Volume 69 January 1976

Section of Odontology President B E D Cooke MDS FRCPath

Meeting 28 April 1975

Paper Experimental Studies on Dental Implants by R B Johns PhD LDS RCS (Department of Conservative Dental Surgery, Guy's Hospital, London SE] 9RT) However long the research into dental caries and periodontal disease and whatever its outcome, there is no doubt that prosthetic teeth will continue to be in demand for a number of dental mishaps. The absence of teeth may be the result of bacterial activity, injury, genetic aberration or even iatrogenic interference. By the definition that an implant is 'a foreign body retained within the tissues of the body', dentistry can claim many millions of successful implants in the form of restorations to teeth. These have succeeded because satisfactory interface has been established between the implant and the tooth. However, for the implant which is to replace a whole tooth, whatever shape it may be, the problem is how to establish an interface which is both functional and stable with cells which are being continually replaced. Success of an implant must be based on two criteria: (1) It must be clinically practicable. It must exhibit stability at least equivalent to that a

demanded of a tooth which is to support a crown or which is to act as a bridge abutment. The intrinsic stability of an implant must be in no way hidden by the stability imparted to it from standing teeth through the intra-oral component of the prosthesis. (2) Histological evidence requires not only that the tissue around an implant shows no marked inflammatory response but that there is evidence that the tissue will support a functional

implant. Classification Any implant material associated with the body must have one of the following relationships with the tissues (Fig 1): (1) Total implantation without epithelial involvement. (2) Partial implantation with discontinuity of the epithelium. (3) Partial implantation with exteriorization by the establishment of epithelial continuity. Implants which are partially buried are normally used in surgery only on a temporary basis; however, dental implants apart from the diodontic variety (often called endodontic) and a few minor exceptions, are all within this group. It is convenient to classify dental implants by their function (Table 1), those which merely aid retention of an intra-oral prosthesis being classified as 'retentive implants'. These implants do not

r'able 1 Classification of dental implants (from Johns 1975)

DENTAL IMPLANTS Retentive ottive Troq i hrti Ihessal _puts hurts tmnridp







peak 11 2 Op.I.tcu


2 Scrmwwith i trsal mts


Fig I Diagram illustrating the three possible relationships of an implant with the tissues: A, totally buried. B, partially buried. c, buried but exteriorized. (Reproducedfrom Johns 1975 by kind permission)


3 Tutnuwutb


4 Wid shaped

4 Tuthhrf 5 Siq . pttpies 6 WOtidcpW (u1 dtic t u.)


SUbiUhgl M tS





Proc. roy. Soc. Med. Volume 69 January 1976

























Implant initially retained by wedging effect. Implant retained by acrylic cement. Represents the time at which the teeth were






