Journal of Dentistry
Volume 37, Issue 10 , Pages 737-747 , October 2009

Assessment of replication of research evidence from animals to humans in studies on peri-implantitis therapy

  • Clovis Mariano Faggion Jr.

      Affiliations

    • Department of Prosthodontics, Dental School Ruprecht-Karls-University of Heidelberg, Heidelberg, Germany
    • Corresponding Author InformationCorresponding author at: Department of Prosthodontics, Dental School Ruprecht-Karls-University of Heidelberg, Im Neuenheimer Feld 400, 69120 Heidelberg, Germany. Tel.: +49 6221 56 6032; fax: +49 6221 56 5371.
    • ,
  • Marc Schmitter

      Affiliations

    • Department of Prosthodontics, Dental School Ruprecht-Karls-University of Heidelberg, Heidelberg, Germany
    • ,
  • Yu-Kang Tu

      Affiliations

    • Department of Periodontology, Leeds Dental Institute and Division of Biostatistics, Centre for Epidemiology and Biostatistics, University of Leeds, Leeds, United Kingdom

Received 17 February 2009 ,Revised 29 May 2009 ,Accepted 16 June 2009.

References 

  1. Rowan AN. Refinement of animal research technique and validity of research data. Fundamental and Applied Toxicology. 1990;15:25–32
  2. Hackam DG, Redelmeier DA. Translation of research evidence from animals to humans. Journal of American Medical Association. 2006;296:1731–1732
  3. Pound P, Ebrahim S, Sandercock P, Bracken MB, Roberts I. Where is the evidence that animal research benefits humans? Reviewing Animal Trials Systematically (RATS) Group. British Medical Journal. 2004;328:514–517
  4. Recommendations for standards regarding preclinical neuroprotective and restorative drug development. Stroke. 1999;30:2752–2758
  5. Eldridge S, Ashby D, Bennett C, Wakelin M, Feder G. Internal and external validity of cluster randomised trials: systematic review of recent trials. British Medical Journal. 2008;336:876–880
  6. Mombelli A, Lang NP. Antimicrobial treatment of peri-implant infections. Clinical Oral Implants Research. 1992;3:162–168
  7. Ericsson I, Persson LG, Berglundh T, Edlund T, Lindhe J. The effect of antimicrobial therapy on periimplantitis lesions. An experimental study in the dog. Clinical Oral Implants Research. 1996;7:320–328
  8. Persson LG, Araújo MG, Berglundh T, Gröndahl K, Lindhe J. Resolution of peri-implantitis following treatment. An experimental study in the dog. Clinical Oral Implants Research. 1999;10:195–203
  9. Wetzel AC, Vlassis J, Caffesse RG, Hämmerle CH, Lang NP. Attempts to obtain re-osseointegration following experimental peri-implantitis in dogs. Clinical Oral Implants Research. 1999;10:111–119
  10. Singh G, O’Neal RB, Brennan WA, Strong SL, Horner JA, Van Dyke TE. Surgical treatment of induced peri-implantitis in the micro pig: clinical and histological analysis. Journal of Periodontology. 1993;64:984–989
  11. Persson LG, Ericsson I, Berglundh T, Lindhe J. Guided bone regeneration in the treatment of periimplantitis. Clinical Oral Implants Research. 1996;7:366–372
  12. Hürzeler MB, Quiñones CR, Schüpback P, Morrison EC, Caffesse RG. Treatment of peri-implantitis using guided bone regeneration and bone grafts, alone or in combination, in beagle dogs. Part 2. Histologic findings. International Journal of Oral and Maxillofacial Implants. 1997;12:168–175
  13. Nociti FH, Machado MA, Stefani CM, Sallum EA. Absorbable versus nonabsorbable membranes and bone grafts in the treatment of ligature-induced peri-implantitis defects in dogs: a histometric investigation. International Journal of Oral and Maxillofacial Implants. 2001;16:646–652
