL S, et al. Case report: successful rescue therapy of extensively drug-resistant acinetobacter baumannii osteomyelitis with cefiderocol[J]. Open Forum Infect Dis, 2020, 7(5): ofaa150. DOI:10.1093/ofid/ofaa150.
[16] TANDE A J, OSMON D R, GREENWOOD-QUAINTANCE K E, et al. Clinical characteristics and outcomes of prosthetic joint infection caused by small colony variant staphylococci[J]. mBio, 2014, 5(5): e01910-e01914. DOI:10.1128/mbio.01910-14.
[17] GRAMMATICO-GUILLON L, BARON S, GETTNER S, et al. Bone and joint infections in hospitalized patients in France, 2008: clinical and economic outcomes[J]. J Hosp Infect, 2012, 82(1): 40-48. DOI:10.1016/j.jhin.2012. 04.025.
[18] KARAU M J, SCHMIDT-MALAN S M, ALBANO M, et al. Novel use of rifabutin and rifapentine to treat methicillin-resistant staphylococcus aureus in a rat model of foreign body osteomyelitis[J]. J Infect Dis, 2020, 222(9): 1498-1504. DOI:10.1093/infdis/jiaa401.
[19] ARCHER N K, MAZAITIS M J, COSTERTON J W, et al. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease[J]. Virulence, 2011, 2(5): 445-459. DOI:10.4161/viru.2.5.17724.
[20] JOHNSON C T, WROE J A, AGARWAL R, et al. Hydrogel delivery of lysostaphin eliminates orthopedic implant infection by Staphylococcus aureus and supports fracture healing[J]. PNAS, 2018, 115(22): E4960-E4969. DOI:10.1073/pnas.1801013115.
[21] GRAF A C, LEONARD A, SCHÄUBLE M, et al. Virulence factors produced by staphylococcus aureus biofilms have a moonlighting function contributing to biofilm integrity[J]. Mol Cell Proteom, 2019, 18(6): 1036-1053. DOI:10.1074/mcp.RA118.001120.
[22] LUO Y, YANG Q Q, ZHANG D, et al. Mechanisms and control strategies of antibiotic resistance in pathological biofilms[J]. J Microbiol Biotechnol, 2021, 31(1): 1-7. DOI:10.4014/jmb.2010.10021.
[23] XU Y Y, ZHANG B P, WANG L, et al. Unusual features and molecular pathways of Staphylococcus aureus L-form bacteria[J]. Microb Pathog, 2020, 140: 103970. DOI:10.1016/j.micpath.2020.103970.
[24] 陈晓东,周之德,胡汝麒,等. 慢性化脓性骨髓炎与细菌L型感染的关系[J]. 中国矫形外科杂志,2000,7(2):134. DOI:10.3969/j.issn.1005-8478.2000.02.031.
[25] SPERANDIO F F, HUANG Y Y, HAMBLIN M R. Antimicrobial photodynamic therapy to kill Gram-negative bacteria[J]. Recent Pat Antiinfect Drug Discov, 2013, 8(2): 108-120. DOI:10.2174/1574891x113089990012.
[26] WU M, XU L, CAI Z, et al. Disinfection of cariogenic pathogens in planktonic lifestyle, biofilm and carious dentine with antimicrobial photodynamic therapy[J]. Photochem Photobiol, 2020, 96(1): 170-177. DOI:10.1111/php.13161.
[27] MAISCH T. A new strategy to destroy antibiotic resistant microorganisms: antimicrobial photodynamic treatment[J]. Mini Rev Med Chem, 2009, 9(8): 974-983. DOI:10.2174/138955709788681582.
[28] BISLAND S K, BURCH S. Photodynamic therapy of diseased bone[J]. Photodiagnosis Photodyn Ther, 2006, 3(3): 147-155. DOI:10.1016/S1572-1000(06)00036-6.
[29] BISLAND S K, CHIEN C, WILSON B C, et al. Pre-clinical in vitro and in vivo studies to examine the potential use of photodynamic therapy in the treatment of osteomyelitis[J]. Photochem Photobiol Sci, 2006, 5(1): 31-38. DOI:10.1039/b507082a.
