| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
RESEARCH REPORT |
1 Departments of Periodontics and
2 Pathology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, San Antonio, TX 78229, USA;
3 Department of Preventive Dentistry, Periodontology, and Cariology, University of Zürich Dental School, Zürich, Switzerland;
4 Department of Oral Surgery and Stomatology, University of Bern, School of Dental Medicine, Bern, Switzerland; and
5 Department of Orthodontics, Universidad Autonoma de Coahuila Facultad de Odontologia, Torreon, Mexico;
*corresponding author, perio{at}dental.uthscsa.edu
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONREFERENCES |
|---|
KEY WORDS: one-piece implant • two-piece implant • peri-implant inflammation • microgap • neutrophil
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONREFERENCES |
|---|
To date, the central focus of long-term human studies (Cochran, 1996) using either conventionally submerged or non-submerged implants has been osseointegration (Brånemark et al., 1977), also known as functional ankylosis (Schroeder et al., 1981). In spite of comparable clinical success rates for hard-tissue integration of various implant designs (Adell et al., 1981; Buser et al., 1997, 1999; Lekholm et al., 1999), the consequences of a microgap at the alveolar bone level are not well-elucidated with respect to peri-implant inflammation, nor is it clear whether the elimination of a second surgical procedure in conventional two-piece, submerged implants renders a different peri-implant soft-tissue response.
Previous studies utilizing two-piece implants have documented that peri-implant soft tissues develop a zone of inflammatory cells in connective tissue below gingival epithelium in the presence of plaque (Berglundh et al., 1992; Ericsson et al., 1992); however, the nature and extent of inflammatory cells along the entire implant surface under normal hygiene conditions remain to be established. The purpose of this study was to determine how changes in abutment connection timing (submerged vs. non-submerged two-piece implants) or the presence of a microgap (two-piece, non-submerged implants vs. one-piece, non-submerged implants) influences the composition of inflammatory cells immediately adjacent to the implant.
MATERIALS & METHODS
Implant Design and Placement
Histologic specimens of three implant designs (two-piece, submerged; two-piece, non-submerged; and one-piece, non-submerged) were procured from a larger study involving 6 different implant types as previously described (Hermann et al., 1997, 2000). In brief, following the approval of the study protocol by the Institutional Animal Care and Use Committee (University of Texas Health Science Center at San Antonio), various experimental implant designs (all sandblasted/acid-etched surfaces) were placed in the edentulous mandibular regions of 5 foxhound dogs. Each implant type was included in duplicate for each animal with random placement in both the left and right mandibles. Mechanical and chemical plaque control were performed 3 times a week by a soft toothbrush and a soft sponge in combination with a 0.2% chlorhexidine gel (PlakOut Gel, Hawe-Neos AG, Bioggio/TI, Switzerland). Abutment connection was performed at the time of initial surgery for two-piece, non-submerged implants and 3 mos after initial implant placement for two-piece, submerged implants. At 4, 8, and 10 wks following second-stage surgery of submerged implants, abutments were loosened and then immediately tightened in all two-piece implants to mimic clinical restorative procedures. Six months after initial implant placement, tissues were obtained and histologic specimens were prepared as previously described (Schenk et al., 1984).
Histomorphometric Analyses
Histomorphometry was performed by means of a light microscope (Vanox-T®, Olympus, Tokyo, Japan) connected to a high-resolution video camera (CCD-Iris® Color Video Camera, Sony Corp., Fujisawa, Japan) that was linked to a monitor (Multisync® XV17+, NEC, Itasca, IL) and personal computer. Histomorphometric software (Image-Pro Plus®, Media Cybernetics, Silver Spring, MD, USA) facilitated digital image capture as well as manual counting of individual inflammatory cells and measurement of tissue area.
