J. BIOMED. MATER. RES. SYMPOSIUM
No. 6, pp. 263-269 (1975)
The Epithelium Contiguous with the Neck of Intraosseous Dental Implants RICHARD B. JOHNS, Department of Conservative Dental Surgery, Guy’s Hospital Dental School, London, England.
Summary There are three distinct regions with which a wedge shaped dental implant is in contact; the intraoral, transitional and intraosseous portions. The environment of each of these is different and will require special consideration. This investigation compares the epithelium found associated with a natural tooth to that which is found contiguous with the transitional region of an implant. The possibility of a pseudojunctional epithelium being formed in association with a glass collar processed onto the neck of a wedge shaped implant is examined. The histological appearance of a specimen in situ for I 1 months shows an altered epithelial structure compared to that found adjacent to the neck of an unmodified titanium wedge shaped implant. Because the implant and glass must be mechanically separated from the tissue being examined, the value of demeneratized histological sections is limited. However, examination by a Scanning Electron Microscope of the surface of the glass after removal reveals an area of clear glass in the deeper region of the collar. Above this there is a deposit, the exact nature of which is unknown, but which might be interpreted as the contents of the gingival crevice. Although this might be interpreted as a type of epithelial attachment, other factors are necessary to ensure close gingival adaptation and limitation on epithelial downgrowth.
INTRODUCTION A material which is implanted within the tissues will evoke a reaction from the environment. Similarly, an implanted material will itself be affected by the environment. The extent of both these reactions will depend not only on the implant material, the shape and surface finish it has, but also on the chemical and mechanical forces to which each is subjected. There are three distinct regions across which these reactions take place in the case of most dental implants. These are the intraoral, the transitional and the intraosseous regions. In the case of diodontic (endosseous endodontic) implants, only an intraosseous interface is involved. The transitional region, where the epithelium is apposed to the implant itself, has attracted attention since Guilford [l] in 1913 suggested that unless a seal were established between the oral epithelium and the implant, long-term success could not be expected. 263
0 1975 by John Wiley & Sons, Inc.
264
JOHNS
The understanding of this particular region should be considered by comparison with the gingival epithelium associated with a natural tooth, described by Smith [2] as having three distinct subdivisions. 1) The masticatory gingival epithelium, characterized by keratinized squamous epithelium on a basal membrane with deep rete ridges. 2) T h e crevicular gingival epithelium, made up of a thinner layer of unkeratinized cells supported on an undulating basal membrane. 3) The attached epithelial cuff, consisting of a thin layer of flattened cells, supported on a smooth basal membrane. The surface layer of the cells is separated from the tooth by a granular layer which has a similarity to the basal membrane found between the epithelium and the underlying connective tissue. The distance over which the junctional epithelium extended appeared to vary according t o the type of surface with which it was in contact. Smith noted that this distance was shortest when the epithelium was confined to cementum, but it was considerably longer when enamel was the sole surface presented t o it. H e also suggested that the apical extension of the junctional epithelium was probably limited by the upper fibers of the periodontal membrane. It has been noted by the author [3] that there was little difference between t h e pseudomasticatory a n d t h e psuedocrevicular epithelia associated with t h e necks of wedge shaped implants and their natural analogues. The psuedojunctional epithelium when it was in contact with the neck of these titanium wedge shaped implants, for which no specific surface treatment had been carried out, was markedly different. Not only were the cell layers thicker and irregular, but they were supported on tissue either infiltrated with inflammatory cells or on granulation tissue. N o apparent demarcation appeared t o exist between the crevicular and attached epithelia. The depth of penetration was variable and could not have been limited by the fibers which surround the implant surface as these were all oriented parallel t o the interface. Epithelial cells in vitro have been shown to become attached t o a n inorganic base by Flaxman et al. [4] using nitrocellulose film. Weiss [5] demonstrated that fibroblasts imparted some material to this surface of glass plates following culture which made the glass more receptive to subsequent tissue adhesion. Taylor [6] demonstrated that freshly cultured epithelial cells showed a far stronger attachment t o a n artificial surface t h a n those which had been maintained longer in vitro. H e also demonstrated that the attachment of these cells was so strong, they were liable to become moribund if they were forcibly detached. T h e possibility of an epithelial attachment being formed t o the neck of a dental implant, onto which a glass collar has been processed, can be postulated on the grounds that: 1) Epithelium has the ability t o reform a close relationship with a tooth following surgical reflection of the gingival tissue; 2) the evidence of Skougaard and Beagrie [7], using labelled Thy-
