Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
권호 표지
DOI QR코드

DOI QR Code

Therapeutic effect of marine bioactive substances against periodontitis based on in vitro, in vivo, and clinical studies

  • Tae-Hee Kim (Research Center for Marine-Integrated Bionics Technology, Pukyong National University) ;
  • Se-Chang Kim (Marine Integrated Biomedical Technology Center, The National Key Research Institutes in Universities, Pukyong National University) ;
  • Won-Kyo Jung (Research Center for Marine-Integrated Bionics Technology, Pukyong National University)
  • Received : 2022.08.19
  • Accepted : 2022.11.05
  • Published : 2023.01.30
Download PDF
⟨ Previous Next ⟩

Abstract

Marine bioactive substances (MBS), such as phlorotannins, collagens, peptides, sterols, and polysaccharides, are increasing attention as therapeutic agents for several diseases due to their pharmacological effects. Previous studies have demonstrated the biological activities of MBS including antibacterial, anticoagulant, antidiabetic, antimicrobial, anti-inflammatory activities. Among numerous human diseases, periodontitis is one of the high-prevalence inflammatory diseases in the world. To treat periodontitis, several surgeries (bone grafting, flap surgery, and soft tissue graft) are usually used. However, the surgery for patients with chronic periodontitis induces several side effects, including additional inflammatory responses at the operated site, chronic wound healing, and secondary surgery. Therefore, this review assessed the most recent trends in MBS using Google Scholar, PubMed, and Web of Science search engines to develop marine-derived therapeutic agents for periodontitis. Further, we summarized the current applications and therapeutic potential of MBS to serve as a reference for developing novel technologies applied to MBS against periodontitis treatment.

Keywords

Acknowledgement

This research was financially supported by the Research Grant of Pukyong National University (2021).

References

  1. Achmad H, Djais AI, Jannah M, Carmelita AB, Uinarni H, Arifin EM, et al. Antibacterial chitosan of milkfish scales (Chanos chanos) on bacteria Prophyromonas gingivalis & Agregatibacter actinomycetemcomitans. Syst Rev Pharm. 2020a;11:836-41.
  2. Achmad H, Huldani, Carmelita AB, Fauziah, Hidayah N, Bokov D. Antioxidant and antiviral potential of brown algae (Phaeophyceae). Int J Pharm Res. 2020b;3:2117-25.
  3. Adam M, Achmad H, Nasir M, Putri SW, Azizah A, Satya DE. Stimulation of osteoblast and osteocalcin in the bone regeneration by giving bonegraft golden sea cucumber. J Int Dent Med Res. 2022;15:140-7.
  4. Alden Schnyder Jason D, Magesh KT, Aravindhan R, Sathya Kumar M. Evaluation of antibacterial activity of marine brown algae Turbinaria conoides against oral pathogens. Res J Pharm Technol. 2022;15:2236-9. https://doi.org/10.52711/0974-360X.2022.00371
  5. Andriopoulos V, Gkioni MD, Koutra E, Mastropetros SG, Lamari FN, Hatziantoniou S, et al. Total phenolic content, biomass composition, and antioxidant activity of selected marine microalgal species with potential as aquaculture feed. Antioxidants. 2022;11:1320.
  6. Antona ME, Ramos C, Stranges A, Monteiro AF, Chaves MMG, Mandalunis P, et al. Fish oil diet effects on alveolar bone loss, in hypercholesterolemic rats. Arch Oral Biol. 2020;109:104553.
  7. Arslan YE, Kantarcioglu I. Salvadora persica extract-laden jellyfish collagen hybrid constructs for periodontal tissue regeneration. J Turk Chem Soc Chem. 2019;6:51-62. https://doi.org/10.18596/jotcsa.484936
  8. Asari MA, Sirajudeen KNS, Yusof NAM, Amin MSIM. DHA-rich fish oil and Tualang honey reduce chronic stress-induced oxidative damage in the brain of rat model. J Tradit Complement Med. 2021;12:361-6. https://doi.org/10.1016/j.jtcme.2021.10.001
  9. Bai YL, Zheng TJ, Zhang ZW, Gan Y, Huang J. Efficacy of minocycline hydrochloride combined with flap surgery for chronic periodontitis: a meta-analysis. West China J Stomatol. 2018;36:421-7.
