Evaluation of Peri-Implant Bone Response in Implants Retrieved for Fracture After More Than 20 Years of Loading: A Case Series

Analysis of human retrieved dental implants is a very useful tool in the evaluation of implant success and failure.¹  These retrieved specimens are extremely valuable because they contain answers to the biological reaction from the host and the effects produced by the presence of the implant on bone remodeling.¹  The studies on retrieved implants have helped to produce new designs in the macro- and microstructure of the implant surface, trying to improve the response of the peri-implant bone.²  As far as osseointegration is concerned, retrieved implants play a relevant role in the long-term evaluation of implants subjected to functional loading.³  Clinical human studies are invaluable for many reasons, but they cannot provide information about the nature of the bone-implant interface.^4,5  More human histological data are needed from samples of long-term implant service.⁶  Even single case reports are extremely important due to the scarcity of long-term human data.⁴  Human specimens, moreover, are extremely important in validating the results obtained from in vitro or animal experimental studies, and the performance of the bone-implant interface over time must be evaluated.⁷ 

Two main problems are related to the evaluation of retrieved human implants: (1) the frequent lack of relevant clinical information, and (2) the problems that can be encountered during implant retrieval, as in some cases where only small portions of peri-implant bone are present and can be evaluated.⁸  Moreover, the quality of the material may vary widely between specimens.⁸  These limitations notwithstanding, often it will be possible to draw some conclusions of clinical importance from the retrieved implants.⁹ 

Implant effectiveness is largely dependent on biological stability and integration between the bone and the implant.⁹  Long-term maintenance and success of an implant is related to a continuous remodeling at the interface to avoid bone fatigue fractures and to replace bone that may have sustained microfractures as a result of cyclic loading.^9–11 

The aim of the present study was a histological and histomorphometrical case series of the peri-implant bone responses in implants retrieved for fracture after more than 20 years' loading period.

The archives of the Implant Retrieval Center of the Department of Medical, Oral and Biotechnological Sciences of the University of Chieti-Pescara, Italy were searched for human dental implants retrieved for fracture after a loading period of more than 20 years (Figures 1 and 2). A total of 5 implants (Dispo, Milano, Italy) inserted in 5 patients were found: 2 had been retrieved after 20 years, 1 after 22 years, 1 after 25 years, and 1 after 27 years. The surface of all these implants was obtained by a sandblasting with 150 microns particles of Al₂O₃, followed by acid-etching with 20% nitric acid for 30 minutes. The implants were then washed under oxygen peroxide, and dried at 100°C temperature. The macrodesign of the implants was characterized by the presence of large threads with a 2-mm distance between the threads. All the implants had been loaded; none had been immediately loaded. All implants had been retrieved for a fracture of the body of the implant. All the patients agreed that their specimens could be used for scientific purposes, and they signed a written informed consent form. In 3 cases, the implants supported partial fixed bridges, while in 2 cases there was a mandibular overdenture supported by 2 implants. Four implants were located in the mandible, and 1 in the maxilla. All these implants were stable before retrieval. All the implants had been retrieved with a 5-mm trephine bur.

All the specimens were washed in saline solution and immediately fixed in 4% para-formaldehyde and 0.1% glutaraldehyde in 0.15 M cacodylate buffer at 4°C and pH 7.4, to be processed for histology. The specimens were processed to obtain thin ground sections with the Precise 1 Automated System (Assing, Rome, Italy).¹²  The specimens were dehydrated in an ascending series of alcohol rinses and embedded in a glycolmethacrylate resin (Technovit 7200 VLC, Kulzer, Wehrheim, Germany). After polymerization, the specimens were sectioned along their longitudinal axis at about 150 μm with a high-precision diamond disk (Micromet, Ceretolo di Casalecchio di Reno [Bo], Italy), and were ground down to about 30 μm with a specially designed grinding machine. A total of 2 slides were obtained for each specimen. The slides were stained with acid fuchsin and toluidine blue. The slides were observed in normal transmitted light under a Leitz Laborlux microscope (Leitz, Wetzlar, Germany) and polarized-light microscopy (Leitz, Wetzlar, Germany).

