Professional Documents
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Bone Regeneration
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uided bone regeneration (GBR) Guided bone regeneration is a supply and undifferentiated mesen-
ciples delineated by Melcher5 described healing. This article describes the 4 design and clinical cases using this
the need for cell exclusion to enable the major biologic principles (i.e., principle are presented. (Implant
healing wound to be populated by cells PASS) necessary for predictable Dent 2006;15:8 –17)
thought to be more favorable for regen- bone regeneration: primary wound Key Words: guided bone regenera-
eration. In GBR, the cells that are re- closure to ensure undisturbed and tion, bone grafts, horizontal bone
quired to repopulate the wound are uninterrupted wound healing, angio- augmentation, implants
primarily osteoblasts. Osteoblasts are genesis to provide necessary blood
responsible for laying down new alveo-
lar bone and for future bone remodeling.
By selectively excluding epithelium and creation/maintenance, and stability of and overall tissue remodeling. In ad-
connective tissue with the use of bone both the initial blood clot and implant dition, postoperative discomfort may
grafting and barrier materials, bone is fixture (PASS). be reduced as a result of less exposure
“guided” into the desired position. of underlying connective tissue. Most
Dahlin et al6 were the first to show that investigators have advocated the ne-
bony defects created in rat mandibles PRIMARY CLOSURE
cessity of primary closure following
could be successfully closed using The 2 basic methods of wound implant placement to ensure predict-
guided tissue regeneration procedures. healing are termed healing by primary able GBR outcomes,7,12-15 while others
The success and predictability of intention and secondary intention, re-
have disputed its importance. 16,17
GBR have since vastly broadened the spectively. In healing by primary in-
Nonetheless, there is a consensus that
applicability of implant therapy. Im- tension, the edges of a wound are
primary wound coverage should be ac-
plants can now be placed in areas of placed together in virtually the same
position they held before the injury. complished whenever possible.
previously deficient bone volume,
Secondary intention describes healing Examining the effect of mem-
with success rates reported higher than
95%.7-11 However, to ensure predict- that occurs when wound edges cannot brane exposure on bone volume gains
ability of this technique, clinical pro- be closely approximated, resulting in a highlights the importance of primary
cedures should be based on sound wound that is slower to heal, requires wound closure. Machtei18 performed a
biologic principles. This article out- more collagen remodeling, and is metaanalysis to evaluate the effects of
lines the 4 major principles underlying more likely to result in scar formation. membrane exposure on treatment out-
successful GBR (Fig. 1): primary Realistically, true healing by primary comes in guided tissue regeneration
wound closure, angiogenesis, space intention is often difficult to achieve. and GBR. When looking at guided
However, primary wound closure is a tissue regeneration cases alone, ex-
fundamental surgical principle for posed membranes showed only 0.47
*Professor and Director of Graduate Periodontics, Department GBR because it creates an environ- mm less attachment gain compared to
of Periodontics and Oral Medicine, School of Dentistry,
University of Michigan, Ann Arbor, MI. ment that is undisturbed/unaltered by membranes that remained submerged.
†Resident, Department of Periodontics and Oral Medicine,
School of Dentistry, University of Michigan, Ann Arbor, MI. outside bacterial or mechanical insult. In comparison, membrane exposure
Passive closure of wound edges seemed to have a significant deleteri-
ISSN 1056-6163/06/01501-008
Implant Dentistry enables the wound to heal with less ous effect on bone formation. In cases
Volume 15 • Number 1
Copyright © 2006 by Lippincott Williams & Wilkins reepithelialization, collagen formation in which the membrane remained sub-
DOI: 10.1097/01.id.0000204762.39826.0f and remodeling, wound contraction, merged, a mean 3.01 mm of new bone
the wound space, initially filled with skulls of 8 rabbits. In each animal, the poorer regenerative outcomes. In ad-
blood clot, then with new bone.55 test side had the outer layer of cortical dition, a pattern of membrane collapse
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Buser et al47 found that introducing bone removed, while the control side in most of the exposed sites (8 of 9)
cortical perforations (i.e., intra-bone was left with an intact cortex. Block was associated with less regeneration.
marrow penetration) allowed migra- section and histology performed at 3 The investigators concluded that space
tion of cells with angiogenic and os- months in all animals revealed no dif- maintenance and membrane coverage
teogenic potential. Nonetheless, some ference in total amount of augmented were the 2 most important factors af-
studies have showed that bone regen- tissue (75.5% compared to 71.2%) or fecting GBR using bioabsorbable col-
eration can occur even from a nonin- the augmented mineralized bone tissue lagen membranes.