  10. Batool F, Petit C, Stutz C, Ozcelik H, Gegout PY, Benkirane-Jessel N, et al. M101, a therapeutic oxygen carrier derived Arenicola marina, decreased Porphyromonas gingivalis-induced hypoxia and improved periodontal healing. J Periodontol. 2022;93:1712-24. https://doi.org/10.1002/JPER.22-0006
  11. Batool F, Stutz C, Petit C, Benkirane-Jessel N, Delpy E, Zal F, et al. A therapeutic oxygen carrier isolated from Arenicola marina decreased P. gingivalis induced inflammation and tissue destruction. Sci Rep. 2020;10:14745.
  12. Campana R, Mangiaterra G, Tiboni M, Frangipani E, Biavasco F, Lucarini S, et al. A fluorinated analogue of marine bisindole alkaloid 2,2-bis(6-bromo-1H-indol-3-yl) ethanamine as potential anti-biofilm agent and antibiotic adjuvant against Staphylococcus aureus. Pharmaceuticals. 2020;13:210.
  13. Chandika P, Oh GW, Heo SY, Kim SC, Kim TH, Kim MS, et al. Electrospun porous bilayer nano-fibrous fish collagen/ PCL bio-composite scaffolds with covalently cross-linked chitooligosaccharides for full-thickness wound-healing applications. Mater Sci Eng C. 2021;121:111871.
  14. Cherian C, Jannet Vennila J, Sharan L. Marine bromophenols as an effective inhibitor of virulent proteins (peptidyl arginine deiminase, gingipain R and hemagglutinin A) in Porphyromas gingivalis. Arch Oral Biol. 2019;100:119-28. https://doi.org/10.1016/j.archoralbio.2019.02.016
  15. Costa FO, Lages EJP, Lages EMB, Cota LOM. Periodontitis in individuals with liver cirrhosis: a case-control study. J Clin Periodontol. 2019;46:991-8. https://doi.org/10.1111/jcpe.13172
  16. Cotas J, Leandro A, Pacheco D, Goncalves AMM, Pereira L. A comprehensive review of the nutraceutical and therapeutic applications of red seaweeds (Rhodophyta). Life. 2020;10:19.
  17. Cui C, Sun S, Wu S, Chen S, Ma J, Zhou F. Electrospun chitosan nanofibers for wound healing application. Eng Regen. 2021;2:82-90. https://doi.org/10.1016/j.engreg.2021.08.001
  18. da Silva FRP, Pinto MSC, de Carvalho Franca LF, Alves EHP, dos Santos Carvalho J, Di Lenardo D, et al. Sulfated polysaccharides from the marine algae Gracilaria caudata prevent tissue damage caused by ligature-induced periodontitis. Int J Biol Macromol. 2019;132:1-8. https://doi.org/10.1016/j.ijbiomac.2019.03.194
  19. De Cubber L, Lefebvre S, Lancelot T, Denis L, Gaudron SM. Annelid polychaetes experience metabolic acceleration as other Lophotrochozoans: inferences on the life cycle of Arenicola marina with a dynamic energy budget model. Ecol Model. 2019;411:108773.
  20. De Domenico S, De Rinaldis G, Paulmery M, Piraino S, Leone A. Barrel jellyfish (Rhizostoma pulmo) as source of antioxidant peptides. Mar Drugs. 2019;17:134.
  21. Deng T, Feng Y, Xu L, Tian X, Lai X, Lyu M, et al. Expression, purification and characterization of a cold-adapted dextranase from marine bacteria and its ability to remove dental plaque. Protein Expr Purif. 2020;174:105678.
  22. Deshpande AP, Baburaj MD, Tambe LV, Prasad U. Extracellular matrix containing nanocomposite bone graft in periodontal regeneration - a randomized controlled clinical and radiographic evaluation. J Indian Soc Periodontol. 2021;25:313-9. https://doi.org/10.4103/jisp.jisp_440_20
  23. dos Santos NC, Araujo CF, Andere NMRB, Miguel MMV, Westphal MRA, Van Dyke T, et al. Omega-3 fatty acids and lowdose aspirin in the treatment of periodontitis and metabolic syndrome: case report. J Int Acad Periodontol. 2020;22:223-30.