Sequential peri-implant test fields (0.25 mm x 0.33 mm) along the entire implant surface were evaluated (Fig. 1
). Each field (0.0825 mm2) was digitally captured at high magnification (x 340). The original bone crest was designated as the histological reference point for all implants. For two-piece implants, this reference point corresponded to the implant-abutment interface. For one-piece implants, the same reference point corresponded to 1 mm above the rough/smooth border of the sandblasted/acid-etched (SLA) and machined surfaces. In each 0.0825-mm2 field, neutrophils and mononuclear cells (lymphocytes, plasma cells, monocytes, and macrophages) were counted. Inflammatory cells within the vessels were excluded. In addition, areas of alveolar bone and gingival or junctional epithelium were eliminated. Thus, only extravascular (interstitial) tissues were assessed. This area of interstitium was then used to calculate cell density, i.e., cells/mm2, for each field along the implant surface. Linear soft-tissue distances were calculated by summation of the apico-coronal dimension from all captured test fields (0.25 mm). Through this histomorphometric approach, the distance below the microgap for two-piece implants (submerged and non-submerged) confirmed results of a previously published study (Hermann et al., 2000) that evaluated bone loss with the use of these same histological specimens.
|
0.05 were considered significant.
RESULTS
In peri-implant soft tissues of both two-piece implants, a considerable cellular infiltrate was concentrated at a level immediately coronal to the implant-abutment interface (microgap) and appeared to decrease gradually and progressively in soft tissues toward either bone or gingival epithelium. In contrast, sparse cells were present in the soft tissues adjacent to one-piece implants (data not shown).
Two-piece Implants
The distribution of peri-implant inflammatory cells was analogous for submerged and non-submerged two-piece implants (Fig. 2A). In each implant type, the peak density of inflammatory cells occurred 0.5 mm coronal to the microgap (9642 ± 946 cells/mm2 and 9103 ± 664 cells/mm2 for submerged and non-submerged, respectively); there were no significant differences in the density of total inflammatory cells at equivalent peri-implant locations. Among individual animals, the maximum density and location of inflammatory cells were comparable (Table 1). The cumulative sum of peri-implant inflammatory cells (1) coronal to the microgap, (2) apical to the microgap, or (3) for the entire peri-implant soft-tissue distance from bone to gingival epithelium revealed no significant differences between these two-piece implant types (Table 2).
|
|
|
). There were no significant differences in the cumulative sum of neutrophils for two-piece implants (Table 2). Thus, the major cell type constituting the inflammatory cell infiltrate for both submerged and non-submerged two-piece implants was the neutrophil (Table 2). Mononuclear cells were evenly distributed along implant surfaces for both two-piece implants (Fig. 2C). Further, the cumulative numbers and density of mononuclear cells were not significantly different between either two-piece design (Tables 1, 2). Finally, there were no significant differences between submerged and non-submerged two-piece designs regarding (1) the entire soft-tissue distance between alveolar bone and gingival epithelium; (2) the soft-tissue distance above the microgap; and (3) bone loss as measured from the microgap to alveolar bone level (Table 2).
One-piece vs. Two-piece Implants
There was no discrete peak of inflammatory cells adjacent to one-piece implants (Fig. 2A). Moreover, there were significant differences in the accumulation of total inflammatory cells between two-piece and one-piece implant types (Fig. 2A). Indeed, inflammatory cell infiltration for all corresponding locations was significantly greater for two-piece implants as compared with one-piece implants. Correspondingly, the cumulative numbers of peri-implant inflammatory cells were significantly greater for two-piece, non-submerged implants as compared with one-piece, non-submerged implants (Table 2).
In parallel with the above, there was no selective neutrophil accumulation adjacent to one-piece implants (Fig. 2B; Table 2), and mononuclear cells were significantly reduced (Fig. 2C). Thus, the cumulative sum of mononuclear cells in two-piece implants was significantly increased as compared with one-piece implants (Table 2). Although the accumulation of mononuclear cells apical to the original bone crest was greater in two-piece implants, the cumulative sum coronal to this reference point was not significantly different between implants (Table 2).
The connective tissue distance adjacent to one-piece implants was significantly less than for two-piece implants (Table 2). Bone loss, i.e., connective tissue distance below the original bone crest, was significantly greater for two-piece implants as compared with that of one-piece implants. Conversely, the soft-tissue distance above the original bone crest was significantly greater for one-piece implants as compared with two-piece implants, in spite of a smaller overall connective tissue distance for the one-piece, non-submerged design.