  14. Nociti FH, Machado MA, Stefani CM, Sallum EA, Sallum AW. Absorbable versus nonabsorbable membranes and bone grafts in the treatment of ligature-induced peri-implantitis defects in dogs. Part I. A clinical investigation. Clinical Oral Implants Research. 2001;12:115–120
  15. Schwarz F, Herten M, Sager M, Bieling K, Sculean A, Becker J. Comparison of naturally occurring and ligature-induced peri-implantitis bone defects in humans and dogs. Clinical Oral Implants Research. 2007;18:161–170
  16. Perel P, Roberts I, Sena E, Wheble P, Briscoe C, Sandercock P, et al. Comparison of treatment effects between animal experiments and clinical trials: systematic review. British Medical Journal. 2007;334:197
  17. Kotsovilis S, Karoussis IK, Trianti M, Fourmousis I. Therapy of peri-implantitis: a systematic review. Journal of Clinical Periodontology. 2008;35:621–629
  18. Renvert S, Roos-Jansåker AM, Claffey N. Non-surgical treatment of peri-implant mucositis and peri-implantitis: a literature review. Journal of Clinical Periodontology. 2008;35(8 Suppl):305–315
  19. Claffey N, Clarke E, Polyzois I, Renvert S. Surgical treatment of peri-implantitis. Journal of Clinical Periodontology. 2008;35(8 Suppl):316–332
  20. Moonesinghe R, Khoury MJ, Janssens AC. Most published research findings are false-but a little replication goes a long way. PLoS Medicine. 2007;4:e28
  21. Johnson DH. The many faces of replication. Crop Science. 2006;46:2486–2491
  22. Karring ES, Stavropoulos A, Ellegaard B, Karring T. Treatment of peri-implantitis by the Vector system. Clinical Oral Implants Research. 2005;16:288–293
  23. Hujoel PP, DeRouen TA. Validity issues in split-mouth trials. Journal of Clinical Periodontology. 1992;19(9 Pt 1):625–627
  24. Antczak-Bouckoms AA, Tulloch JF, Berkey CS. Split-mouth and cross-over designs in dental research. Journal of Clinical Periodontology. 1990;17(7 Pt 1):446–453
  25. Tu YK, Blance A, Clerehugh V, Gilthorpe MS. Statistical power for analyses of changes in randomized controlled trials. Journal of Dental Research. 2005;84:283–287
  26. Tu YK, Maddick I, Kellett M, Clerehugh V, Gilthorpe MS. Evaluating the quality of active-control trials in periodontal research. Journal of Clinical Periodontology. 2006;33:151–156
  27. Witte JS, Elston RC, Cardon LR. On the relative sample size required for multiple comparisons. Statistics in Medicine. 2000;19:369–372
  28. Faggion CM Jr, Chambrone L, Gondim V, Schmitter M, Tu YK. Comparison of the effects of treatment of Peri-implant infection in animal and human studies: systematic review and meta-analysis. Clinical Oral Implants Research, forthcoming.
  29. Friedman LM, Furberg CD, DeMets DL. Introduction to clinical trials. Fundamentals of clinical trials. 3rd ed.. Springer; 1999;p. 1–15
  30. Hackam DG. Translating animal research into clinical benefit. British Medical Journal. 2007;334:163–164
  31. Stern JM, Simes RJ. Publication bias: evidence of delayed publication in a cohort study of clinical research projects. British Medical Journal. 1997;315:640–645
  32. Sutton AJ, Duval SJ, Tweedie RL, Abrams KR, Jones DR. Empirical assessment of effect of publication bias on meta-analyses. British Medical Journal. 2000;320:1574–1577
  33. Seglen PO. Why the impact factor of journals should not be used for evaluating research. British Medical Journal. 1997;314:498–502
  34. Saha S, Saint S, Christakis DA. Impact factor: a valid measure of journal quality?. The Journal of the Medical Library Association. 2003;91:42–46