  24. Eke PI, Borgnakke WS, Genco RJ. Recent epidemiologic trends in periodontitis in the USA. Periodontol 2000. 2020;82:257-67. https://doi.org/10.1111/prd.12323
  25. Elango J, Selvaganapathy PR, Lazzari G, Bao B, Wenhui W. Biomimetic collagen-sodium alginate-titanium oxide (TiO2) 3D matrix supports differentiated periodontal ligament fibroblasts growth for periodontal tissue regeneration. Int J Biol Macromol. 2020;163:9-18. https://doi.org/10.1016/j.ijbiomac.2020.06.173
  26. Elnagdy S, Raptopoulos M, Kormas I, Pedercini A, Wolff LF. Local oral delivery agents with anti-biofilm properties for the treatment of periodontitis and peri-implantitis. A narrative review. Molecules. 2021;26:5661.
  27. Gani A, Yulianty R, Supiaty S, Rusdy M, Dwipa Asri G, Eka Satya D, et al. Effectiveness of combination of chitosan gel and hydroxyapatite from crabs shells (Portunus pelagicus) waste as bonegraft on periodontal network regeneration through IL-1 and BMP-2 analysis. Int J Biomater. 2022;2022:1817236.
  28. Gao H, Kang N, Hu C, Zhang Z, Xu Q, Liu Y, et al. Ginsenoside Rb1 exerts anti-inflammatory effects in vitro and in vivo by modulating toll-like receptor 4 dimerization and NF-kB/MAPKs signaling pathways. Phytomedicine. 2020;69:153197.
  29. Guo H, Huang S, Yang X, Wu J, Kirk TB, Xu J, et al. Injectable and self-healing hydrogels with double-dynamic bond tunable mechanical, gel-sol transition and drug delivery properties for promoting periodontium regeneration in periodontitis. ACS Appl Mater Interfaces. 2021;13:61638-52. https://doi.org/10.1021/acsami.1c18701
  30. Han JM, Cho SD, Chung GH, Choi SJ, Shin JA, Hong SD, et al. Agarum clathratum inhibits LPS-induced IL-1β expression through the regulation of the JNK/c-Jun signaling pathway. Korean J Oral Maxillofac Pathol. 2021;45:111-20. https://doi.org/10.17779/KAOMP.2021.45.4.001
  31. Heo SY, Ko SC, Nam SY, Oh J, Kim YM, Kim JI, et al. Fish bone peptide promotes osteogenic differentiation of MC3T3-E1 pre-osteoblasts through upregulation of MAPKs and Smad pathways activated BMP-2 receptor. Cell Biochem Funct. 2018;36:137-46. https://doi.org/10.1002/cbf.3325
  32. Hussain B, Karaca EO, Kuru BE, Gursoy H, Haugen HJ, Wohlfahrt JC. Treatment of residual pockets using an oscillating chitosan device versus regular curettes alone-a randomized, feasibility parallel-arm clinical trial. J Periodontol. 2022;93:780-9. https://doi.org/10.1002/JPER.21-0496
  33. Hussein HA, Mohamad H, Ghazaly MM, Laith AA, Abdullah MA. Anticancer and antioxidant activities of Nannochloropsis oculata and Chlorella sp. extracts in co-application with silver nanoparticle. J King Saud Univ Sci. 2020;32:3486-94. https://doi.org/10.1016/j.jksus.2020.10.011
  34. Ide M, Harris M, Stevens A, Sussams R, Hopkins V, Culliford D, et al. Periodontitis and cognitive decline in Alzheimer's disease. PLOS ONE. 2016;11:e0151081.
  35. Jalal AA, Al-Qassab ZA, Al-Rawi RA. Effects of the systemic administration of omega-3-polyunsaturated fatty acid on experimental periodontitis: a histopathological study for rat's periodontal tissue. Ann Trop Med Public Health. 2020a;23:SP231226.