Fig 2 Diagram showing the three regions Fig 3 1Duration ofimplants in situ. The initial letter of the ordinaite indicates the animal; the second letter indicates the of a wedge-shaped or 'blade vent' implant described by Linkow (1968b) side, leeft or right relieve the mucoperiostium from the function of on the dimensions of the spaces within the overall transmitting loads from the prosthesis to the outline of the implant. bone. Not only is this tissue unsuited for such a purpose but as age increases it becomes pro- Experimental Method gressively less able to withstand compressive Shortly after Linkow (1968a) described 'vent forces. In contrast, those implants which transmit plant' screws he also proposed wedge-shaped or functional loads and bypass the mucoperiostium 'blade vent' implants of various outline forms are termed 'supportive implants'. (Linkow 1968b). The implants within the supportive group are In this investigation the implants were made to further divided into those which gain their the general design shown in Fig 2. They were support from the outer aspect of the cortical bone, made of titanium and this study is based on the for example subperiosteal implants, and those tissue response of Macaca irus monkeys to them. which gain their support from within the cortical This monkey was chosen because it is a nearbone, the endosseous varieties. The subperiosteal human primate with eating habits and an oral design originated from the work of Dahl (1943) flora closely related to those of man. Following and was further developed by Gerschoff & extraction of mandibular premolar and molar Goldberg (1949, 1957). There are many reports of teeth which were erupted, a minimum period of 3 similar designs having been used (Natiella et al. months was allowed for healing to take place. A total of 14 implants were inserted of which 8 1972), including some animal studies by Mack (1958). In spite of the claim of long-term success were either exfoliated or had to be removed by Trainin (1957) and Bodine & Mohammed during the course of the experiment. At the ehd (1970), Obwegeser (1959) reported that only 9 of the experimental period 6 implants were still out of 32 implants studied were successftl and in situ. The duration of the healing period and furthermore he was unable to determine the retention of the various implants is indicated in Fig 3; failures may have been attributable to the reasons for success. The endosseous designs have the attraction ability of the monkeys to touch the intra-oral that their support appears to be gained in a projections and to manipulate small objects manner analagous to that of a tooth. However, beside the implants. Clinical records were kept they suffer from the problem of the transition of the mobility of the implants, the appearance of from immediate to long-term retention. Im- the tissues immediately adjacent to the abutments mediate retention may be achieved either by and the apparent depth of the pseudogingival splinting the implant to an adjacent structure, crevice. like a tooth, or by screwing or wedging it into When the animals were killed a perfusion compact cortical bone. Unfortunately the reten- technique was employed (Brain 1966) to ensure tion may be only short lived if the supporting rapid tissue fixation. The direction and spacing tooth is too mobile or if the stress induced in the of each tissue block was decided on the basis of surrounding bone is too little or too great. If bone the post-mortem radiograph of each mandible formation were stimulated in the same manner (Fig 4). These divisions were made by thin that dynamic compression plates stimulate bone silicon carbide blades appropriately separated by in the repair of fractures of long bones (Perren washers and mounted coaxially on a cutting et al. 1969), then screw and wedge-shaped machine. The blocks were prepared simultaneousimplants may indeed undergo a rapid transition ly in order to reduce the risk of distortion at the from immediate to long-term retention. The tissue/implant interface which might have ocrapidity and extent to which bone ingrowth will curred if sequential cutting had been used. Alternate blocks were demineralized for conoccur depends not only on the stress, stability of the implant, age and individual variation, but also ventional histological cutting and staining,

Section of Odontology



Results Five examples are chosen of the tissue reaction resulting from these experiments:



Fig 4 A, post-mortem radiograph. B, line drawing representing the direction and spacing chosen for the sectioning of each tissue block implant material being removed when the tissue had reached the stage of being embedded in wax. The other blocks were embedded in a polyester resin using a technique similar to that described by Mack (1958) but modified by E H Jennings (1971, personal communication). Sections prepared from these blocks were ground to approximately 80 ,um thickness for microscopic examination under ultraviolet light. This was done to show the fluorescence induced in the forming bone (Milch et al. 1958, Milch et al. 1961) by the administration of single doses of tetracycline at weekly intervals in the four weeks preceding the killing of the animals. Microradiographs were also made of the same sections in a manner similar to that described by Jowsey et al. (1965) and Kalwitter & Hulbert (1971).

(1) An implant, which was in situ eighteen months, had shown clinically slight buccolingual mobility at one week and an approximately even pseudocrevicular depth of 3 mm for the first seven weeks. The tissue routid the implant abutment had bled on being touched during this period but subsequently the inflammation and pocket depth were no more than that found associated with functional teeth in the same animal. The histological appearance of the tissue around the abutment showed the pseudocrevicular epithelium to be similar to that seen round a tooth but there was no clear demarcation in the region where the attached epithelium might have been expected. The downgrowth of epithelium in this region appears to have been limited by the presence of inflammatory cells (Fig 5). Even after eighteen months there was no evidence that exteriorization had taken place. The proximity of the bone to the implant, away from the abutment region, is evident from a microradiograph of a section prepared from tissue mesial to the abutment region (Fig 6). That this bone was actively being formed in the month before the end of the experiment was evident from the fluorescence, due to the tetracycline marking of the bone, close to the apex of the wedge of the implant (Fig 7). (2) An implant, which had been in situ ten weeks, had appeared clinically firm for the first two weeks but at the end of the experimental period it had had a mobility of 3 mm in a buccolingual direction. The inflammation round the implant

Fig 5 Photomicrograph ofsection adjacent Fig 6 Microradiographs ofsection mesial to abutment to an implant abutment which had been in region of that shown in Fig 5. A, X 3.5. B, X 35 situ eighteen months, showing bone (B) and thin layer ofepithelial cells (E) over granulation tissue (G). H. & E. x 55