jured cortical layer.56,57 Future studies (17.8% compared to 16.0%). Together, Reinforced membranes allow
in this area are certainly encouraged. the aforementioned literature shows the space maintenance by preventing
The concept of a regional accel- need for adequate blood supply and an- membrane collapse that may occur
eratory phenomenon was introduced giogenesis for bone regeneration to oc- from pressure of overlying tissues. A
several decades ago.58-61 Melcher and cur. Although, to date, no consensus has titanium mesh incorporated into the
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Dryer62 also emphasized the impor- been established on the beneficial effect membrane also improves the strength
tance of the blood clot in healing of of cortical perforation. of the membrane and allows adaptabil-
bony defects. Several potential advan- ity to the shape of the osseous defect.
tages of decortication exist. Providing Jovanovic et al81 used a canine model
communication with marrow spaces SPACE CREATION/MAINTENANCE and compared 3 treatment groups in
may enhance revascularization. Growth Providing adequate space for bone terms of bone regeneration. Group 1
factors, such as platelet derived growth regeneration is a fundamental princi- had a titanium-reinforced membrane,
factor, and bone morphogenetic proteins ple of GBR. Space is needed to ensure group 2 had a standard expanded poly-
can be released to enhance periodontal the proliferation of bone forming cells tetrafluoroethylene membrane, and
regeneration63 and peri-implant bone while excluding unwanted epithelial group 3 was a control and had no
formation.64 Osteogenic cells important and connective tissue cells. For exam- membrane. A marked gain of alveolar
to bone healing can be derived from 3 ple, in areas of natural space mainte- bone volume, resulting in complete
main sources: the periosteum, en- nance, such as after the placement of supracrestal regeneration, was noted
dosteum, and undifferentiated pluripo- immediate implants, there is evidence in both expanded polytetrafluoroethyl-
tential mesenchymal cells. The marrow to suggest that the addition of bone ene groups (1.82 and 1.9 mm) com-
provides a rich source of these undiffer- grafting materials and membranes has pared to only 0.53 mm achieved in the
entiated cells that can be transformed no beneficial effect over no mem- control group. Several other studies
into osteoblasts and osteoclasts. In ad- brane/no graft control sites.50,72,73 A have compared the use of reinforced
dition, the perforations through the consensus has yet to be formed regard- nonresorbable and absorbable mem-
cortical bone provide a mechanical in- ing the need for the use of barrier branes using various bone grafting
terlock with the newly regenerated materials and/or bone grafts around materials.22,43,82-84 From the available
bone. It has even been suggested that immediately placed implants.74-78 It literature, it can be concluded that
the cortical plate may act as a temporary may be that assuming the critical when a significant volume of bone is
hindrance for access of desirable cells jumping distance has not been ex- required for implant placement, the
and tissue components from the marrow ceeded, the space formed between the use of reinforced membranes or addi-
because resorption of the cortical bone extraction socket and implant fixture tional bone grafts is more beneficial.
has to take place before access to bone provides an ideal environment for When higher amounts of bone re-
forming components is achieved.65 clot stabilization and subsequent generation are required, space making
Beneficial effects of regional ac- osteogenesis.79,80 with a barrier membrane is critical. As
celeratory phenomenon have been re- Various animal studies have mentioned previously, absorbable mem-
ported in several animal studies.52,66-68 proved that by excluding the epithe- branes have various beneficial proper-
Larger perforations have been associ- lium and connective tissue, a secluded ties. However, a major challenge of using
ated with a shorter time to obtain bone space is thereby created, allowing an absorbable membrane alone is mem-
fill but without any differences in the slowly migrating osteoblast cells to brane collapse that may be caused by
total amount of new bone formed.68 populate the wound, resulting in en- the overlying soft tissue pressure. Var-
Misch69 has advocated the use of both hanced bone formation.4,6,57 In a clin- ious techniques have been developed
buccal and lingual decortication to en- ical and histomorphometric study in a to overcome this challenge. Using
hance bony healing 2-10 times higher canine model, Oh et al31 used a beagle coronally advanced flaps, placing
than normal. However, conflicting re- dog model to compare the effects of 2 bone grafting materials under the
predictable surgical protocol that is a rich source of cytokines (e.g., clinical and radiographic evalua-
would enable the maintenance of a interleukin-1, interleukin-8, tumor ne- tion is needed to assess the need
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secluded space that could be occu- crosis factor), growth factors (e.g., plate- for bone augmentation during im-
pied by cells with an osteogenic let derived growth factor, insulin-like plant placement.