  35. Hanisch O, Tatakis DN, Rohrer MD, Wöhrle PS, Wozney JM, Wikesjö UM. Bone formation and osseointegration stimulated by rhBMP-2 following subantral augmentation procedures in nonhuman primates. The International Journal of Oral and Maxillofacial Implants. 1997;12:785–792
  36. Persson LG, Ericsson I, Berglundh T, Lindhe J. Osseointegration following treatment of peri-implantitis and replacement of implant components. An experimental study in the dog. Journal of Clinical Periodontology. 2001;28:258–263
  37. Deppe H, Horch HH, Henke J, Donath K. Per-implant care of ailing implants with the carbon dioxide laser. The International Journal of Oral and Maxillofacial Implants. 2001;16:659–667
  38. Persson LG, Berglundh T, Lindhe J, Sennerby L. Re-osseointegration after treatment of peri-implantitis at different implant surfaces. An experimental study in the dog. Clinical Oral Implants Research. 2001;12:595–603
  39. Schou S, Holmstrup P, Jørgensen T, Stoltze K, Hjørting-Hansen E, Wenzel A. Autogenous bone graft and ePTFE membrane in the treatment of peri-implantitis. I. Clinical and radiographic observations in cynomolgus monkeys. Clinical Oral Implants Research. 2003;14:391–403
  40. Schou S, Holmstrup P, Skovgaard LT, Stoltze K, Hjørting-Hansen E, Gundersen HJ. Autogenous bone graft and ePTFE membrane in the treatment of peri-implantitis. II. Stereologic and histologic observations in cynomolgus monkeys. Clinical Oral Implants Research. 2003;14:404–411
  41. Schou S, Holmstrup P, Jørgensen T, Skovgaard LT, Stoltze K, Hjørting-Hansen E, et al. Anorganic porous bovine-derived bone mineral (Bio-Oss) and ePTFE membrane in the treatment of peri-implantitis in cynomolgus monkeys. Clinical Oral Implants Research. 2003;14:535–547
  42. Schou S, Holmstrup P, Jørgensen T, Skovgaard LT, Stoltze K, Hjørting-Hansen E, et al. Implant surface preparation in the surgical treatment of experimental peri-implantitis with autogenous bone graft and ePTFE membrane in cynomolgus monkeys. Clinical Oral Implants Research. 2003;14:412–422
  43. Shibli JA, Martins MC, Nociti FH, Garcia VG, Marcantonio E. Treatment of ligature-induced peri-implantitis by lethal photosensitization and guided bone regeneration: a preliminary histologic study in dogs. Journal of Periodontology. 2003;74:338–345
  44. Hayek RR, Araújo NS, Gioso MA, Ferreira J, Baptista-Sobrinho CA, Yamada , et al. Comparative study between the effects of photodynamic therapy and conventional therapy on microbial reduction in ligature-induced peri-implantitis in dogs. Journal of Periodontology. 2005;76:1275–1281
  45. Stübinger S, Henke J, Donath K, Deppe H. Bone regeneration after peri-implant care with the CO2 laser: a fluorescence microscopy study. The International Journal of Oral and Maxillofacial Implants. 2005;20:203–210
  46. Shibli JA, Martins MC, Ribeiro FS, Garcia VG, Nociti FH, Marcantonio E. Lethal photosensitization and guided bone regeneration in treatment of peri-implantitis: an experimental study in dogs. Clinical Oral Implants Research. 2006;17:273–281
  47. Schwarz F, Jepsen S, Herten M, Sager M, Rothamel D, Becker J. Influence of different treatment approaches on non-submerged and submerged healing of ligature induced peri-implantitis lesions: an experimental study in dogs. Journal of Clinical Periodontology. 2006;33:584–595
  48. You TM, Choi BH, Zhu SJ, Jung JH, Lee SH, Huh JY, et al. Treatment of experimental peri-implantitis using autogenous bone grafts and platelet-enriched fibrin glue in dogs. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology. 2007;103:34–37
