The socket-shield technique: a proof-of-principle report

 

Markus B. Hu ̈rzeler1,2, Otto Zuhr1,

3
Peter Schupbach , Stephan F.

Rebele1, Notis Emmanouilidis4 and Stefan Fickl4,5

 

 

Hu ̈rzeler MB, Zuhr O, Schupbach P, Rebele SF, Emmanouilidis N, Fickl S. The socket- shield technique: a proof-of-principle report. J Clin Periodontol 2010; 37: 855–862. doi: 10.1111/j.1600-051X.2010.01595.x.

 

 

 

Aim: Clinical studies have suggested that retaining roots of hopeless teeth may avoid tissue alterations after tooth extraction.

Therefore, the objective of this proof-of- principle experiment was to histologically assess a partial root retention (socket-shield technique) in combination with immediate implant placement.

 

 

Material and Methods:

In one beagle dog, the third and fourth mandibular pre-molar were hemisected and the buccal fragment of the distal root was retained approximately 1 mm coronal to the buccal bone plate.

Following application of enamel matrix derivate,

a titanium implant was placed lingual to that tooth fragment

either with or without contact to the buccal tooth fragment

and a healing abutment was connected.

Four months after implant placement, histological evaluation, and backscatter scanning electron microscopy were performed.

Results: All four implants were osseointegrated without any histologic inflammatory reaction and the tooth fragment was devoid of any resorptional processes.

On the buccal side, the tooth fragment was attached to the buccal bone plate by a physiologic periodontal ligament.

On the lingual side of the fragment, newly formed cementum could be detected. In the areas where the implant was placed into the fragment, newly formed cementum was demonstrated directly on the implant surface.

Key words: extraction socket; immediate implant placement; tooth-retention

 

 

 

Numerous publications have verified that tooth extraction is followed by dimensional changes of the alveolar ridge contour (Amler et al. 1960, Pie- trokovski & Massler 1967, Schropp et al. 2003, Arau ́jo & Lindhe 2005, Fickl et al. 2008b). The resorption of the alveolar ridge is more pronounced on the buccal than on the lingual aspect of the extraction socket (Pietrokovski & Massler 1967, Arau ́ jo & Lindhe 2005).

 

 

In order to overcome the negative consequences of tooth extraction, various treatment approaches have been advocated and described in the literature, such as:

immediate implants (Botticelli et al. 2004, Araújo et al. 2005),

graft materials (Carmagnola et al. 2003, Nevins et al. 2006, Araújo et al. 2008, Fickl et al. 2008a, Araújo et al. 2009)

and/or barrier membranes (Lekovic et al. 1997, Leko- vic et al. 1998)

 

As a conclusion, the majority of the studies show that socket preservation is a suitable technique for socket augmentation with the ability to maintain the ridge dimension to a certain amount (Araújo et al. 2008, Fickl et al. 2008a, Araújo et al. 2009).

However, a complete preservation and/or entire regeneration of the extraction socket have not been documented yet.

 

 

The marked alterations after tooth extraction appear to be attributable to the loss of periodontal ligament and the consecutive trauma in particular at the buccal bone plate (Araújo & Lindhe 2005). Thus, it can be assumed that root retention may have an influence on the occurring resorption process.

 

Clinical studies have tested the hypothesis that root retention, either of vital or pulpless teeth, may be able to avoid tissue alterations after tooth extraction. Filippi et al. (2001) showed in a case report that decoronation of an ankylosed tooth preserved the alveolar bone before implant placement.

 

Few studies have demonstrated that the preservation of decoronated roots in the alveolar process not only helps main- taining existing bone volume but also enables vertical bone growth, which can be observed coronally to the decoronated root (Malmgren et al. 1984, Malmgren et al. 1994, Andersson et al. 2003). Bjo ̈rn (1963) confirmed regeneration of alveolar bone around endodontically treated teeth that were submerged and covered by a surgical flap. Reames et al. (1975) demonstrated in an animal study that even though epithelium commonly occurred over the amputation sites of submerged teeth, bone formation coronal to the submerged roots was evident.