DISCUSSION
This study has provided histomorphometric evidence that a unique pattern of inflammatory cell infiltrate develops adjacent to implants and varies on the basis of implant design. In brief, an intense inflammatory cell infiltrate (predominantly neutrophils) and significant bone loss were associated with the presence of a microgap at the bone crest, regardless of surgical technique, i.e., submerged or non-submerged. Conversely, minimal inflammatory cell infiltrate (predominantly mononuclear cells) and minimal bone loss were observed adjacent to one-piece implants. Thus, the presence of a microgap at the level of alveolar bone was associated with persistent inflammation and increased alveolar bone loss.
The association of neutrophils with the implant-abutment interface of two-piece implants suggests that this physical attribute of implant design contributes to the recruitment of these cells when located at alveolar bone. Significant and comparable inflammatory cell infiltrates were associated with the presence of a microgap at the bone crest regardless of the timing of abutment connection (immediately or delayed) but were not observed in the absence of a microgap. The differential pattern of peri-implant neutrophil accumulation suggests that a chemotactic stimulus originating at or near the microgap of two-piece implants initiates and sustains recruitment of inflammatory cells. Since the presence of microbes at the internal aspects of implant components (Quirynen and van Steenberghe, 1993; Persson et al., 1996; O’Mahony et al., 2000) as well as the phenomenon of microbial and/or fluid leakage through the implant-abutment interface (Quirynen et al., 1994; Jansen et al., 1997; Gross et al., 1999) have been previously described, it is conceivable that microbes from the oral cavity could gain access and provide such a stimulus. Consequently, activation of the host defense system (e.g., antibody, complement, and cytokines) would initiate a differential host response and result in a gradient of inflammatory cells around the microgap. This scenario, together with inherently restricted access of host defense mechanisms to the microgap, could perpetuate an acute inflammatory process and be further exacerbated by limited access for effective oral hygiene. Thus, this aspect of implant design may create a reservoir of bacteria and possibly facilitate the development of peri-implant inflammation. It is unknown whether different implant-abutment connections, such as an internal cone, would yield a different distribution or intensity of inflammatory cell recruitment as compared with the flat, butt-joint interface used in the present study. However, since microleakage is unavoidable among current implant systems, regardless of the connection type or interface size (Jansen et al., 1997; Gross et al., 1999), it would appear that one could expect a similar inflammatory response for any interface located at alveolar bone.
In addition to an intense inflammatory process, significantly greater bone loss was observed around two-piece implants as compared with one-piece implants. A relationship between inflammatory events and bone loss seems likely (Assuma et al., 1998; Graves et al., 1998). In this regard, we noted a positive trend between the accumulation of inflammatory cells apical to the microgap and the degree of alveolar bone loss, although significance could not be established given the relatively small number of animals in this study.
These results from the present study may have important clinical implications in aspects of optimal implant placement and design. While longitudinal descriptive studies (Adell et al., 1981; Apse et al., 1991; Nevins and Langer, 1993) have indicated that implants may remain functional for extended intervals, conventional success criteria for acceptable bone loss have included 1.5 mm during the first year of function (after prosthesis connection) and < 0.2 mm every year thereafter (Adell et al., 1981; Albrektsson et al., 1986). This criterion had evolved from consistent observations of such bone loss around submerged implants with an implant-abutment interface placed at the level of bone (Brånemark et al., 1969). This phenomenon around two-piece implants was also demonstrated in later studies (Ericsson et al., 1996; Hermann et al., 1997) and confirmed by the present study. Although remaining functional, the possible sequelae of bone loss may not meet subjective and exacting esthetic goals. For example, it has been shown that peri-implant bone loss may lead to proportional soft-tissue recession (Hermann et al., 2001), as indicated in a study of natural dentition in patients which found less predictability of papilla height with greater distances between the contact point and crest of bone (Tarnow, 1992). Indeed, our own results demonstrated that, with a higher bone level maintained adjacent to one-piece implants, the soft-tissue distance above the original bone crest was significantly greater as compared with two-piece implants. These findings may motivate a clinician to place an implant shoulder above the alveolar crest or to utilize a one-piece implant to minimize potential inflammation and/or possible hard- or soft-tissue loss.