  49. Takasaki AA, Aoki A, Mizutani K, Kikuchi S, Oda S, Ishikawa I. Er:YAG laser therapy for peri-implant infection: a histological study. Lasers in Medical Science. 2007;22:143–157
  50. Romanos GE, Nentwig GH. Regenerative therapy of deep peri-implant infrabony defects after CO2 laser implant surface decontamination. International Journal of Periodontics and Restorative Dentistry. 2008;28:245–255
  51. Renvert S, Lessem J, Dahlén G, Renvert H, Lindahl C. Mechanical and repeated antimicrobial therapy using a local drug delivery system in the treatment of peri-implantitis: a randomized clinical trial. Journal of Periodontology. 2008;79:836–844
  52. Schwarz F, Sculean A, Bieling K, Ferrari D, Rothamel D, Becker J. Two-year clinical results following treatment of peri-implantitis lesions using a nanocrystalline hydroxyapatite or a natural bone mineral in combination with a collagen membrane. Journal of Clinical Periodontology. 2008;35:80–87
  53. Roos-Jansåker AM, Renvert H, Lindahl C, Renvert S. Submerged healing following surgical treatment of peri-implantitis: a case series. Journal of Clinical Periodontology. 2007;34:723–727
  54. Roos-Jansåker AM, Renvert H, Lindahl C, Renvert S. Surgical treatment of peri-implantitis using a bone substitute with or without a resorbable membrane: a prospective cohort study. Journal of Clinical Periodontology. 2007;34:625–632
  55. Salvi GE, Persson GR, Heitz-Mayfield LJ, Frei M, Lang NP. Adjunctive local antibiotic therapy in the treatment of peri-implantitis. II. Clinical and radiographic outcomes. Clinical Oral Implants Research. 2007;18:281–285
  56. Romeo E, Lops D, Chiapasco M, Ghisolfi M, Vogel G. Therapy of peri-implantitis with resective surgery. A 3-year clinical trial on rough screw-shaped oral implants. Part II. Radiographic outcome. Clinical Oral Implants Research. 2007;18:179–187
  57. Deppe H, Horch HH, Neff A. Conventional versus CO2 laser-assisted treatment of peri-implant defects with the concomitant use of pure-phase beta-tricalcium phosphate: a 5-year clinical report. The International Journal of Oral and Maxillofacial Implants. 2007;22:79–86
  58. Persson GR, Salvi GE, Heitz-Mayfield LJ, Lang NP. Antimicrobial therapy using a local drug delivery system (Arestin) in the treatment of peri-implantitis. I. Microbiological outcomes. Clinical Oral Implants Research. 2006;17:386–393
  59. Schwarz F, Bieling K, Latz T, Nuesry E, Becker J. Healing of intrabony peri-implantitis defects following application of a nanocrystalline hydroxyapatite (Ostim) or a bovine-derived xenograft (Bio-Oss) in combination with a collagen membrane (Bio-Gide). A case series. Journal of Clinical Periodontology. 2006;33:491–499
  60. Renvert S, Lessem J, Dahlén G, Lindahl C, Svensson M. Topical minocycline microspheres versus topical chlorhexidine gel as an adjunct to mechanical debridement of incipient peri-implant infections: a randomized clinical trial. Journal of Clinical Periodontology. 2006;33:362–369
  61. Schwarz F, Bieling K, Nuesry E, Sculean A, Becker J. Clinical and histological healing pattern of peri-implantitis lesions following non-surgical treatment with an Er:YAG laser. Lasers in Surgery and Medicine. 2006;38:663–671
  62. Zhou L, Lin Y, Qiu LX, Chen B, Hu XL, Wang X. Clinical study of periocline on peri-implantitis treatment. Zhonghua Kou Qiang Yi Xue Za Zhi. 2006;41:299–303
  63. De Araújo Nobre M, Capelas C, Alves A, Almeida T, Carvalho R, Antunes E, et al. Non-surgical treatment of peri-implant pathology. International Journal of Dental Hygiene. 2006;4:84–90