INTRAOSSEOUS DENTAL IMPLANTS
265
midine H3, showed that there was a dynamic cell movement in the region of the junctional epithelium and therefore a fresh attachment was being continually established between these cells and the tooth surface; and 3) the demonstrations in vitro of cell attachment to an inorganic surface by Weiss [ 5 ] and Flexman et al. [4]. If such a n attachment were to be effective in this region of an implant the following would have to be considered: 1 ) The shape. This would probably have to bear some resemblance to the neck of a tooth. 2) The texture. It would be necessary to ensure that the surface did not impede dynamic cell movement. 3) The chemical surface activity. Cell attachment to glass in vitro may require pretreatment with acid to promote attachment for some types of glass. In vivo the presence of blood plasma may obviate this pretreatment. 4) The presence of bacterial plaque. The liberation of toxins from bacterial plaque will inhibit epithelial attachment. However, Listgarten and Ellegaard [8] have demonstrated that epithelial attachment to calculus was possible following regular irrigation with chlorhexidine gluconate. TECHNIQUE T h e investigation t o study the epithelial response to a glass collar processed onto the neck of an implant was undertaken in collaboration with the Atomic Weapons Research Establishment, Aldermaston, England. Standard titanium wedge shaped implants were modified as follows. First, by the plasma spraying of the intraosseous region with titanium hydride to give a porous surface, this being part of a concurrent investigation. Secondly, the implants were modified by the processing of a glass collar approximately 3 mm high and 1 mm thick just below the neck of the abutment (Fig. 1). Four of these implants were placed into the mandibles of 2 Macaca irus monkeys, the appropriate teeth having been extracted 32 weeks previously. The implant shown in Figure 2 remained firm and in function after insertion until the animal was sacrificed 48 weeks later. Preparation of the Material
Sectioning was planned so that the mandible containing the implant was cut buccolingually into 6 small blocks. Simultaneous cutting with 5 or 7 discs mounted on one shaft ensured that there was a minimum of implant movement within the tissues and therefore a minimum of damage to the specimens. The middle disc was aligned to pass through the center of the abutment (Fig. 3).
266
JOHNS
Fig. 1 . A wedge shaped dental implant, the body of which is coated with porous titanium. A glass collar has been processed onto the neck of the implant.
Alter'nate blocks were demineralized and this necessitated the removal of the implant material when the specimens were embedded in wax and just before sections were cut. The study of the junctional epithelium is therefore restricted by a histological method which necessitated the physical rupture of any attachment which might have existed. For this reason the glass surface of the implant was examined before and after
Fig. 2. Intraoral view of an implant similar to that shown in Figure 1 which had been in situ in a Macaca irus monkey for 6 months.
INTRAOSSEOUS DENTAL IMPLANTS
261
Fig. 3 . Sectioning machine showing 5 silicon carbide discs mounted on one shaft cutting through a section of mandible supported in a plaster block.
implantation with a Scanning Electron Microscope t o detect any alteration in the surface. Those blocks which were not demineralized were embedded in a polyester resin in preparation for surface staining and later sectioning for microradiographic analysis.
RESULTS Although clinically some form of attachment seemed to have occurred in association with the glass, histologically the evidence is only that there is an altered epithelial response compared to the tissue contiguous with an untreated titanium surface over a comparable period. A low power magnification of the glass collar using a Scanning Electron Microscope (Fig. 4), does show what appears to be a clear area of glass below a region on which a deposit is evident. The chemical composition of this materi a1 is being investigated.
DISCUSSION Mack [9] suggested, in relation t o subperiosteal implants, that a process of exteriorization by epithelial proliferation took place around
268
JOHNS
Fig. 4. Scanning electron micrograph of the glass collar of a dental implant which had been in situ 48 weeks. (13 x ) .
implants. It would appear that this was not the case with these particular implants. However, it is not clear whether epithelial downgrowth is limited by the type of surface with which it is in contact, the character of the tissue over which it passes, or the presence of fibrous tissue surrounding the implant. Nevertheless if some form of attachment were proved t o exist, Loe [lo], and Schroeder and Listgarter [ I l l regarded the strength of the epithelial attachment to a tooth as having a relatively minor effect in resisting the disruptive forces to which the whole gingival region is subjected. It was their opinion that the more significant forces of adaptation were the presence of circular, free gingival and crestal fibers, together with the capillary blood pressure within the gingiva, which maintained the contact between the epithelium and the tooth. Although the arrangement of the fibrous tissue and capillaries round the implant abutments appears haphazard, compared with that seen around teeth, the effect of the blood pressure within these tissues could be expected to have at least some adaptive influence.