 

O’Neal et al. (1978) showed histological and radiographic evidence that new cementum and connective tissue will form over the coronal surface of submerged roots separating the dentin from the new bone. Conclusively, histological and radiographic evidences suggest few inflammatory changes and bone apposi- tion around roots that had been sub- merged for alveolar bone preservation. Bowers et al. (1989) submerged vital teeth with infrabony defects in nine patients and created notches at regions on the root that had been covered with dental calculus. After 6 months, no root resorption, ankylosis, or pulp death was observed.

 

Salama et al. (2007) reported that the Root Submergence Technique (RST) maintains the natural attachment appa- ratus of the tooth in the pontic site, which in turn allows for complete pre- servation of the alveolar bone frame and assists in the creation of an aesthetic result in adjacent multiple-tooth-repla- cement cases.

 

Davarpanah & Szmukler-Moncler (2009) reported implant placement in contact with ankylosed root fragments in a five-case-report study without any specific pathological sign after a period of 12–42 months of loading.

 

No study yet has evaluated partial root retention around dental implants. Thus, the goal of this proof-of-principle experiment in conjunction with a case report was to histologically assess and clinically demonstrate the effect of buc- cal root retention (socket-shield techni- que) in combination with immediate implant placement.

 

 

One beagle dog (1 year old and weighting 17.5 kg) was used for this experiment. Supragingival scaling was performed 5 days before tooth extraction and implant placement.

 

In both quadrants of the mandible, the third and fourth pre- molars (3P3 and 4P4) were used as experimental sites.

 

The third and fourth mandibular pre-molars were hemisected using a fissure bur. Consecutively, a coarse-grained diamond bur was used to decoronate the distal aspect of the pre-molar. After performing the osteotomy drills for the dental implant on the lingual part of the root, residual tooth fragments were completely removed on the lin- gual, distal, and mesial region of the extraction socket (Fig. 1).

Consecutively, enamel matrix derivate (Emdogains , Straumann, Basel, Swit- zerland) was administered on the internal aspect of the fragment.

The buccal fragment of the root was retained approximately 1 mm coronal to the buccal bone plate.

 

The implant (SPIs ELEMENT 4 11 mm, Thommen Medical, Walden- burg, Switzerland) was placed accord- ing to the manufacturer’s recommenda- tion and was situated at the height of the buccal root segment (Fig. 2).

Randomly, two out of four implants were placed intentionally in direct contact with the buccal root fragment.

Healing abutments of 4 mm in height were connected (Fig. 3).

The animal was terminated 4 months after implant placement.

 

 

 

The bucco-lingual overview illustrated the presence of a tooth fragment located buccally from the implant (Fig. 4).

 

The tooth fragment consisted of a small portion of enamel and an up to 0.5mm- wide piece of root dentin.

On its buccal side, the tooth fragment was still attached to the buccal bone plate by a physiologic periodontal ligament.

Towards the implant, a small, up to 0.5mm-wide gap, filled with connective tissue was interposed between the tooth fragment and the implant.

The implant was osseointegrated into the alveolar bone on the lingual side.

The height of the alveolar bone crest was identical on the buccal and on lingual side.

The peri- implant soft tissue revealed a physiologic junctional epithelium and was free of any inflammatory reaction.

A higher magnification of the coronal part of the tooth fragment revealed buccally a physiologic junctional epi- thelium terminating at the cemento- enamel junction (supporting information Fig. S1).

 

The uppermost end of the tooth fragment was in contact with the junc- tional epithelium tapering down along the implant.

Initiating from this contact point, a thin layer of junctional epithe- lium was present on the internal surfaces of the tooth fragment and tapered down in the apical direction (Fig. S2).

Apically to the latter, the dentin surface was covered by a thin layer of newly formed cementum (Fig. S2) The thickness of the cementum layer increased continuously in the apical direction (Fig. 5).

 

The most coronal part of the new cementum was an acellular type of cementum, which was apically continuous with cellular cementum (Fig. 5).

At a higher magnification, the acellular cementum showed ongoing formation of cementum by the presence of a cementoid and cementoblasts (Fig. 6) and was characterized by the insertion of collagen fibre bundles anchored in cementum (Fig. S3).