Based on the findings of the current study, we hypothesize that the creation of a microgap at the bone level leads to microbial leakage and a persistent bacterial presence at this peri-implant location. The chemotactic stimuli originating from the microgap then promote sustained neutrophil accumulation. In parallel, mononuclear cells are recruited to the implant surface. The combined and sustained activation of inflammatory cells promotes osteoclast formation/growth and activation to result in alveolar bone loss.
|
ACKNOWLEDGMENTS |
|---|
Received March 22, 2002; Last revision November 1, 2002; Accepted November 25, 2002
|
REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONREFERENCES |
|---|
Albrektsson T, Zarb G, Worthington P, Eriksson AR (1986). The long-term efficacy of currently used dental implants: a review and proposed criteria of success. Int J Oral Maxillofac Implants 1:11–25.[Medline]
Apse P, Zarb GA, Schmitt A, Lewis DW (1991). The longitudinal effectiveness of osseointegrated dental implants. The Toronto Study: peri-implant mucosal response. Int J Periodontics Rest Dent 11:94–111.
Assuma R, Oates T, Cochran D, Amaro S, Graves DT (1998). IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol 160:403–409.
Berglundh T, Lindhe J, Marinello C, Ericsson I, Liljenberg B (1992). Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog. Clin Oral Implants Res 3:1–8.[Medline]
Brånemark PI, Adell R, Breine U, Hansson BO, Lindstrom J, Ohlsson A (1969). Intra-osseous anchorage of dental prostheses. I. Experimental studies. Scand J Plast Reconstr Surg 3:81–100.[Medline]
Brånemark PI, Hansson BO, Adell R, Breine U, Lindstrom J, Hallen O, et al. (1977). Osseointegrated implants in the treatment of the edentulous jaw. Experience from a10-year period. Scand J Plast Reconstr Surg 16(Suppl):1–132.
Buser D, Mericske-Stern R, Bernard JP, Behneke A, Behneke N, Hirt HP, et al. (1997). Long-term evaluation of non-submerged ITI implants. Part 1: 8-year life table analysis of a prospective multi-center study with 2359 implants. Clin Oral Implants Res 8:161–172.[ISI][Medline]
Buser D, Mericske-Stern R, Dula K, Lang NP (1999). Clinical experience with one-stage, non-submerged dental implants. Adv Dent Res 13:153–161.[Abstract]
Cochran DL (1996). Implant therapy I. Ann Periodontol 1:707–791.[Medline]
Ericsson I, Berglundh T, Marinello C, Liljenberg B, Lindhe J (1992). Long-standing plaque and gingivitis at implants and teeth in the dog. Clin Oral Implants Res 3:99–103.[Medline]
Ericsson I, Nilner K, Klinge B, Glantz PO (1996). Radiographical and histological characteristics of submerged and nonsubmerged titanium implants. An experimental study in the Labrador dog. Clin Oral Implants Res 7:20–26.[ISI][Medline]
Ericsson I, Randow K, Nilner K, Petersson A (1997). Some clinical and radiographical features of submerged and non-submerged titanium implants. A 5-year follow-up study. Clin Oral Implants Res 8:422–426.[ISI][Medline]
Graves DT, Delima AJ, Assuma R, Amar S, Oates T, Cochran D (1998). Interleukin-1 and tumor necrosis factor antagonists inhibit the progression of inflammatory cell infiltration toward alveolar bone in experimental periodontitis. J Periodontol 69:1419–1425.[ISI][Medline]
Gross M, Abramovich I, Weiss EI (1999). Microleakage at the abutment-implant interface of osseointegrated implants: a comparative study. Int J Oral Maxillofac Implants 14:94–100.[ISI][Medline]
Hermann JS, Cochran DL, Nummikoski PV, Buser D (1997). Crestal bone changes around titanium implants. A radiographic evaluation of unloaded nonsubmerged and submerged implants in the canine mandible. J Periodontol 68:1117–1130.[ISI][Medline]