  36. Jalal AA, Al-Qassab ZA, Al-Rawi RA. Effects of the systemic administration of omega-3 polyunsaturated fatty acid on experimental periodontitis (immunological analysis for rat's serum). Ann Trop Med Public Health. 2020b;23:SP231127.
  37. Jiang CS, Müller WEG, Schröder HC, Guo YW. Disulfide- and multisulfide-containing metabolites from marine organisms. Chem Rev. 2012;112:2179-207. https://doi.org/10.1021/cr200173z
  38. Johnson A, He JL, Kong F, Huang YC, Thomas S, Lin HTV, et al. Surfactin-loaded ĸ-carrageenan oligosaccharides entangled cellulose nanofibers as a versatile vehicle against periodontal pathogens. Int J Nanomedicine. 2020;15:4021-47. https://doi.org/10.2147/IJN.S238476
  39. Jung JI, Kim S, Baek SM, Choi SI, Kim GH, Imm JY. Ecklonia cava extract exerts anti-inflammatory effect in human gingival fibroblasts and chronic periodontitis animal model by suppression of pro-inflammatory cytokines and chemokines. Foods. 2021;10:1656.
  40. Kang MS, Moon JH, Park SC, Jang YP, Choung SY. Spirulina maxima reduces inflammation and alveolar bone loss in Porphyromonas gingivalis-induced periodontitis. Phytomedicine. 2021;81:153420.
  41. Kao YF, Tu MC, Chai HJ, Lin YL, Chen YC. Suppressive effects of an apoptotic mimicry prepared from jumbo-flying squidskin phospholipids on the osteoclastogenesis in receptor activator of nuclear factor kappa B ligand/macrophage colony-stimulating factor-induced RAW 264.7 cells. J Chin Med Assoc. 2021;84:51-60. https://doi.org/10.1097/JCMA.0000000000000447
  42. Ke CL, Deng FS, Chuang CY, Lin CH. Antimicrobial actions and applications of chitosan. Polymers. 2021;13:904.
  43. Kim EN, Nabende WY, Jeong H, Hahn D, Jeong GS. The marine-derived natural product epiloliolide isolated from Sargassum horneri regulates NLRP3 via PKA/CREB, promoting proliferation and anti-inflammatory effects of human periodontal ligament cells. Mar Drugs. 2021a; 19:388.
  44. Kim GH, Park HH, Chandika P, Ko SC, Jung KM, Yoon SC, et al. Chemical compositions and biological activities of marine invertebrates from the East Sea of South Korea. Fish Aquat Sci. 2019a; 22:13.
  45. Kim H, Kim MB, Kim C, Hwang JK. Inhibitory effects of panduratin A on periodontitis-induced inflammation and osteoclastogenesis through inhibition of MAPK pathways in vitro. J Microbiol Biotechnol. 2018;28:190-8. https://doi.org/10.4014/jmb.1707.07042
  46. Kim S, Choi SI, Kim GH, Imm JY. Anti-inflammatory effect of Ecklonia cava extract on Porphyromonas gingivalis lipopolysaccharide-stimulated macrophages and a periodontitis rat model. Nutrients. 2019b; 11:1143.
  47. Kim SC, Heo SY, Oh GW, Yi M, Jung WK. A 3D-printed polycaprolactone/marine collagen scaffold reinforced with carbonated hydroxyapatite from fish bones for bone regeneration. Mar Drugs. 2022a;20:344.
  48. Kim TH, Heo SY, Oh GW, Heo SJ, Jung WK. Applications of marine organism-derived polydeoxyribonucleotide: its potential in biomedical engineering. Mar Drugs. 2021b;19:296.
  49. Kim TH, Heo SY, Oh GW, Park WS, Choi IW, Kang HW, et al. A phlorotannins-loaded homogeneous acellular matrix film modulates post-implantation inflammatory responses. J Tissue Eng Regen Med. 2022b; 16:51-62. https://doi.org/10.1002/term.3258
  50. Kim TH, Jung WK. R&D trends of brown algae as potential candidates in biomedical application. J Mar Biosci Biotechnol. 2019;11:1-13.