Cellular cementum was deposited in multiple layers (Fig. 7).

The connective tissue interposed between the newly formed cementum and the implant surface was healthy and was adherent to the implant surface (Fig. 7). Occasionally, new formation of woven bone was observed on the latter (Fig. 7).

The apical end of the tooth fragment showed no resorption processes.

The surface also was partially covered by a thin layer of newly formed cementum (Fig. S4).

 

The alveolar bone crest was free of any resorption processes.

In contrary, new formation of woven bone was observed (Fig. S2).

 

 

 

 

 

 

The coronal part of the tooth fragment was separated by connective tissue interposed between tooth fragment and implant (Fig. 9).

 

 

 

 

 

 

Again, the border between the apical end of junctional epithelium and the newly formed acellular cementum was clearly visible (Fig. S5).

 

The more apical portion of the tooth fragment was in direct contact with the tips of the implant threads and covered by a cellular type of cementum (Figs 10, 11; Fig S6).

The areas between the threads were partially filled with an amorphous mineralized tissue and connective tissue (Figs 10, S6).

In some areas, formation of new cementum via cementoblasts and a cementoid occurred directly on and along the implant surface (Fig. 11).

Higher magnifications of the tips of the implant threads demonstrated their integration in the newly formed cementum interposed between dentin and the implant (Fig. 11).

Higher magnifications showed the intimate contact, without any fibrous tissues inter- posed, between the new cementum and the implant surface (Fig. 12).

The buccal side of the tooth fragment revealed a normal and intact periodontal ligament (Fig. S6).

No signs of bone resorption were observed at the alveolar bone crest (Fig. S8).

 

 

 

 

 

 

 

 

 

 

Case Report

A 45-year-old patient presented with a non-contributory medical history, requesting replacement of tooth #21 due to a vertical root fracture (Fig. 13).

Tooth #21 was decoronated with a coarse-grained diamond approximately 1 mm apical to the gingival margin (Fig. S9).

Consecutively, the osteotomy drills were performed through the lingual aspect of the root. Then, all root fragments were removed on the lingual, mesial and distal aspect, retaining only the buccal portion of the root (Fig. 14).

Following application of enamel matrix derivate (Emdogains , Straumann), the implant (SPIsELEMENT, Thommen Medical 4 13 mm) was inserted and positioned slightly apical to the preserved root fragment (Fig. 15).

A screw-retained provisional was fabricated and hand tightened onto the implant (Fig. S10). Care was taken to remove all centric and eccentric functional contacts from the provisional crown. A soft diet was recommended for the duration of the implant- healing phase. The patient was advised against functioning or activities to the implant site.

The gingival architecture around the implant was well preserved after 6 months (Fig. 16). The final impressions were made and the definitive restoration consisted of a full-ceramic abutment and a full-ceramic crown (Figs 17, 18).

 

Scientific evidence has shown that immediate implant placement is able to predictably achieve osseointegration (den Hartog et al. 2008), but does not appear to have an influence on the biological response of the extraction socket (Botticelli et al. 2004, Araújo et al. 2005, Vignoletti et al. 2009a, b).

 

The technique of retaining roots to avoid alveolar bone remodelling was adopted from dental traumatology, where Malmgren et al. (1984) suggested the decoronation technique of ankylosed teeth. Decoronation may be considered a type of guided bone regeneration due to the fact that the remaining residual root will undergo a resorptive process by osteoclasts from the adjacent bone marrow and gradually be replaced by bone.

 

 

Multiple experimental and clinical studies have shown, that the decoronation of ankylosed teeth predictably preserves the alveolar ridge contour (Malmgren 2000, Filippi et al. 2001, Malmgren & Malmgren 2002, Cohenca & Stabholz 2007, Sapir & Shapira 2008).

 

 

However, the results of the present study illustrate that a non-ankylosed tooth fragment does not appear to undergo resorptional processes.

 

However, in this study – contrary to the above-cited studies – only the buccal part of the root and its supra-periosteal attachment were preserved and furthermore no primary closure was obtained.