[30] LU X, CHEN R, LV J, et al. High-resolution bimodal imaging and potent antibiotic/photodynamic synergistic therapy for osteomyelitis with a bacterial inflammation-specific versatile agent[J]. Acta Biomater, 2019, 99: 363-372. DOI:10.1016/j.actbio.2019.08.043.
[31] JORI G, FABRIS C, SONCIN M, et al. Photodynamic therapy in the treatment of microbial infections: basic principles and perspective applications[J]. Lasers Surg Med, 2006, 38(5): 468-481. DOI:10.1002/lsm.20361.
[32] GOTO B, IRIUCHISHIMA T, HORAGUCHI T, et al. Therapeutic effect of photodynamic therapy using Na-pheophorbide A on osteomyelitis models in rats[J]. Photomed Laser Surg, 2011, 29(3): 183-189. DOI:10.1089/pho.2010.2803.
[33] TARDIVO J P, BAPTISTA M S. Treatment of osteomyelitis in the feet of diabetic patients by photodynamic antimicrobial chemotherapy[J]. Photomed Laser Surg, 2009, 27(1): 145-150. DOI:10.1089/pho.2008.2252.
[34] KLAUSEN M, UCUNCU M, BRADLEY M. Design of photosensitizing agents for targeted antimicrobial photodynamic therapy[J]. Molecules, 2020, 25(22): 5239. DOI:10.3390/molecules25225239.
[35] KHAYYAT S A, ROSELIN L S. Recent progress in photochemical reaction on main components of some essential oils[J]. J Saudi Chem Soc, 2018, 22(7): 855-875. DOI:10.1016/j.jscs.2018.01.008.
[36] BOYLE R W, DOLPHIN D. Structure and biodistribution relationships of photodynamic sensitizers[J]. Photochem Photobiol, 1996, 64(3): 469-485. DOI:10.1111/j.1751-1097.1996.tb03093.x.
[37] ZHANG X, ABID S, SHI L M, et al. New conjugated meso-tetrathienylporphyrin-cored derivatives as two-photon photosensitizers for singlet oxygen generation[J]. Dyes Pigments, 2018, 153: 248-255. DOI:10.1016/j.dyepig.2018.01.028.
[38] BELYKH D V, KOZLOV A S, PYLINA Y I, et al. Copper сomplexes of сhlorin derivatives of chlorophyll a as potential photosensitizers for medical purposes[J]. Macroheterocycles, 2019, 12(1): 68-74. DOI:10.6060/mhc19 0128b.
[39] SELMAN S H, HAMPTON J A, MORGAN A R, et al. Copper benzochlorin, a novel photosensitizer for photodynamic therapy: effects on a transplantable urothelial tumor[J]. Photochem Photobiol, 1993, 57(4): 681-685. DOI:10.1111/j.1751-1097.1993.tb02937.x.
[40] BALÇIK-ERÇIN P, ÇETIN M, GÖKSEL M, et al. Improved targeting for photodynamic therapy via a biotin-phthalocyanine conjugate: synthesis, photophysical and photochemical measurements, and in vitro cytotoxicity assay[J]. New J Chem, 2020, 44(8): 3392-3401. DOI:10.1039/c9nj04991f.
[41] JIA R, TIAN W, BAI H, et al. Sunlight-driven wearable and robust antibacterial coatings with water-soluble cellulose-based photosensitizers[J]. Adv Healthc Mater, 2019, 8(5): e1801591. DOI:10.1002/adhm.201801591.
[42] WANG S, WANG X, YU L M, et al. Progress and trends of photodynamic therapy: from traditional photosensitizers to AIE-based photosensitizers[J]. Photodiagnosis Photodyn Ther, 2021, 34: 102254. DOI:10.1016/j.pdpdt.2021.102254.
[43] YIN Y, CHEN Z, YANG Y, et al. Thiophene-containing tetraphenylethene derivatives with different aggregation-induced emission(AIE)and mechanofluorochromic characteristics[J]. RSC Adv, 2019, 9(42): 24338-24343. DOI:10.1039/c9ra04611a.