  51. Kim TH, Ko SC, Oh GW, Park HH, Lee DS, Yim MJ, et al. Studies on bioactive substances and antioxidant activities of marine algae from Jeju island. J Mar Biosci Biotechnol. 2016;8:30-8. https://doi.org/10.15433/ksmb.2016.8.1.030
  52. Kim TH, Lee HS, Oh SJ, Hwang CW, Jung WK. Phlorotannins ameliorate extracellular matrix production in human vocal fold fibroblasts and prevent vocal fold fibrosis via aerosol inhalation in a laser-induced fibrosis model. J Tissue Eng Regen Med. 2020;14:1918-28. https://doi.org/10.1002/term.3140
  53. Kujur SK, Goswami V, Nikunj AM, Singh G, Bandhe S, Ghritlahre H. Efficacy of omega 3 fatty acid as an adjunct in the management of chronic periodontitis: a randomized controlled trial. Indian J Dent Res. 2020;31:220-35. https://doi.org/10.4103/ijdr.IJDR_647_18
  54. Le Dare B, Ferron PJ, Bellamri N, Ribault C, Delpy E, Zal F, et al. A therapeutic oxygen carrier isolated from Arenicola marina decreases amanitin-induced hepatotoxicity. Toxicon. 2021;200:87-91. https://doi.org/10.1016/j.toxicon.2021.07.004
  55. Leal D, Mansilla A, Matsuhiro B, Moncada-Basualto M, Lapier M, Maya JD, et al. Chemical structure and biological properties of sulfated fucan from the sequential extraction of subAntarctic Lessonia sp (Phaeophyceae). Carbohydr Polym. 2018;199:304-13. https://doi.org/10.1016/j.carbpol.2018.07.012
  56. Lee HS, Jeong MS, Ko SC, Heo SY, Kang HW, Kim SW, et al. Fabrication and biological activity of polycaprolactone/ phlorotannin endotracheal tube to prevent tracheal stenosis: an in vitro and in vivo study. J Biomed Mater Res Part B. 2020;108:1046-56. https://doi.org/10.1002/jbm.b.34456
  57. Li B, Shi L, Liu R, Li Z, Cao S, Li J. A lingering mouthwash with sustained antibiotic release and biofilm eradication for periodontitis. J Mater Chem B. 2021;9:8694-707. https://doi.org/10.1039/D1TB01742J
  58. Liao Y, Li H, Shu R, Chen H, Zhao L, Song Z, et al. Mesoporous hydroxyapatite/chitosan loaded with recombinant-human amelogenin could enhance antibacterial effect and promote periodontal regeneration. Front Cell Infect Microbiol. 2020;10:180.
  59. Magesh KT, Aravindhan R, Kumar MS, Sivachandran A. Antibacterial efficacy of the extract of Sargassum Wightii against oral pathogen: an in vitro study. J Orofac Sci. 2020;12:96-100. https://doi.org/10.4103/jofs.jofs_80_20
  60. Matarese G, Ramaglia L, Cicciu M, Cordasco G, Isola G. The effects of diode laser therapy as an adjunct to scaling and root planning in the treatment of aggressive periodontitis: a 1-year randomized controlled clinical trial. Photomed Laser Surg. 2017;35:702-9. https://doi.org/10.1089/pho.2017.4288
  61. Mulawarmanti D, Parisihni K, Widyastuti. The effect of Sticopus hermanii-hyperbaric oxygen therapy to inflammatory response of diabetic periodontitis. IOP Conf Ser Earth Environ Sci. 2019a; 217:012060.