 

 

The major findings of the histological analysis were that:

the internal aspect of the root was covered with new cementum and new periodontal attachment.

In addition, in areas where the implant has been placed into the root fragment, cementum could be detected on the implant surface. This can be seen in accordance with the study conducted by Buser et al. (1990) concluding that in areas where the implant has been placed in close relationship to the root fragment, the examination of the undecalcified sections revealed a cementum layer on the implant surface with inserting collagen fibres

The fact that a new periodontal attachment could be detected on the inside of the root frag- ment may be explanative by the use of enamel matrix derivate, which plays a major role in the development of perio- dontal tissues and show effectiveness in the regeneration of the periodontium (Hammarstrom 1997, Heijl et al. 1997, Sculean et al. 2000).

Enamel matrix derivative have also been documented to prevent epithelial proliferation and to have an antimirobial capacity (Bos- shardt 2008).

In order, to prevent epithe- lial down-growth along the retained root and to preserve the characteristics of the root fragment, enamel matrix derivative was used as an adjunct to immediate implant placement.

On the other hand, Nyman et al. (1982) has shown that exclusion of epithelial cells leads to periodontal regeneration due to cells from the perio- dontal ligament. Within the limits of this experiment, it may be speculated that the blood clot between implant and root may have prevented the epithelium from colonizing the root surface. Amler et al. (1960) and Cardaropoli et al. (2003) have histologically demonstrated that it takes approximately 4 weeks after tooth extraction to cover the extraction socket with epithelium.

 

 

 

Furthermore, the retained root portion appears to preserve its characteristics with particular respect to its periodontal ligament and the supra-peri- osteal attachment.

 

 

 

the retained root portion appears to preserve its charac- teristics with particular respect to its periodontal ligament and the supra-peri- osteal attachment.

Reviews conclude that submerging teeth appear to be a viable and safe technique to preserve alveolar bone (Casey & Lauciello 1980, Dugan et al. 1981).

 

However, in this study – contrary to the above-cited studies – only the buccal part of the root and its supra-periosteal attachment were preserved and further- more no primary closure was obtained.

 

It may be assumed that the same process occurs between the implant and the retained tooth fragment. As the blood clot prevents the epithelium from growing along the internal root surface, it appears that cells from the remaining periodontal liga- ment are capable of colonizing the root surface and regenerate new periodontal attachment.

 

 

 

 

 

Clinical Relevance

Scientific rationale for this study: The goal of this proof-of-principle experi- ment was to histologically assess the biological response following partial tooth retention in combination with

immediate implant placement.

when placed in direct contact to it.

Principal findings: The retained root was devoid of any inflammatory or resorptive reactions. A newly formed root cementum could be detected on the internal part of the root fragment and on top of the implant surface,

Practical implications: Retaining parts of the root is a viable technique to achieve osseointegration. It may also have the potential to preserve the buccal bone plate.

 

 

 

References

Amler, M., Johnson, P. & Salsman, I. (1960) Histologic and histochemical investigation of human alveolar socket healing in undisturbed extraction wounds. Journal of American Dental Association 61, 46–48.

Andersson, L., Emami-Kristiansen, Z. & Hogstrom, J. (2003) Single-tooth implant treatment in the ante- rior region of the maxilla for treatment of tooth loss after trauma: a retrospective clinical and interview study. Dental Traumatology 19, 126–131.

Arau ́jo, M., Linder, E. & Lindhe, J. (2009) Effect of a xenograft on early bone formation in extraction sockets: an experimental study in dog. Clinical Oral Implants Research 20, 1–6.

Arau ́jo, M., Linder, E., Wennstro ̈m, J. & Lindhe, J. (2008) The influence of Bio-Oss collagen on heal- ing of an extraction socket: an experimental study in the dog. International Journal of Periodontics & Restorative Dentistry 28, 123–135.

Arau ́jo, M., Sukekava, F., Wennstrom, J. & Lindhe, J. (2005) Ridge alterations following implant place- ment in fresh extraction sockets: an experimental study in the dog. Journal of Clinical Perio- dontology 32, 645–652.