potential.2,46,51,84,87 growth factor, fibroblast growth factor), • Initial incision (Fig. 2C): An at-
Whether the use of bone graft ma- and signaling molecules that recruit tempt is always made to locate the
terial has any additional use other than clearing cells to the wound site. Platelet initial incision away from the de-
space maintenance is debatable. 88 derived growth factor in particular is a fect site so that closure is not
Mellonig et al83 reported results from potent mitogen and chemoattractant for directly over the defect site. Ver-
human cases in a delayed implant with neutrophils and monocytes.95 The blood tical releasing incisions, either fol-
simultaneous GBR technique. There clot serves as the precursor of initial lowing the mucogingival junction
were 3 treatment groups compared highly vascular granulation tissue. The or extending beyond mucogingival
(i.e., bioabsorbable membrane with granulation tissue is then the site of ini- junction, are used whenever indi-
decalcified freeze-dried bone allograft tial intramembranous bone formation cated. Mucogingival junction inci-
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Fig. 2. Case No. 2. Augmentation of horizontal ridge defect in conjunction with implant placement. A, Preoperative view showing inadequate
ridge width and height. B, Presurgical radiograph illustrated potential apical lesion. C, Initial incisions depict 2 divergent vertical releasing
incisions. D, Surgical view showing ridge defects with granulomatous tissues. E, Area was débrided to the bare bone. F, Initial implant drill
following the surgical guide to indicate ideal buccolingual location. G, Implant placement with horizontal ridge deficiency. H, Intra-bone marrow
penetration using half-round bur. I, Sandwich bone augmentation. First layer of bone graft aimed at promoting better bone to implant contact
(human mineralized cancellous bone allograft, Puros; Zimmer Dental Inc.). J, Sandwich bone augmentation. Second layer of bone graft aimed
at creating/maintaining space (human mineralized bone cortical allograft, Puros) was used for barrier support and space creation, both
horizontally and vertically. K, Sandwich bone augmentation. Outer layer used for barrier support and space creation, both horizontally and
vertically (collagen membrane, BioMend Extend). L, Suture with 4-0 and 5-0 Vicryl suture (primary coverage with passive flap tension). M,
Four-week healing indicated uneventful healing. N, Reentry at 6 months showing new bone formation.
Implant drills were performed ac- defects associated with existing the margins of the defect in all
cording to manufacturer’s recom- implants, epithelium should be re- directions. Usually, the collagen
mended protocol. In addition, moved from the inner surface of membrane is hydrated in sterile
drilling was based upon the prefab- the flap using a sharp curette or saline or sterile water for 5-10
ricated surgical guides that consider diamond bur. The implant surface minutes before use, to improve
proper esthetic profile (Fig. 2F). should then be detoxified with ap- handling (malleability), however,
Fig. 2G shows implant placement propriate agents (e.g., 50 mg/mL this is not mandatory.
in a proper position with an obvious tetracycline for 3 minutes). • Fitting the flap: The flap is
horizontal ridge deficiency. • Fitting the membrane: Collagen checked and trimmed if necessary
• Removal of epithelium: Where membrane is trimmed and fitted to ensure that primary tension-
appropriate, as in treatment of so that it extends 2-3 mm beyond free closure is possible.
mineralized bone allograft) is GBR. In addition, the technique in- term results and survival rate of implants
placed at the defect site to support volved in this principle was clearly treated with guided bone regeneration: A
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plants influence their bone integration after Sci U S A. 1978;75:871-875. 52. Schmid J, Wallkamm B, Hammerle
simultaneous placement of implant and 38. Wang HL, O’Neal RB, Thomas CL, CH, et al. The significance of angiogenesis
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GBR membrane. Clin Oral Implants Res. et al. Evaluation of an absorbable collagen in guided bone regeneration. A case report
2003;14:669-679. membrane in treating class II furcation de- of a rabbit experiment. Clin Oral Implants