Histomorphometry of the percentages of bone-implant contact percentages was carried out on all the surface available of the fractured implants using a light microscope (Laborlux S, Leitz, Wetzlar, Germany) connected to a high resolution video camera (3CCD, JVC KY-F55B, JVC, Yokohama, Japan) and interfaced to a monitor and PC (Intel Pentium III 1200 MMX, Intel, Santa Clara, Calif). This optical system was associated with a digitizing pad (Matrix Vision GmbH, Oppenweiler, Germany) and a histometry software package with image capturing capabilities (Image-Pro Plus 4.5, Media Cybernetics Inc., Immagini & Computer Snc Milano, Italy).

Compact, mature bone in close contact with the implant surface was observed in all specimens, with no gaps or connective tissue at the interface (Figures 3 through 5). In all implants, the peri-implant bone started below the fracture line of the implant. Small- or medium-sized marrow spaces were present with no inflammatory infiltrate. Around the implants, bone was present in different maturation stages. Many remodeling areas and secondary osteons were present (Figure 6). Primarily newly formed bone was observed in proximity of the implant surface, while mature compact bone with many remodeling areas and cement lines were detected in areas distant from the implant. In some areas, a rim of osteoblasts depositing osteoid matrix directly on the implant surface was observed (Figures 7 and 8). In some areas of the peri-implant bone, it was possible to see a hemi-osteon in direct contact with the implant surface (Figure 9). In the apical portion of some of the implants, there was a lesser quantity of osteoblasts with a more compact bone and many cement lines. In some portion of the interface, it was possible to observe a small gap, an artifact produced during the implant retrieval. Many small blood vessels were present in the marrow spaces (Figures 9 and 10). In the most coronal portion of one implant, it was possible to detect the presence of connective tissue adhering to the implant surface with few fibroblasts and, in some fields, a moderate inflammatory infiltrate. The results of the histomorphometric evaluation of bone-to-implant contact were summarized in the Table.

Few papers are present in the literature discussing histology of human implants retrieved after a long period of function.^13–28  These studies, reporting human retrieved implants after in vivo functional loading periods ranging from months to decades, have usually shown an intimate contact between bone and implant surface. Human retrieval analysis is one of the most valuable tools for evaluation of implant successes or failures,¹  due to the fact that clinical studies cannot provide information regarding BIC.⁴  The retrieved specimens contain important information regarding the biological reaction from the host and the effects of the implant presence on bone remodeling.¹ 

In the present case series, histology and histomorphometry showed that even after many years of function, all implants presented more than adequate bone-to-implant contact, ranging from 37% to 76%.^{1,4,23,29–31}  All implants were clinically stable and were not mobile before retrieval. All implants appeared to be very well integrated in the peri-implant bone. Haversian canals were frequently seen in close proximity to the implant-bone interface. Many remodeling areas and cement lines—lines visible in microscopic examination of bone, marking the boundary of an osteon (haversian system)—were present between osteons at different maturation stages. Many primary and secondary osteons were also present; some of these osteons were seen abutting the implant surface. No signs of epithelial migration were present. No foreign body reactions or osteolytic lesions were present at the interface. These findings suggested that bone immediately adjacent to these implants maintained structure and biomechanical properties after about 20 years in vivo.⁹ 

It is widely accepted that mechanical stimuli alter the mass and the structure of bone.¹³  The load induces strains in the bone that affects the remodeling processes to adapt the bone.¹³ In a recent study using a very sophisticated technique called nanoindentation, Baldassarri et al found that both the elastic modulus and the hardness of the peri-implant bone showed increased values as time in vivo progressed.²⁹  These authors found that human cortical bone presented an increase in elastic modulus and hardness during the first 5 years, and presented stable mechanical properties thereafter. These results suggest that bone remodeling around the implants had achieved full maturity only after 5 years.²⁹  Implant effectiveness is largely dependent upon biological stability and integration between bone and implant.⁹  Endosseous implants may function over a wide range of degrees of osseointegration.¹ 

In conclusion, the present case series that histologically and histomorphometrically characterized the bone-implant environment after several years of function helped to formulate the following:

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  Analysis of retrieved dental implants may help to investigate the possible reasons for the implant removal;

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  The condition of the retrieved implants and the surrounding peri-implant bone can be thoroughly evaluated;

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  The histological and histomorphometrical analysis could produce an evaluation of the biocompatibility of the implants over the long term;

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  There is always a more than adequate bone-to-implant contact percentage in fractured implants;

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  The bone is always present below the fracture line;^32–34 

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  Many remodeling areas of bone were present and these were probably critical for the long-term success of the implants.

This work was partially supported by the Ministry of Education, University, Research (M.I.U.R.), Rome, Italy.