  62. Mulawarmanti D, Parisihni K, Widyastuti W. The effect of Sticopus hermaniii-hyperbaric oxygen therapy to osteogenesis of diabetic periodontitis. Diabetes Complicat. 2019b; 3:1-3. https://doi.org/10.33425/2639-9326.1060
  63. Murgia MS, Aspriello SD. Dietary supplementation with omega-3 alpha-linoleic acid and polyunsaturated fatty acids (PUFAs): a new therapeutic protocol additional to scaling and root planning in the treatment of chronic periodontitis: a 6 months follow up. J Dent Oral Disord Ther. 2021;9:1-7. https://doi.org/10.15226/jdodt.2021.001128
  64. Nguyen VT, Ko SC, Oh GW, Heo SY, Jeon YJ, Park W, et al. Anti-inflammatory effects of sodium alginate/gelatine porous scaffolds merged with fucoidan in murine microglial BV2 cells. Int J Biol Macromol. 2016;93:1620-32. https://doi.org/10.1016/j.ijbiomac.2016.05.078
  65. Oh GW, Nam SY, Heo SJ, Kang DH, Jung WK. Characterization of ionic cross-linked composite foams with different blend ratios of alginate/pectin on the synergistic effects for wound dressing application. Int J Biol Macromol. 2020;156:1565-73. https://doi.org/10.1016/j.ijbiomac.2019.11.206
  66. Oh GW, Nguyen VT, Heo SY, Ko SC, Kim CS, Park WS, et al. 3D PCL/fish collagen composite scaffolds incorporating osteogenic abalone protein hydrolysates for bone regeneration application: in vitro and in vivo studies. J Biomater Sci Polym Ed. 2021;32:355-71. https://doi.org/10.1080/09205063.2020.1834908
  67. Ohno O, Terasaki T, Sano T, Hitomi Y, Miyamoto J, Matsuno K. Inhibitory effects of biseokeaniamide A against lipopolysaccharide-induced signal transduction. Bioorg Med Chem Lett. 2020;30:127069.
  68. Ozcelik H, Batool F, Corre M, Garlaschelli A, Conzatti G, Stutz C, et al. Characterization of a hyaluronic acid-based hydrogel containing an extracellular oxygen carrier (M101) for periodontitis treatment: an in vitro study. Int J Pharm. 2021;605:120810.
  69. Ozdogan AI, Akca G, Senel S. Development and in vitro evaluation of gel formulation of atorvastatin solid dispersions. J Drug Deliv Sci Technol. 2021;61:102199.
  70. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, et al. Periodontitis: consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89:S173-82. https://doi.org/10.1002/JPER.17-0721
  71. Papapanou PN, Susin C. Periodontitis epidemiology: is periodontitis under-recognized, over-diagnosed, or both? Periodontol 2000. 2017;75:45-51. https://doi.org/10.1111/prd.12200
  72. Pech-Puch D, Perez-Povedano M, Martinez-Guitian M, Lasarte-Monterrubio C, Vazquez-Ucha JC, Bou G, et al. In vitro and in vivo assessment of the efficacy of bromoageliferin, an alkaloid isolated from the sponge Agelas dilatata, against Pseudomonas aeruginosa. Mar Drugs. 2020;18:326.
  73. Peers S, Montembault A, Ladaviere C. Chitosan hydrogels for sustained drug delivery. J Control Release. 2020;326:150-63. https://doi.org/10.1016/j.jconrel.2020.06.012
  74. Poornima P, Krithikadatta J, Ponraj RR, Velmurugan N, Kishen A. Biofilm formation following chitosan-based varnish or chlorhexidine-fluoride varnish application in patients undergoing fixed orthodontic treatment: a double blinded randomised controlled trial. BMC Oral Health. 2021;21:465.
  75. Potempa J, Mydel P, Koziel J. The case for periodontitis in the pathogenesis of rheumatoid arthritis. Nat Rev Rheumatol. 2017;13:606-20. https://doi.org/10.1038/nrrheum.2017.132
  76. Puscasu CG, Caraiane A, Dumea E, sachir EE, Raftu G, Puscasu RA, et al. Measurement of the clinical effects of a marine fish extract on periodontal healing-a preliminary clinical interventional study. Appl Sci. 2022;12:677.
  77. Rachmawati R, Hidayat M, Permatasari N, Widyarti S. Jellyfish (Aurelia aurita) collagen scaffolds potential in alveolar bone regeneration. F1000research. 2021;10:318.
  78. Rajabi M, McConnell M, Cabral J, Ali MA. Chitosan hydrogels in 3D printing for biomedical applications. Carbohydr Polym. 2021;260:117768.