25. Mombelli A, Lang NP, Nyman S. fects. J Periodontol. 1994;65:1029-1036. Res. 1997;8:244-248.
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26. Simion M, Trisi P, Maglione M, et al. 40. Chen CC, Wang HL, Smith F, et al. using guided bone regeneration. A pilot
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27. Nowzari H, London R, Slots J. The fects utilizing a bioresorbable collagen 55. Hammerle CH, Schmid J, Olah AJ,
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guided periodontal tissue regeneration and Dent 1995;7:59-66. experimental guided bone formation in hu-
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AUTOR(EN): Hom-Lay Wang, DDS, MSD*, “PASS”-Prinzipien für eine vorhersagbar erfolgreiche Knochengewebsregeneration
Lakshmi Boyapati, BDS**. *Professor und
Leiter des Graduiertenkollegs für Orthodon- ABSTRACT: Die geleitete Knochengewebswiederherstellung stellt eine eingeführte
tie, Abteilung für Orthodontie und Oralmedi- Methode zur Anreicherung unzureichender Alveolarleisten dar. Eine vorhersagbare gute
zin, zahnmedizinische Fakultät, Universität Regeneration bedarf sowohl der groen technischen Fähigkeiten wie auch eines pro-
von Michigan, Ann Arbot, MI, USA. **Assis- funden Kenntnisstandes bezüglich der einer erfolgreichen Wundheilung zu Grunde lieg-
tenzarzt, Abteilung für Orthodontie und enden Prinzipien. Die vorliegende Arbeit beschreibt die vier wesentlichen biologischen
Oralmedizin, zahnmedizinische Fakultät, Uni- Prinzipien (d.h. PASS), die für eine vorhersagbar gute Knochenregeneration erforderlich
versität von Michigan, Ann Arbot, MI, USA. sind. Hierzu gehören: der primäre Wundverschluss zur Gewährleistung einer ungestörten
Schriftverkehr: Dr. Hom-Lay Wang, Professor und ununterbrochenen Wundheilung; Gefäbildung zur Bereitstellung eines aus-
und Leiter des Graduiertenkollegs für Orth- reichenden Blutzuflusses sowie unveränderte Mesenchymalzellen; Raumerhaltung oder
odontie (Professor and Director of Graduate -schaffung, um den entsprechenden Platz für Neuknochenbildung bereit zu stellen; und
Periodontics), Abteilung für Orthodontie und Wund- sowie Implantatstabilität zur Vermeidung von Blutgerinnselbildung und unerwün-
Oralmedizin (Department of Periodontics and schten Begleiterscheinungen bei der Heilung. Auerdem werden in der Abhandlung eine
Oral Medicine), zahnmedizinische Fakultät neuartige Lappenkonstruktion sowie klinische Fälle, die dieses Prinzip praktisch zur
der Universität von Michigan (University of Anwendung gebracht haben, vorgestellt.
Michigan School of Dentistry), 1011 North
University Avenue, Ann Arbor, Michigan SCHLÜSSELWÖRTER: Geleitete Knochengewebswiederherstellung, Knochentrans-
48109-1078, USA. Telefon: (734) 763-3383, plantat, horizontale Knochengewebsanreicherung, Implantate
Fax: (734) 936-0374. eMail: homlay@umich.
edu
AUTOR(ES): Hom-Lay Wang, DDS, MSD*, Los principios “PASS” para la regeneración pronosticable del hueso
Lakshmi Boyapati, BDS**. *Profesor y Direc-
tor de Periodóntica Graduada, Departamento ABSTRACTO: La regeneración guiada del hueso es una técnica bien establecida para
de Periodóntica y Medicina Oral, Facultad de aumentar crestas alveolares deficientes. La regeneración pronosticable requiere un alto
Odontologı́a, Universidad de Michigan, Ann Ar- nivel de aptitud técnica y un completo entendimiento de los principios de curación de una
bor, MI, EE.UU. **Residente, Departamento de herida. Esta manuscrito describe los cuatro principios biológicos principales (PASS)
Periodóntica y Medicina Oral, Facultad de Od- necesarios para la regeneración pronosticable del hueso; cierre de la herida principal para
ontologı́a, Universidad de Michigan, Ann Arbor, asegurar una curación de la herida sin problemas y sin interrupciones; angiogénesis para
MI, EE.UU. Correspondencia a: Dr. Hom-Lay proporcionar el suministro necesario de sangre y células mesenquimales indiferenciadas;
Wang, Professor and Director of Graduate Pe- mantenimiento/creación del espacio para facilitar un espacio adecuado para el crecimiento
riodontics, Departament of Periodontics and del hueso; y estabilidad para la herida y el implante para inducir la formación de un
Oral Medicine, University of Michigan School of coágulo sanguı́neo y una curación sin dificultades. Además, se presentan un diseño nuevo de
Dentistry, 1011 North University Avenue, Ann la aleta y casos clı́nicos que utilizan este principio.
Arbor, MI 48109-1078, U.S.A. Teléfono: (734)
763-3383 Fax: (734) 936-0374. Dirección PALABRAS CLAVES: GBR; regeneración guiada del hueso; injertos de hueso; aumento
electrónica: horizontal del hueso, implantes.
Medicina Oral, Faculdade de Odontologia, suprimento necessário de sangue e células mesenquimais indiferenciadas; Manutenção/
Universidade de Michigan, Ann Arbor, MI, criação de espaço para facilitar espaço adequado para crescimento para dentro do osso; e
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EUA.Correspondência para: Dr. Hom-Lay estabilidade de ferida e implante para induzir a formação de coágulo sangüı́neo e eventos
Wang, Professor and Director of Graduate de cura tranqüilos. Além disso, um original design de borda e casos clı́nicos que utilizam
Periodontics, Department of Periodontics and este princı́pio são apresentados.
Oral Medicine, University of Michigan School
of Dentistry, 1011 North University Avenue, PALAVRAS-CHAVE: GBR; Regeneração óssea guiada; enxertos ósseos; aumento hor-
Ann Arbor, Michigan 48109-1078, USA. Tele- izontal do osso; implantes.
fone: (734) 763-3383, Fax: (734) 936-0374.
E-mail: homlay@umich.edu
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