[44] CHEN K Q, ZHANG R Y, WANG Z M, et al. Structural modification orientated multifunctional AIE fluorescence probes: organelles imaging and effective photosensitizer for photodynamic therapy[J]. Adv Optical Mater, 2020, 8(2): 1901433. DOI:10.1002/adom.201901433.
[45] CHEN Y, AI W, GUO X, et al. Mitochondria-targeted polydopamine nanocomposite with AIE photosensitizer for image-guided photodynamic and photothermal tumor ablation[J]. Small, 2019, 15(30): e1902352. DOI:10.1002/smll.201902352.
[46] LI Y Y, PENG Q C, LI S J, et al. A multifunctional quinoxalin-based AIEgen used for fluorescent thermo-sensing and image-guided photodynamic therapy[J]. Sens Actuat B Chem, 2019, 301: 127139. DOI:10.1016/j.snb.2019.127139.
[47] GAO H, BAO P, DAI S, et al. Far-red/near-infrared emissive(1, 3-dimethyl)barbituric acid-based AIEgens for high-contrast detection of metastatic tumors in the lung[J]. Chem Asian J, 2019, 14(6): 871-876. DOI:10.1002/asia.201801660.
[48] ALAM P, HE W, LEUNG N L C, et al. Red AIE-active fluorescent probes with tunable organelle-specific targeting[J]. Adv Funct Mater, 2020, 30(10): 1909268. DOI:10.1002/adfm.201909268.
[49] LIU J T, DU P, LIU T R, et al. A black phosphorus/manganese dioxide nanoplatform: oxygen self-supply monitoring, photodynamic therapy enhancement and feedback[J]. Biomaterials, 2019, 192: 179-188. DOI:10.1016/j.biomaterials.2018.10.018.
[50] CHEN Q, LIANG C, SUN X, et al. H₂O₂-responsive liposomal nanoprobe for photoacoustic inflammation imaging and tumor theranostics via in vivo chromogenic assay[J]. PNAS, 2017, 114(21): 5343-5348. DOI:10.1073/pnas.1701976114.
[51] SALEHPOUR F, RASTA S H, MOHADDES G, et al. Therapeutic effects of 10-HzPulsed wave lasers in rat depression model: a comparison between near-infrared and red wavelengths[J]. Lasers Surg Med, 2016, 48(7): 695-705. DOI:10.1002/lsm.22542.
[52] SALEHPOUR F, CASSANO P, ROUHI N, et al. Penetration profiles of visible and near-infrared lasers and light-emitting diode light through the head tissues in animal and human species: a review of literature[J]. Photobiomodul Photomed Laser Surg, 2019, 37(10): 581-595. DOI:10.1089/photob.2019.4676.
[53] NÖTZLI H P, SWIONTKOWSKI M F, THAXTER S T, et al. Laser Doppler flowmetry for bone blood flow measurements: helium-neon laser light attenuation and depth of perfusion assessment[J]. J Orthop Res, 1989, 7(3): 413-424. DOI:10.1002/jor.1100070314.
[54] DAI T, TEGOS G P, ZHIYENTAYEV T, et al. Photodynamic therapy for methicillin-resistant Staphylococcus aureus infection in a mouse skin abrasion model[J]. Lasers Surg Med, 2010, 42(1): 38-44. DOI:10.1002/lsm.20887.
[55] LIU Y, QIN R, ZAAT S A J, et al. Antibacterial photodynamic therapy: overview of a promising approach to fight antibiotic-resistant bacterial infections[J]. J Clin Transl Res, 2015, 1(3): 140-167.
[56] BARTOLOMEU M, ROCHA S, CUNHA Â, et al. Effect of photodynamic therapy on the virulence factors of staphylococcus aureus[J]. Front Microbiol, 2016, 7: 267. DOI:10.3389/fmicb.2016.00267.