Arau ́jo, M. G. & Lindhe, J. (2005) Dimensional ridge alterations following tooth extraction. An experi- mental study in the dog. Journal of Clinical Perio- dontology 32, 212–218.

Bjo ̈rn, H. (1963) Free transplantation of gingival propria. Sven Tandlak Tidskr 22: 684.

Bosshardt, D. D. (2008) Biological mediators and periodontal regeneration: a review of enamel matrix proteins at the cellular and molecular levels. Jour- nal of Clinical Periodontology 35, 87–105.

Botticelli, D., Berglundh, T. & Lindhe, J. (2004) Hard- tissue alterations following immediate implant pla- cement in extraction sites. Journal of Clinical Periodontology 31, 820–828.

Bowers, G., Chadroff, B. & Carnevale, R. (1989) Histologic evaluation of new attachment apparatus formation in humans. Part II. Journal of Perio- dontology 60, 675–682.

Buser, D., Warrer, K. & Karring, T. (1990) Formation of a periodontal ligament around titanium implants. Journal of Periodontology 61, 597–601.

Cardaropoli, G., Arau ́jo, M. & Lindhe, J. (2003) Dynamics of bone tissue formation in tooth extrac- tion sites. An experimental study in dogs. Journal of Clinical Periodontology 30, 809–818.

Carmagnola, D., Adriaens, P. & Berglundh, T. (2003) Healing of human extraction sockets filled with Bio-Oss. Clinical Oral Implants Research 14, 137–143.

Casey, D. M. & Lauciello, F. R. (1980) A review of the submerged-root concept. The Journal of Prosthetic Dentistry 43, 128–132.

Cohenca, N. & Stabholz, A. (2007) Decoronation – a conservative method to treat ankylosed teeth for preservation of alveolar ridge prior to perma- nent prosthetic reconstruction: literature review and case presentation. Dental Traumatology 23, 87–94.

Davarpanah, M. & Szmukler-Moncler, S. (2009) Unconventional implant treatment I. Implant place- ment in contact with ankylosed root fragments. A

r 2010 John Wiley & Sons A/S

series of five case reports. Clinical Oral Implants

Research 20, 851–856.
den Hartog, L., Slater, J. J., Vissink, A., Meijer, H. J. &

Raghoebar, G. M. (2008) Treatment outcome of immediate, early and conventional single-tooth implants in the aesthetic zone: a systematic review to survival, bone level, soft-tissue, aesthetics and patient satisfaction. Journal of Clinical Perio- dontology 35, 1073–1086.

Donath, K. & Breuner, G. (1982) A method for the study of undecalcified bones and teeth with attached soft tissues. The Sage-Schliff (sawing and grinding) technique. Journal of Oral Pathology 11, 318–326.

Dugan, D. J., Getz, J. B. & Epker, B. N. (1981) Root banking to preserve alveolar bone: a review and clinical recommendation. Journal of American Dental Association 103, 737–743.

Fickl, S., Zuhr, O., Wachtel, H., Bolz, W. & Huerzeler, M. (2008a) Hard tissue alterations after various socket preservation techniques – an experimental study in the beagle dog. Clinical Oral Implants Research 19, 1111–1118.

Fickl, S., Zuhr, O., Wachtel, H., Stappert, C., Stein, J. & Hurzeler, M. B. (2008b) Dimensional changes of the alveolar ridge contour after different socket preservation techniques. Journal of Clinical Perio- dontology 35, 906–913.

Filippi, A., Pohl, Y. & von Arx, T. (2001) Decorona- tion of an ankylosed tooth for preservation of alveolar bone prior to implant placement. Dental Traumatology 17, 93–95.

Hammarstrom, L. (1997) Enamel matrix, cementum development and regeneration. Journal of Clinical Periodontology 24, 658–668.

Heijl, L., Heden, G., Sva ̈ rdstro ̈ m, G. & O ̈ stgren, A. (1997) Enamel matrix derivative (EMDOGAIN) in the treatment of intrabony defects. Journal of Clinical Periodontology 24, 705–714.