INTRAOSSEOUS DENTAL IMPLANTS
269
Attempts to measure the force required to separate the junctional epithelium from the tooth are vulnerable to experimental error and, according to Zander [ 121 were not attempted in this investigation.
CONCLUSION The effect on the tissues of a smooth glass collar in the region of the penetration of the epithelium by an implant, gives a clinically satisfactory appearance. However, histologically, it is not yet possible to demonstrate attachment, although SEM views suggest that some form of attachment might exist. The finite limitation of epithelial downgrowth may have to await the development of a prosthesis which can simulate cementum to the extent of allowing the formation of all associated types of periodontal fibers. Whatever prosthesis may be developed, it is clearly necessary that the pseudogingival tissue must be capable of being cleaned easily by the patient and inspected by the operator; for this reason all intraoral superstructures should be designed to be removable whenever possible. References [I] D. Guilford, Denf. Cosmos, 55. 437 (1913). [2] C. Smith, in Biology of f h e Periodontiurn, A. H . Melcher, and W. H. Bowen, Acad. Press, London, 1969. [3] R. B. Johns, Ph.D Thesis, University of London, 1974. [4] B. A. Flaxman, M. A. Lutzner, and E. J . Van Scott, J . Cell. Biol., 36, 406 (1968). [5] L. Weiss,Exp. Cell. Res. Suppl., 8 . 141 (1961). [6] A. C. Taylor, in Adhesion in Biological Sysfems. R. S. Manly, Academic Press, New York, 1970. [7] M . R . Skougaard and G . S. Beagrie, A c f a . Odonfol. Scand., 20, 467 (1960). 181 M. A. Listgarten and B. El1egaard.J. Periodontal Res., 8. 143 (1973). 191 A. 0. Mack, M. D. S. Thesis, University of Durham, 1958. [lo] H. Loe, in Periodonml Therapy, H. M . Goldman and D. W. Cohen, Eds., Mosby, St. Louis, 1968. [ I l l H. E. Schroeder and M . A. Listgarten, Monographs in Developrnenral Biology, Vol. 2, Bade, New York, 197 I . [I21 H. A. ZanderJ. Denr. Res. 3.5, 308 (1956).
No. 6, pp. 263-269 (1975)
The Epithelium Contiguous with the Neck of Intraosseous Dental Implants RICHARD B. JOHNS, Department of Conservative Dental Surgery, Guy’s Hospital Dental School, London, England.
Summary There are three distinct regions with which a wedge shaped dental implant is in contact; the intraoral, transitional and intraosseous portions. The environment of each of these is different and will require special consideration. This investigation compares the epithelium found associated with a natural tooth to that which is found contiguous with the transitional region of an implant. The possibility of a pseudojunctional epithelium being formed in association with a glass collar processed onto the neck of a wedge shaped implant is examined. The histological appearance of a specimen in situ for I 1 months shows an altered epithelial structure compared to that found adjacent to the neck of an unmodified titanium wedge shaped implant. Because the implant and glass must be mechanically separated from the tissue being examined, the value of demeneratized histological sections is limited. However, examination by a Scanning Electron Microscope of the surface of the glass after removal reveals an area of clear glass in the deeper region of the collar. Above this there is a deposit, the exact nature of which is unknown, but which might be interpreted as the contents of the gingival crevice. Although this might be interpreted as a type of epithelial attachment, other factors are necessary to ensure close gingival adaptation and limitation on epithelial downgrowth.
INTRODUCTION A material which is implanted within the tissues will evoke a reaction from the environment. Similarly, an implanted material will itself be affected by the environment. The extent of both these reactions will depend not only on the implant material, the shape and surface finish it has, but also on the chemical and mechanical forces to which each is subjected. There are three distinct regions across which these reactions take place in the case of most dental implants. These are the intraoral, the transitional and the intraosseous regions. In the case of diodontic (endosseous endodontic) implants, only an intraosseous interface is involved. The transitional region, where the epithelium is apposed to the implant itself, has attracted attention since Guilford [l] in 1913 suggested that unless a seal were established between the oral epithelium and the implant, long-term success could not be expected. 263
0 1975 by John Wiley & Sons, Inc.