Proc. roy. Soc. Med. Volume 69 January 1976

Fig 7 Photomicrograph ofsection shown in Fig 6B viewed by transmitted ultraviolet light (3650 nm). Both autofluorescence and tetracycline-induced fluorescence (T) can be identified. x 35

abutment had been marked until the fifth week and had then improved to a condition apparently similar to that observed round functional teeth by the end of the experiment. The post-mortem radiograph (Fig 8) had indicated areas of bone loss round the implant and these were confirmed by the microradiographs. The demineralized sections showed that the implant was surrounded by inflammatory cells and a thick layer of fibrous tissue; there was also evidence of active bone resorption. Epithelial cells were proliferating beside the abutment and were also identifiable adjacent to the implant in sections remote from that region. The origin of these latter cells is likely to have been either a result of migration along the surface of the implant or by their inclusion within the tissues when the implant was inserted. (3) An implant, which had been in situ only eight weeks at the end of the experiment, had remained firm during the whole of the period. The apparent depth of the pseudogingival crevice had remained at no more than one millimetre and the appearance of the tissue was similar to that seen round functional teeth. It might be assumed that in this instance the implant had made a successful transition from immediate retention due to impaction against cortical bone, to longer term retention due to proliferation of bone through and round the implant. Demineralized sections

Fig 8 Post-mortem radiograph of right half of mandibl. The

implant had been in


eighteen weeks


prepared from blocks of tissue from either end of this implant suggested that the bone had indeed formed in a very similar manner to the bony thimble seen round the roots of teeth. However, there was some contradictory evidence in the sections through the abutment region. These showed not only a thickening of the epithelium of the pseudocrevicular region but also that the bone had not been closely adapted to the neck of the implant (Fig 9). A 'U' shaped trough, similar to a periodontal infrabony pocket, was seen round teeth and this may have been a consequence of the absence of fibres, analagous to Sharpey's fibres, stimulating the crestal bone.

Fig 9 A, low power photomicrograph of section through abutment ofimplant which had been in situ eight weeks. H. & E. x 3.5. B, diagram indicating the section

(4) An implant, which was assessed as a clinical failure after only two weeks, was very mobile with deep pocketing and gingival tissue which was inflamed and bled easily. Two implants had previously been placed at the same site (monkey DR, Fig 3): the first lasted a little less than nine weeks, the second was inserted after a healing period of twenty-nine weeks and remained only a fortnight. The third implant had been inserted after a healing period of ten weeks. The demineralized histological appearance supported the clinical assessment at the end of the experiment in this instance. The microradiographs demonstrated the effect upon the bone of the current and previous implant attempts and possibly that of the extractions as well (Fig 10). The explanation for this bone formation may have been that it was a result of the weakening effect on the mandible by the discontinuity created in the upper aspect of the cortical bone to accommodate the implant. Alternatively, it may have been a result of the compression imposed on the outer aspect of the lower border by the insertion of a wedge-shaped implant. However, the stress imposed by the wedging effect would have been of a relatively short duration. It would seem more li1kely, therefore, that the phenomenon of this pattern of bone formation was a direct consequence of the weakening effect of the whole implant procedure upon the mandible.

Section ofOdontology



of the whole implant procedure on the mandible rather than the stress induced by the wedging effect. This explanation is further supported by the fact that, because acrylic was used to retain the implant, little or no wedging stress had been imposed upon the bone.

Fig 10 Microradiograph oflower border ofmandible of monkey with three implants inserted (see Fig 3, monkey DR). A, mature cortical bone, some osteones in resting phase, some actively mineralizing and some showing evidence ofresorption. B, generally less well mineralizedperiosteal bone. c, periosteal bone with more numerous vascular channels. D, similar vascular channels but the least mineralized tissue. x 60

Fig 11 Demineralized

section of mandible of monkey DL from which an implant had been shed ten weeks previously. It shows almost complete infilling of the medullary space with woven bone. H.& E. x 3.5

As a result of the information gathered from these experiments a further series was embarked upon. It was felt that the tissue response at the neck of the implants might be influenced by the surface characteristics of the implant. It was decided to process a glass collar on to this region of a wedge-shaped implant. This was based on three facts: (1) Reattachment of epithelium to a tooth can occur following surgical procedures. (2) The apposition of junctional epithelium to a tooth is regarded as a dynamic state in which attachment and separation are a normal part of the mechanism. (3) A firm bond between epithelial cells and glass can be established in vitro (Weiss 1961). An implant modified not only with a coating of plasma-sprayed porous titanium over its body, but also with a fused glass collar (Fig 12), remained firm for the experimental period of eleven months. After the initial healing the pocket depth appeared to remain between 2 and 3 mm and the pseudogingival tissue appeared similar to that of the normal gingive (Fig 13).