[57] HAJIM K I, SALIH D S, RASSAM Y Z. Laser light combined with a photosensitizer may eliminate methicillin-resistant strains of Staphylococcus aureus[J]. Lasers Med Sci, 2010, 25(5): 743-748. DOI:10.1007/s 10103-010-0803-z.
[58] MALÁ Z, ZˇRSKÁ L, BAJGAR R, et al. The application of antimicrobial photodynamic inactivation on methicillin-resistant S. aureus and ESBL-producing K. pneumoniae using porphyrin photosensitizer in combination with silver nanoparticles[J]. Photodiagnosis Photodyn Ther, 2021, 33: 102140. DOI:10.1016/j.pdpdt.2020.102140.
[59] XU Z, GAO Y, MENG S, et al. Mechanism and in vivo evaluation: photodynamic antibacterial chemotherapy of lysine-porphyrin conjugate[J]. Front Microbiol, 2016, 7: 242. DOI:10.3389/fmicb.2016.00242.
[60] GARCEZ A S, KAPLAN M, JENSEN G J, et al. Effects of antimicrobial photodynamic therapy on antibiotic-resistant Escherichia coli[J]. Photodiagnosis Photodyn Ther, 2020, 32: 102029. DOI:10.1016/j. pdpdt.2020.102029.
[61] ROSA L P, SILVA F C, NADER S A, et al. In vitro effectiveness of antimicrobial photodynamic therapy(APDT)using a 660nm laser and malachite green dye in Staphylococcus aureus biofilms arranged on compact and cancellous bone specimens[J]. Lasers Med Sci, 2014, 29(6): 1959-1965. DOI:10.1007/s10103-014-1613-5.
[62] BANERJEE S, GHOSH D, VISHAKHA K, et al. Photodynamic antimicrobial chemotherapy(PACT)using riboflavin inhibits the mono and dual species biofilm produced by antibiotic resistant Staphylococcus aureus and Escherichia coli[J]. Photodiagnosis Photodyn Ther, 2020, 32: 102002. DOI:10.1016/j.pdpdt.2020.102002.
[63] DOSREIS J A Jr, DOSSANTOS J N, BARRETO B S, et al. Photodynamic antimicrobial chemotherapy(PACT)in osteomyelitis induced by Staphylococcus aureus: Microbiological and histological study[J]. J Photochem Photobiol B Biol, 2015, 149: 235-242. DOI:10.1016/j.jphotobiol.2015.06.005.
[64] 马金超,刘天盛,刘爱鹏,等.光动力抗微生物化学疗法修复骨髓炎模型兔的实验[J].中国组织工程研究, 2020, 24(8): 1254-1259. DOI:10.3969/j.issn.2095-4344.2480.
[65] LINDBLOOM B J, JAMES E R, MCGARVEY W C. Osteomyelitis of the foot and ankle: diagnosis, epidemiology, and treatment[J]. Foot Ankle Clin, 2014, 19(3): 569-588. DOI:10.1016/j.fcl.2014.06.012.
[66] FAGLIA E, CLERICI G, CAMINITI M, et al. Influence of osteomyelitis location in the foot of diabetic patients with transtibial amputation[J]. Foot Ankle Int, 2013, 34(2): 222-227. DOI:10.1177/1071100712467436.
[67] TARDIVO J P, ADAMI F, CORREA J A, et al. A clinical trial testing the efficacy of PDT in preventing amputation in diabetic patients[J]. Photodiagnosis Photodyn Ther, 2014, 11(3): 342-350. DOI:10.1016/j.pdpdt.2014.04.007.
[68] TARDIVO J P, SERRANO R, ZIMMERMANN L M, et al. Is surgical debridement necessary in the diabetic foot treated with photodynamic therapy? [J]. Diabet Foot Ankle, 2017, 8(1): 1373552. DOI:10.1080/2000625 X.2017.1373552.
[69] GARCIA V G, LIMA M A, OKAMOTO T, et al. Effect of photodynamic therapy on the healing of cutaneous third-degree-burn: histological study in rats[J]. Lasers Med Sci, 2010, 25(2): 221-228. DOI:10.1007/s10103-009-0694-z. (