  79. Rane R, Sahu N, Shah C, Karpoormath R. Marine bromopyrrole alkaloids: synthesis and diverse medicinal applications. Curr Top Med Chem. 2014;14:253-73. https://doi.org/10.2174/1568026613666131216110001
  80. Ratheesh V, Subramanian S, Prakash PSG, Victor DJ. Evaluation of association of vitamin D receptor genetic polymorphism with severe chronic periodontitis in an Ethnic Tamilian population. Genet Test Mol Biomark. 2018;22:615-21. https://doi.org/10.1089/gtmb.2018.0190
  81. Ren D, Wang Q, Yang Y, Hu Y, Song Y, He Y, et al. Hypolipidemic effects of fucoidan fractions from Saccharina sculpera (Laminariales, Phaeophyceae). Int J Biol Macromol. 2019;140:188-95. https://doi.org/10.1016/j.ijbiomac.2019.08.002
  82. Revianti S, Andriani D, Parisihni K, Wahjuningsih E. Effectiveness of oral irrigation with an extract of green microalga Nannochloropsis oculata as an anti-inflammatory in rats infected with Aggregatibacter actinomycetemcomitans. Biodivers J Biol Divers. 2020;21:2977-81.
  83. Ribeiro-Vidal H, Sanchez MC, Alonso-Espanol A, Figuero E, Ciudad MJ, Collado L, et al. Antimicrobial activity of EPA and DHA against oral pathogenic bacteria using an in vitro multi-species subgingival biofilm model. Nutrients. 2020;12:2812.
  84. Sadeghianmaryan A, Naghieh S, Sardroud HA, Yazdanpanah Z, Soltani YA, Sernaglia J, et al. Extrusion-based printing of chitosan scaffolds and their in vitro characterization for cartilage tissue engineering. Int J Biol Macromol. 2020;164:3179-92. https://doi.org/10.1016/j.ijbiomac.2020.08.180
  85. Samarakoon KW, Nam KO, Ko JY, Lee JH, Kang MC, Kim D, et al. Purification and identification of novel angiotensin-I converting enzyme (ACE) inhibitory peptides from cultured marine microalgae (Nannochloropsis oculata) protein hydrolysate. J Appl Phycol. 2013;25:1595-606. https://doi.org/10.1007/s10811-013-9994-6
  86. Sarhadizadeh N, Afkhami M, Ehsanpour M. Evaluation bioactivity of a sea cucumber, Stichopus hermanni from Persian Gulf. Eur J Exp Biol. 2014;4:254-8.
  87. Satpathy AA, Dash S, Das SK, Shyamasuta S, Pradhan S. Functional and bioactive properties of chitosan from Indian major carp scale. Aquacult Int. 2021;29:417-30. https://doi.org/10.1007/s10499-020-00622-0
  88. Sharan LV, Vennila JJ. Phyto-pharmacological investigation of marine red algae Kappaphycus alvarezii (Doty) doty ex silva for oral diseases. Int J Algae. 2021;23:183-209. https://doi.org/10.1615/InterJAlgae.v23.i2.40
  89. Shrestha S, Shrestha SM, Pradhan A, Aryal S. Platelet rich fibrin and bone graft in the treatment of intrabony defect in periodontitis patients. J Nepal Soc Periodontol Oral Implantol. 2018;2:49-55. https://doi.org/10.3126/jnspoi.v2i2.23614
  90. Slots J. Periodontitis: facts, fallacies and the future. Periodontol 2000. 2017;75:7-23. https://doi.org/10.1111/prd.12221
  91. Spanou A, Nelson K, Ermer MA, Steybe D, Poxleitner P, Voss PJ. Primary wound closure and perioperative antibiotic therapy for prevention of bisphosphonate-related osteonecrosis of the jaw after tooth extraction. Quintessence Int. 2020;51:220-8.
  92. Stando M, Piatek P, Namiecinska M, Lewkowicz P, Lewkowicz N. Omega-3 polyunsaturated fatty acids EPA and DHA as an adjunct to non-surgical treatment of periodontitis: a randomized clinical trial. Nutrients. 2020;12:2614.