Hermann JS, Buser D, Schenk RK, Cochran DL (2000). Crestal bone changes around titanium implants. A histometric evaluation of unloaded non-submerged and submerged implants in the canine mandible. J Periodontol 71:1412–1424.[ISI][Medline]
Hermann JS, Buser D, Schenk RK, Schoolfield JD, Cochran DL (2001). Biologic width around one- and two-piece titanium implants. Clin Oral Implants Res 12:559–571.[ISI][Medline]
Jansen VK, Conrads G, Richter EJ (1997). Microbial leakage and marginal fit of the implant-abutment interface. Int J Oral Maxillofac Implants 12:527–540.[ISI][Medline]
Kupeyan HK, May KB (1998). Implant and provisional crown placement: a one stage protocol. Implant Dent 7:213–219.[Medline]
Lekholm U, Gunne J, Henry P, Higuchi K, Linden U, Bergstrom C, et al. (1999). Survival of the Brånemark implant in partially edentulous jaws: a 10-year prospective multicenter study. Int J Oral Maxillofac Implants 14:639–645.[ISI][Medline]
Nevins M, Langer B (1993). The successful application of osseointegrated implants to the posterior jaw: a long-term retrospective study. Int J Oral Maxillofac Implants 8:428–432.[Medline]
O’Mahony A, MacNeill SR, Cobb CM (2000). Design features that may influence bacterial plaque retention: a retrospective analysis of failed implants. Quintessence Int 31:249–256.[ISI][Medline]
Persson LG, Lekholm U, Leonhardt A, Dahlen G, Lindhe J (1996). Bacterial colonization on internal surfaces of Brånemark system implant components. Clin Oral Implants Res 7:90–95.[ISI][Medline]
Quirynen M, van Steenberghe D (1993). Bacterial colonization of the internal part of two-stage implants. An in vivo study. Clin Oral Implants Res 4:158–161.[ISI][Medline]
Quirynen M, Bollen CM, Eyssen H, van Steenberghe D (1994). Microbial penetration along the implant components of the Brånemark system. An in vitro study. Clin Oral Implants Res 5:239–244.[ISI][Medline]
Roynesdal AK, Ambjornsen E, Haanaes HR (1999). A comparison of 3 different endosseous nonsubmerged implants in edentulous mandibles: a clinical report. Int J Oral Maxillofac Implants 14:543–548.[ISI][Medline]
Schenk RK, Olah AJ, Herrmann W (1984). Preparation of calcified tissues for light microscopy. In: Methods of calcified tissue preparation. Vol. 1. Dickson GR, editor. Amsterdam: Elsevier Science Publishers BV, pp. 1-56.
Schroeder A, van der Zypen E, Stich H, Sutter F (1981). The reactions of bone, connective tissue, and epithelium to endosteal implants with titanium-sprayed surfaces. J Maxillofac Surg 9:15–25.[ISI][Medline]
Tarnow DP, Magner AW, Fletcher P (1992). The effect of the distance from the contact point to the crest of bone on the presence or absence of the interproximal dental papilla. J Periodontol 63:995–996.[ISI][Medline]
This article has been cited by other articles:
|
|
 |
|
  S.M. Heckmann, J.J. Linke, F. Graef, Ch. Foitzik, M.G. Wichmann, and H.-P. Weber Stress and Inflammation as a Detrimental Combination for Peri-implant Bone Loss. J. Dent. Res., August 1, 2006; 85(8): 711 - 716. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Broggini, L.M. McManus, J.S. Hermann, R. Medina, R.K. Schenk, D. Buser, and D.L. Cochran Peri-implant Inflammation Defined by the Implant-Abutment Interface. J. Dent. Res., May 1, 2006; 85(5): 473 - 478. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| IADR Journals | Advances in Dental Research ® |
| Journal of Dental Research ® | Critical Reviews (1990-2004) |