(5) Finally, consideration was given to the effect on the tissues of the loss of an implant. A mandible, from which a wedge-shaped implant had been shed ten weeks before the end of the experiment, was studied (monkey DL, Fig 3). The im- Fig 12 Glass collarfused round neck ofplasma-sprayed plant had been in position only four weeks and porous titanium implant

had been retained by acrylic bone cement (Surgical Simplex 'C': North Hill Plastics) when it was exfoliated. The demineralized sections show that the medullary space had been almost completely filled in with woven bone (Fig 1 1). A microradiograph of an adjacent section showed this bone not to be highly mineralized, in fact only a small region of the whole section showed evidence of well mineralized mature bone. It was only during the period that the implant was in situ that the bone-marking technique was employed in this instance. The tetracycline staining showed that much of the subperiosteal bone formation round the lower border of the mandible had in fact taken place after the implant had been shed. This suggests that the bone formation is indeed in response to the weakening

Fig 13 Intra-oral view of wedge-shaped implant shown in Fig 12 six months after insertion



Proc. roy. Soc. Med. Volume 69 January 1976


.--=_I . wWQs

Fig 16 Scanning electron micrograph of surface ofglass adjacent to that shown in Fig 15. x 320

Fig 14 Demineralized section ofneck regiion of implant which had been in situ eleven months. H. i{E. x 35

The histological material was prepared in a manner similar to that described previously but with the addition of surface staining of the ground sections with a polychromatic stain (Paragon 1301: Paragon C & C, Bronx, NY 10454, USA) as mentioned by Kalwitter & Hulbert (1971). This method gives moderately good cell detail and has the advantage that soft tissue can be seen in a relationship to the implant which is only very slightly distorted. It can be seen from the demineralized section (Fig 14) that although 'there appears to be a demarcation between the pseudocrevicular and pseudojunctional epithelium, the latter is unlike its natural analogue and -is proliferating beyond the glass neck of the implant. It is also evident that the surface of the glass from this region no longer appears smooth (Fig 15), as it had been before the experiment. On examination with a scanning electron microscope the surface of the glass showed that it had undergone erosion (Fig 16).


(1) Wedge-shaped dental implants inserted from within the mouth can remain in the tissues without evoking an adverse reaction from the bone. (2) These implants do not appear to have stimulated the formation of a structure which is in any way analagous to a periodontal membrane. (3) The response of the epithelium to the unpolished titanium at the neck of the implant was unlike that associated with a tooth. Although crevicular-like epithelium did appear to have formed there was no evidence of a pseudojunctional epithelium. (4) When the neck of an implant had been modified with a glass collar there was still no evidence of the establishment of a pseudojunctional epitheliurii, but there was evidence of erosion of the glass.

Fig 15 Ground section ofneck region ofi? nplant which had been in situ eleven months. G, glass c ollar. E, epithelium. Paragon 1301. x 60

Discussion The widespread practice of inserting wedgeshaped implants does not appear to be founded on sound experimental evidence. The exact criteria for judging the ability of bone to withstand the



procedure, let alone a method of preoperative assessment of the bone morphology, have yet to be satisfactorily agreed. The functional parameters by which the number and size of these implants may be judged are obscure and probably empirical. However, it is clear from these experiments that the loads imposed on the implants were, in some instances, within.the necessary limits. Jaquette (1913) suggested that the major problem with dental implants would be in the region where the epithelium was penetrated. This study has shown nothing to alter this view. Total exteriorization, suggested by Mack (1968) to be inevitable and to give a physiologically satisfactory reaction as far as subperiosteal implants were concerned, did not appear to occur with wedge-shaped implants. Nevertheless the exact mechanism by which epithelial downgrowth is limited is not clear. It may depend not only on the shape, the physical and chemical characteristics of the neck of the implant and the contour of the intra-oral superstructure, but also on the orientation of the fibrous tissue immediately below the point of penetration. Until a pseudocementum can be developed which could evoke the formation of a tissue analagous to Sharpey's fibres, neither a satisfactory pseudojunctional epithelium nor a well-contoured bony support round an abutment may be possible.