264
JOHNS
The understanding of this particular region should be considered by comparison with the gingival epithelium associated with a natural tooth, described by Smith [2] as having three distinct subdivisions. 1) The masticatory gingival epithelium, characterized by keratinized squamous epithelium on a basal membrane with deep rete ridges. 2) T h e crevicular gingival epithelium, made up of a thinner layer of unkeratinized cells supported on an undulating basal membrane. 3) The attached epithelial cuff, consisting of a thin layer of flattened cells, supported on a smooth basal membrane. The surface layer of the cells is separated from the tooth by a granular layer which has a similarity to the basal membrane found between the epithelium and the underlying connective tissue. The distance over which the junctional epithelium extended appeared to vary according t o the type of surface with which it was in contact. Smith noted that this distance was shortest when the epithelium was confined to cementum, but it was considerably longer when enamel was the sole surface presented t o it. H e also suggested that the apical extension of the junctional epithelium was probably limited by the upper fibers of the periodontal membrane. It has been noted by the author [3] that there was little difference between t h e pseudomasticatory a n d t h e psuedocrevicular epithelia associated with t h e necks of wedge shaped implants and their natural analogues. The psuedojunctional epithelium when it was in contact with the neck of these titanium wedge shaped implants, for which no specific surface treatment had been carried out, was markedly different. Not only were the cell layers thicker and irregular, but they were supported on tissue either infiltrated with inflammatory cells or on granulation tissue. N o apparent demarcation appeared t o exist between the crevicular and attached epithelia. The depth of penetration was variable and could not have been limited by the fibers which surround the implant surface as these were all oriented parallel t o the interface. Epithelial cells in vitro have been shown to become attached t o a n inorganic base by Flaxman et al. [4] using nitrocellulose film. Weiss [5] demonstrated that fibroblasts imparted some material to this surface of glass plates following culture which made the glass more receptive to subsequent tissue adhesion. Taylor [6] demonstrated that freshly cultured epithelial cells showed a far stronger attachment t o a n artificial surface t h a n those which had been maintained longer in vitro. H e also demonstrated that the attachment of these cells was so strong, they were liable to become moribund if they were forcibly detached. T h e possibility of an epithelial attachment being formed t o the neck of a dental implant, onto which a glass collar has been processed, can be postulated on the grounds that: 1) Epithelium has the ability t o reform a close relationship with a tooth following surgical reflection of the gingival tissue; 2) the evidence of Skougaard and Beagrie [7], using labelled Thy-
INTRAOSSEOUS DENTAL IMPLANTS
265
midine H3, showed that there was a dynamic cell movement in the region of the junctional epithelium and therefore a fresh attachment was being continually established between these cells and the tooth surface; and 3) the demonstrations in vitro of cell attachment to an inorganic surface by Weiss [ 5 ] and Flexman et al. [4]. If such a n attachment were to be effective in this region of an implant the following would have to be considered: 1 ) The shape. This would probably have to bear some resemblance to the neck of a tooth. 2) The texture. It would be necessary to ensure that the surface did not impede dynamic cell movement. 3) The chemical surface activity. Cell attachment to glass in vitro may require pretreatment with acid to promote attachment for some types of glass. In vivo the presence of blood plasma may obviate this pretreatment. 4) The presence of bacterial plaque. The liberation of toxins from bacterial plaque will inhibit epithelial attachment. However, Listgarten and Ellegaard [8] have demonstrated that epithelial attachment to calculus was possible following regular irrigation with chlorhexidine gluconate. TECHNIQUE T h e investigation t o study the epithelial response to a glass collar processed onto the neck of an implant was undertaken in collaboration with the Atomic Weapons Research Establishment, Aldermaston, England. Standard titanium wedge shaped implants were modified as follows. First, by the plasma spraying of the intraosseous region with titanium hydride to give a porous surface, this being part of a concurrent investigation. Secondly, the implants were modified by the processing of a glass collar approximately 3 mm high and 1 mm thick just below the neck of the abutment (Fig. 1). Four of these implants were placed into the mandibles of 2 Macaca irus monkeys, the appropriate teeth having been extracted 32 weeks previously. The implant shown in Figure 2 remained firm and in function after insertion until the animal was sacrificed 48 weeks later. Preparation of the Material
Sectioning was planned so that the mandible containing the implant was cut buccolingually into 6 small blocks. Simultaneous cutting with 5 or 7 discs mounted on one shaft ensured that there was a minimum of implant movement within the tissues and therefore a minimum of damage to the specimens. The middle disc was aligned to pass through the center of the abutment (Fig. 3).
266
JOHNS
Fig. 1 . A wedge shaped dental implant, the body of which is coated with porous titanium. A glass collar has been processed onto the neck of the implant.