Lekovic, V., Carmargo, P., Klokkevold, P., Weinlaen- der, M., Kenney, E., Dimitrijevic, B. & Nedic, M. (1998) Preservation of alveolar bone in extraction sockets using bioabsorbable mebranes. Journal of Periodontology 69, 1044–1049.

Lekovic, V., Kenney, E., Weinlaender, M., Han, T., Klokkevold, P., Nedic, M. & Orsini, M. (1997) A bone regenerative approach to alveolar ridge main- tenance following tooth extractions. Report of 10 cases. Journal of Periodontology 68, 563–570.

Malmgren, B. (2000) Decoronation: how, why, and when? Journal of the California Association 28, 846–854.

Malmgren, B., Cvek, M., Lundberg, M. & Frykholm, A. (1984) Surgical treatment of ankylosed and infrapositioned reimplanted incisors in adolescents. Scandinavian Journal of Dental Research 92, 391–399.

Malmgren, B. & Malmgren, O. (2002) Rate of infra- position of reimplanted ankylosed incisors related to age and growth in children and adolescents. Dental Traumatology 18, 28–36.

Malmgren, O., Malmgren, B. & Goldson, L. (1994)

Orthodontic Management of the Traumatized Den-

tition, pp. 587–633. Copenhagen, Munksgaard. Nevins, M., Camelo, M., De Paoli, S., Friedland, B., Schenk, R. K., Parma-Benfenati, S., Simion, M., Tinti, C. & Wagenberg, B. (2006) A study of the fate of the buccal wall of extraction sockets of teeth with prominent roots. International Journal of

Periodontics and Restorative Dentistry 26, 19–29. Nyman, S., Lindhe, J., Karring, T. & Rylander, H. (1982) New attachment following surgical treat- ment of human periodontal disease. Journal of

Clinical Periodontology 9, 290–296.
O’Neal, R. B., Gound, T., Levin, M. P. & del Rio, C.

E. (1978) Submergence of roots for alveolar bone preservation. I. Endodontically treated roots. Oral

Surgery, Oral Medicine and Oral Pathology 45,

803–810.
Pietrokovski, J. & Massler, M. (1967) Alveolar ridge

resorption following tooth extraction. Journal of

Prosthetic Dentistry 17, 21–27.
Reames, R. L., Nickel, J. S., Patterson, S. S., Boone,

M. & el-Kafrawy, A. H. (1975) Clinical, radio- graphic, and histological study of endodontically treated retained roots to preserve alveolar bone. Journal of Endodontics 1, 367–373.

Salama, M., Ishikawa, I., Salama, H., Funato, A. & Garber, D. A. (2007) Advantages of the Root Submergence technique for Pontic Site Develop- ment in esthetic implant therapy. International Journal of Periodontics & Restorative Dentistry 27, 521–527.

Sapir, S. & Shapira, J. (2008) Decoronation for the management of an ankylosed young permanent tooth. Dental Traumatology 24, 131–135.

Schropp, L., Wenzel, A., Kostopoulos, L. & Karring, T. (2003) Bone healing and soft tissue contour changes following single-tooth extraction: a clinical and radiographic 12-month prospective study. International Journal of Periodontics & Restorative Dentistry 23, 313–323.

Sculean, A., Chiantella, G. C., Windisch, P. & Donos, N. (2000) Clinical and histologic evaluation of human intrabony defects treated with an enamel matrix protein derivative (Emdogain). International Journal of Periodontics & Restorative Dentistry 20, 374–381.

Vignoletti, F., de Sanctis, M., Berglundh, T., Abra- hamsson, I. & Sanz, M. (2009a) Early healing of implants placed into fresh extraction sockets: an experimental study in the beagle dog. II: ridge alterations. Journal of Clinical Periodontology 36, 688–697.

Vignoletti, F., Johansson, C., Albrektsson, T., De Sanctis, M., San Roman, F. & Sanz, M. (2009b) Early healing of implants placed into fresh extrac- tion sockets: an experimental study in the beagle dog. De novo bone formation. Journal of Clinical Periodontology 36, 265–277.