Section of Odontology


Acknowledgments: I am grateful to Professor A H R Rowe for his advice and encouragement with this work, and to the Department of Medical Illustration and the Dental Photographic Department, Guy's Hospital, for assistance with the illustrations. REFERENCES Bodine R L & Mthammed C I (1970) Dental Clinics of North America 14, 145 Brain E B (1966) The Preparation of Decalcified Sections. Thomas, Springfield, III.; pp 62-68 Dahl G S O (1943) Odontologisk tidskrift 51, 440 Gerschoff A & Goldberg N I (1949) Dental Digest 55,490 (1957) Implant Dentures. Pitman, London Jaquette W A (1913) Dental Cosmos 55,438 Johns R B (1975) In: Scientific Foundations of Dentistry. Ed. B Cohen & I R Kramer. Heinemann Medical Books London (in press) Jowsey J, Kelly P J, Riggs B L, Bianco A J jr, Scholz D A & Gershon-Cohen J (1965) Journal of Bone and Joint Surgery 47A, 785 Kalwitter J J & Hulbert S F (1971) Journal of Biomedical Material Research. Symposium No. 2; pp 161-229 Linkow L (1968a) Dental Concepts 11, 3 Linkow L (1968b) Journal ofProsthetic Dentistry 20, 367 Mack A 0 (1958) MDS Thesis, Durham (1968) International Dental Journal 18, 779 Milch R A, Rail D P & Tobie J E (1958) Journal of Bone andJoint Surgery 40A, 897 Milch R A, Tobie J E & Robinson R A (1961) Journal ofHistochemistry and Cytochemistry 9, 261 Natiella J R, Armitage G W, Greene G W jr & Meenaghan M A (1972) Journal of the American Dental Association 84, 1358 Obwegeser H L (1959) Oral Surgery 12, 777 Perren S M, Huggler A, Russenberger M, et al. (1969) Acta odontologica Scandinavica Suppl. 125 Trainin B (1957) Dental Delineator 8, 7 Weiss L (1961) Experimental Cell Research Suppl. 8, p 141

Meeting 19 May 1975 at the Royal College of Surgeons of England, London WC2

Papers Immunological Processes Involving the Oral Mucosa in Lichen Planus by D M Walker MB FDS RCS (Department ofOral Medicine, Dental School, Welsh National School of Medicine, Heath Park, Cardiff, CF4 4XY) The familiar epithelial changes of the lichen planus lesion are invariably accompanied by a striking mononuclear cell infiltrate in the subepithelial zone of the corium. This inflammatory infiltrate, which appears to be composed predominantly of lymphocytes and macrophages at the light microscope level, is present almost at the level of the earliest detectable epithelial change (Thyresson & Moberger 1957). Preliminary investigation of the T and B subpopulations of lymphocytes and macrophages in the infiltrate of mucosal and skin lesions of lichen

planus has been carried out by detecting the membrane receptors of these mononuclear cells. The thymus-derived (T) lymphocytes, important in cellular immunity, can be identified by their property of forming rosettes -with untreated sheep erythrocytes (E) (Lay et al. 1971). It has been claimed that such rosetting can also be used to localize T lymphocytes in frozen sections of human tissue (Silveira et al. 1972). Most bursa-equivalent (B) lymphocytes, precursors of antibody forming cells, have a membrane receptor for the activated C3 component of complement. These complement-receptor-bearing B lymphocytes can be identified in suspension or in tissue sections by their binding complexes of sheep erythrocytes, sensitized with IgM antibody (A) and complement (IgMEAC). The third cell of importance in immune responses, the macrophage, also has membrane receptors for complement but can be distinguished in frozen sections

Experimental studies on dental implants.

I I Volume 69 January 1976 Section of Odontology President B E D Cooke MDS FRCPath Meeting 28 April 1975 Paper Experimental Studies on Dental Imp...
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