  93. Sun X, Wang L, Lynch CD, Sun X, Li X, Qi M, et al. Nanoparticles having amphiphilic silane containing Chlorin e6 with strong anti-biofilm activity against periodontitis-related pathogens. J Dent. 2019;81:70-84. https://doi.org/10.1016/j.jdent.2018.12.011
  94. Suvan J, Leira Y, Moreno Sancho FM, Graziani F, Derks J, Tomasi C. Subgingival instrumentation for treatment of periodontitis. A systematic review. J Clin Periodontol. 2020;47:155-75. https://doi.org/10.1111/jcpe.13245
  95. Tang S, Zhang H, Mei L, Dou K, Jiang Y, Sun Z, et al. Fucoidan-derived carbon dots against Enterococcus faecalis biofilm and infected dentinal tubules for the treatment of persistent endodontic infections. J Nanobiotechnology. 2022;20:321.
  96. Tapia-Martinez J, Hernandez-Cruz K, Franco-Colin M, Mateo-Cid LE, Mendoza-Gonzalez C, Blas-Valdivia V, et al. Safety evaluation and antiobesogenic effect of Sargassum liebmannii J. Agardh (Fucales: Phaeophyceae) in rodents. J Appl Phycol. 2019;31:2597-607. https://doi.org/10.1007/s10811-019-1752-y
  97. Teeuw WJ, Kosho MXF, Poland DCW, Gerdes VEA, Loos BG. Periodontitis as a possible early sign of diabetes mellitus. BMJ Open Diabetes Res Care. 2017;5:e000326.
  98. Teughels W, Feres M, Oud V, Martin C, Matesanz P, Herrera D. Adjunctive effect of systemic antimicrobials in periodontitis therapy: a systematic review and meta-analysis. J Clin Periodontol. 2020;47:257-81. https://doi.org/10.1111/jcpe.13264
  99. Umnyakova ES, Gorbunov NP, Zhakhov AV, Krenev IA, Ovchinnikova TV, Kokryakov VN, et al. Modulation of human complement system by antimicrobial peptide arenicin-1 from Arenicola marina. Mar Drugs. 2018;16:480.
  100. Wahyuningtyas E, Hsu LC, Lan WC, Wen SC, Ou KL, Chou HH, et al. Application of a promising bone graft substitute in bone tissue regeneration: characterization, biocompatibility, and in vivo animal study. BioMed Res Int. 2019;2019:1614024.
  101. Wang R, Bao B, Bao C, Wang S, Ur Rahman S, Hou C, et al. Resveratrol and celastrol loaded collagen dental implants regulate periodontal ligament fibroblast growth and osteoclastogenesis of bone marrow macrophages. Chem Biodivers. 2020b;17:e2000295.
  102. Wang W, Meng Q, Li Q, Liu J, Zhou M, Jin Z, et al. Chitosan derivatives and their application in biomedicine. Int J Mol Sci. 2020a;21:487.
  103. Xu S, Zhou Q, Jiang Z, Wang Y, Yang K, Qiu X, et al. The effect of doxycycline-containing chitosan/carboxymethyl chitosan nanoparticles on NLRP3 inflammasome in periodontal disease. Carbohydr Polym. 2020;237:116163.
  104. Yoon HS, Kim HJ, Park CM. Anti-inflammatory activity of various seaweeds in LPS-PG stimulated HGF-1 cells. J Korean Soc Oral Health Sci. 2020;8:25-30. https://doi.org/10.33615/jkohs.2020.8.4.25
  105. Zhou K, Sun M, Xia Y, Xie Y, Shu R. Effects of eicosapentaenoic acid on biological activity and inflammatory factor expression of human gingival fibroblasts. Shanghai J Stomatol. 2021;30:225-31.
  106. Zhou T, Zheng K, Sui B, Boccaccini AR, Sun J. In vitro evaluation of poly (vinyl alcohol)/collagen blended hydrogels for regulating human periodontal ligament fibroblasts and gingival fibroblasts. Int J Biol Macromol. 2020;163:1938-46. https://doi.org/10.1016/j.ijbiomac.2020.09.033
  107. Zufia J, Blasi G, Gomez-Meda R, Blasi A. The four-layer graft technique, a hard and soft tissue graft from the tuberosity in one piece. J Esthet Restor Dent. 2019;31:304-10. https://doi.org/10.1111/jerd.12480