  64. Schwarz F, Sculean A, Rothamel D, Schwenzer K, Georg T, Becker J. Clinical evaluation of an Er:YAG laser for nonsurgical treatment of peri-implantitis: a pilot study. Clinical Oral Implants Research. 2005;16:44–52
  65. Romeo E, Ghisolfi M, Murgolo N, Chiapasco M, Lops D, Vogel G. Therapy of peri-implantitis with resective surgery. A 3-year clinical trial on rough screw-shaped oral implants. Part I. Clinical outcome. Clinical Oral Implants Research. 2005;16:9–18
  66. Büchter A, Meyer U, Kruse-Lösler B, Joos U, Kleinheinz J. Sustained release of doxycycline for the treatment of peri-implantitis: randomised controlled trial. British Journal of Oral and Maxillofacial Surgery. 2004;42:439–444
  67. Leonhardt A, Dahlén G, Renvert S. Five-year clinical, microbiological, and radiological outcome following treatment of peri-implantitis in man. Journal of Periodontology. 2003;74:1415–1422
  68. Tang Z, Cao C, Sha Y, Lin Y, Wang X. Effects of non-surgical treatment modalities on peri-implantitis. Zhonghua Kou Qiang Yi Xue Za Zhi. 2002;37:173–175
  69. Dörtbudak O, Haas R, Bernhart T, Mailath-Pokorny G. Lethal photosensitization for decontamination of implant surfaces in the treatment of peri-implantitis. Clinical Oral Implants Research. 2001;12:104–108
  70. Mombelli A, Feloutzis A, Brägger U, Lang NP. Treatment of peri-implantitis by local delivery of tetracycline. Clinical, microbiological and radiological results. Clinical Oral Implants Research. 2001;12:287–294
  71. Khoury F, Buchmann R. Surgical therapy of peri-implant disease: a 3-year follow-up study of cases treated with 3 different techniques of bone regeneration. Journal of Periodontology. 2001;72:1498–1508
  72. Stellini E, Migliorato A, Mazzoleni S, Mottola A, Lombardi L, Favero GA. Topical treatment of peri-implantitis with metronidazole dental gel 25%. Clinical analysis and microbiological control. Minerva Stomatologica. 2000;49:59–67
  73. Haas R, Baron M, Dörtbudak O, Watzek G. Lethal photosensitization, autogenous bone, and e-PTFE membrane for the treatment of peri-implantitis: preliminary results. The International Journal of Oral and Maxillofacial Implants. 2000;15:374–382
  74. Bach G, Neckel C, Mall C, Krekeler G. Conventional versus laser-assisted therapy of periimplantitis: a five-year comparative study. Implant Dentistry. 2000;9:247–251
  75. Behneke A, Behneke N, d’Hoedt B. Treatment of peri-implantitis defects with autogenous bone grafts: six-month to 3-year results of a prospective study in 17 patients. The International Journal of Oral and Maxillofacial Implants. 2000;15:125–138
  76. Behneke A, Behneke N, d’Hoedt B. Regenerative Behandlung knöcherner Defekte mit autologen Knochentransplantaten im Rahmen der Periimplantitistherapie. Erste klinische Ergebnisse. Zeitschrift für Zahnärztliche Implantologie. 1997;13:5–14
  77. Buchmann R, Khoury F, Müller RU, Lange D. Die Therapie der progressiven marginalen Parodontitis und Periimplantitis. Deutsche Zahnärztliche Zeitschrift. 1997;52:421–426
  78. Buchmann R, Khoury F, Hesse Th , Müller RF, Lange DE. Antimikrobielle Therapie der periimplantären Erkrankung. Zeitschrift für Zahnärztliche Implantologie. 1996;12:152–157
  79. Augthun M, Richter EJ, Hauptmann S, Yildirim M. Untersuchungen zur Behandlung von tiefen periimplantären Knochentaschen mit e-PTFE-Membranen. Zeitschrift für Zahnärztliche Implantologie. 1992;8:246–250

PII: S0300-5712(09)00154-7

doi: 10.1016/j.jdent.2009.06.010

Journal of Dentistry
Volume 37, Issue 10 , Pages 737-747 , October 2009

Article Tools

* Image Usage & Resolution