Alter'nate blocks were demineralized and this necessitated the removal of the implant material when the specimens were embedded in wax and just before sections were cut. The study of the junctional epithelium is therefore restricted by a histological method which necessitated the physical rupture of any attachment which might have existed. For this reason the glass surface of the implant was examined before and after
Fig. 2. Intraoral view of an implant similar to that shown in Figure 1 which had been in situ in a Macaca irus monkey for 6 months.
INTRAOSSEOUS DENTAL IMPLANTS
261
Fig. 3 . Sectioning machine showing 5 silicon carbide discs mounted on one shaft cutting through a section of mandible supported in a plaster block.
implantation with a Scanning Electron Microscope t o detect any alteration in the surface. Those blocks which were not demineralized were embedded in a polyester resin in preparation for surface staining and later sectioning for microradiographic analysis.
RESULTS Although clinically some form of attachment seemed to have occurred in association with the glass, histologically the evidence is only that there is an altered epithelial response compared to the tissue contiguous with an untreated titanium surface over a comparable period. A low power magnification of the glass collar using a Scanning Electron Microscope (Fig. 4), does show what appears to be a clear area of glass below a region on which a deposit is evident. The chemical composition of this materi a1 is being investigated.
DISCUSSION Mack [9] suggested, in relation t o subperiosteal implants, that a process of exteriorization by epithelial proliferation took place around
268
JOHNS
Fig. 4. Scanning electron micrograph of the glass collar of a dental implant which had been in situ 48 weeks. (13 x ) .
implants. It would appear that this was not the case with these particular implants. However, it is not clear whether epithelial downgrowth is limited by the type of surface with which it is in contact, the character of the tissue over which it passes, or the presence of fibrous tissue surrounding the implant. Nevertheless if some form of attachment were proved t o exist, Loe [lo], and Schroeder and Listgarter [ I l l regarded the strength of the epithelial attachment to a tooth as having a relatively minor effect in resisting the disruptive forces to which the whole gingival region is subjected. It was their opinion that the more significant forces of adaptation were the presence of circular, free gingival and crestal fibers, together with the capillary blood pressure within the gingiva, which maintained the contact between the epithelium and the tooth. Although the arrangement of the fibrous tissue and capillaries round the implant abutments appears haphazard, compared with that seen around teeth, the effect of the blood pressure within these tissues could be expected to have at least some adaptive influence.
INTRAOSSEOUS DENTAL IMPLANTS
269
Attempts to measure the force required to separate the junctional epithelium from the tooth are vulnerable to experimental error and, according to Zander [ 121 were not attempted in this investigation.
CONCLUSION The effect on the tissues of a smooth glass collar in the region of the penetration of the epithelium by an implant, gives a clinically satisfactory appearance. However, histologically, it is not yet possible to demonstrate attachment, although SEM views suggest that some form of attachment might exist. The finite limitation of epithelial downgrowth may have to await the development of a prosthesis which can simulate cementum to the extent of allowing the formation of all associated types of periodontal fibers. Whatever prosthesis may be developed, it is clearly necessary that the pseudogingival tissue must be capable of being cleaned easily by the patient and inspected by the operator; for this reason all intraoral superstructures should be designed to be removable whenever possible. References [I] D. Guilford, Denf. Cosmos, 55. 437 (1913). [2] C. Smith, in Biology of f h e Periodontiurn, A. H . Melcher, and W. H. Bowen, Acad. Press, London, 1969. [3] R. B. Johns, Ph.D Thesis, University of London, 1974. [4] B. A. Flaxman, M. A. Lutzner, and E. J . Van Scott, J . Cell. Biol., 36, 406 (1968). [5] L. Weiss,Exp. Cell. Res. Suppl., 8 . 141 (1961). [6] A. C. Taylor, in Adhesion in Biological Sysfems. R. S. Manly, Academic Press, New York, 1970. [7] M . R . Skougaard and G . S. Beagrie, A c f a . Odonfol. Scand., 20, 467 (1960). 181 M. A. Listgarten and B. El1egaard.J. Periodontal Res., 8. 143 (1973). 191 A. 0. Mack, M. D. S. Thesis, University of Durham, 1958. [lo] H. Loe, in Periodonml Therapy, H. M . Goldman and D. W. Cohen, Eds., Mosby, St. Louis, 1968. [ I l l H. E. Schroeder and M . A. Listgarten, Monographs in Developrnenral Biology, Vol. 2, Bade, New York, 197 I . [I21 H. A. ZanderJ. Denr. Res. 3.5, 308 (1956).
