Leading Clinical Paper
Dental Implants
Histological comparison
between implants retrieved from
patients with and without
osteoporosis
J. A. Shibli, K. C. D. S. Aguiar, L. Melo, S. d’Avila, E. G. Zeno´bio, M. Faveri, G. Iezzi, A. Piattelli: Histological comparison between implants retrieved from patients with and without osteoporosis. Int. J. Oral Maxillofac. Surg. 2008; 37: 321–327. #2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
J. A. Shibli1, K. C. D. S. Aguiar1, L. Melo1, S. d’Avila1,
E. G. Zeno´ bio2
, M. Faveri1, G. Iezzi3, A. Piattelli3
1Department of Periodontology, Dental
Research Division, Guarulhos University, Guarulhos, Sa˜o Paulo, Brazil;2Department of
Periodontology, Dental Research Division, Pontific Catholic University of Minas Gerais, Brazil;3Department of Oral Medicine and Pathology, Dental School, University of Chieti, Chieti, Italy
Abstract. The aim of this restrospective histologic study was to evaluate the bone-to-implant contact of loaded bone-to-implants retrieved from patients with and without osteoporosis. The evaluated material consisted of 22 threaded, cylindrical, loaded dental implants retrieved from 21 patients: 7 from 7 women with postmenopausal osteoporosis (osteoporosis group) and the remaining 15 from 14 patients without history of osteoporosis or other metabolic diseases (control group). Histologic analysis revealed bone tissue in the threads of the retrieved implants, with variations in the percentage of bone-to-implant contact for the implants retrieved from both groups. The pristine bone was mostly mature bone and/or lamellar and compact, and numerous osteocytes were observed in the lacunae, although areas of woven bone could be distinguished. In some specimens, there were areas of newly formed bone exhibiting different degrees of maturation and remodeling. The mean bone-to-implant contact was 46.00 11.46% and 47.84 14.03% for the osteoporosis group and control group, respectively. The results of this histomorphometric study suggest that osteoporosis may not be a contra-indication for implant placement, at least after osseointegration has been established.
Keywords: dental implants; osteoporosis; hu-man histology; retrieved implants; osseointe-gration.
Accepted for publication 23 November 2007 Available online 11 February 2008
The successful outcome of dental implan-tation is influenced by a number of con-founding factors such as the bone-remodeling response, implant design and topography, clinical protocols, and the patient’s level of physical activity6,19. Bone quality is another important factor, with a higher failure rate having been
observed in implants placed at type IV bone12,14,23.
Osteoporosis is a disease that influences the quality of bone tissue such that it may become susceptible to fracture. Although this disease may have an influence on periodontal attachment loss15, there are no clinical studies that present a clear
association between implant failure and osteoporosis1,24.
Earlier animal studies have described the deleterious effect of osteoporosis on the osseointegration process7,8,22 mainly with regard to trabecular bone volume. It has been demonstrated that resorption and remodeling of the alveolar bone, not only
after extraction of the tooth but also after dental implant placement, are accelerated following experimental ovariectomy8,20.
Concern over dental implants being contraindicated in patients with osteo-porosis is based on the assumption that this metabolic disease affects the jaws in the same way as it affects other parts of the skeleton, such as the lumbar spine, femur, neck and forearm15,25. The mechanism by which osteoporosis acts on peri-implant bone is based on the decrease in both cancellous bone volume and bone-to-implant contact, consequently reducing the bone tissue available to support dental implants22. Osteoporosis is thought to be a result of an altered bone-remodeling pro-cess, i.e. bone-tissue formation decreases while resorptive capacity remains con-stant16.
Osteoporosis may represent a contra-indication or risk factor for osseointegra-tion, but this is still controversial1,2,5,13,24. The objective of this retrospective histo-logic study was to evaluate bone-to-implant contact in loaded implants retrieved from patients with and without osteoporosis.
Materials and Methods
Over a time period of 4 years (March 2003–March 2007), a total of 22 threaded, cylindrical dental implants of different brands were retrieved for different rea-sons: infection, inflammation and bone loss, mechanical failures of implant com-ponents (fracture of implant neck and fracture of abutment screw), and iatro-genic reasons, i.e. paresthesia or hyper-esthesia of lower lip. (Fig. 1)
The patients were referred for prosthetic treatment and/or maintenance care. After diagnosis of failure of the implant restora-tion and/or extensive bone loss (>75% of the length of the implant), these failed implants were scheduled for removal. All the retrieved implants were considered ‘‘problematic’’ according to the local Institutional Review Board (IRB). Implants were not removed if bone loss was <75% of the length, they were work-ing as ‘‘sleepwork-ing’’ implants, or informed consent from the patient to remove the implant was not obtained. The ‘‘non-pro-blematic’’ implants were treated accord-ing to their prognosis: peri-implantitis or kept in the jaws without occlusal function (submerged). Dental implants with clini-cal mobility and/or loss of osseointegra-tion were excluded from this study. Lack of osseointegration was recorded as the slightest mobility tested by rotating and moving every dental implant back and
forward. This study was reviewed by the local IRB. The study met requirements for exemption from IRB review, which included obtaining informed consent from the patients.
Of the 22 implants retrieved from 21 patients (mean age 61.19 7.65 years) included in this study, 7 implants were obtained from 7 women with postmeno-pausal osteoporosis determined by DPX-IQ AP in the lumbar spine and femoral neck. The diagnosis of osteoporosis was established for these patients, based on criteria used by the World Health Orga-nization: T-score <2.5 SD. According to their files, all the patients claimed that the dental implants were placed at the same time as, or after, osteoporosis was diag-nosed by bone densitometry. After their diagnosis of osteoporosis, the patients (according to anamnesis) received a diet and some medications with calcium, but glucocorticosteroids or other immunosup-pressive drugs were not used. Only one patient received treatment with estrogen. The remaining 15 dental implants were obtained from 14 patients without bone
densitometry, clinical history of osteo-porosis or other metabolic diseases that could affect osseointegration healing. Histological Processing and Evaluation
The implants were removed using an internal 4.25-mm-wide trephine, and together with surrounding bone tissues were immediately stored in 10% buffered formalin and processed to obtain thin ground sections with the Precise 1 Auto-mated System (Assing, Rome, Italy). The specimens were dehydrated in an ascend-ing series of alcohol rinses and embedded in a glycol methacrylate resin (Techno-vit17200 VLC, Kulzer, Wehrheim, Ger-many). After polymerization, the specimens were sectioned longitudinally along the major axis of the implant with a high-precision diamond disk at about 150 mm and ground down to about 30 mm. Two slides were obtained for each implant. The slides were stained with basic fuchsin and toluidine blue. Histo-morphometry of bone-to-implant contact Fig. 1. A) Radiographic view of fractured implant abutment screw (arrow) in anterior maxilla in patient with osteoporosis. The other implant presented no osseointegration (*) and was not included in the study. B) Clinical view of the implant (!).
percentage was performed using a light microscope (Laborlux S1, Leitz, Wetzlar, Germany) connected to a high-resolution video camera (3CCD1, JVC KY-F55B, Milan, Italy), and interfaced to a monitor and personal computer (Intel Pentium III 1200 MMX). This optical system was associated with a digitizing pad (Matrix Vision GmbH, Milan, Italy) and a histo-metry software package with image-cap-turing capabilities (Image-Pro Plus14.5, Media Cybernetics Inc., Immagini & Computer Snc, Milan, Italy). The mea-surements14,23of bone-to-implant contact were performed at a magnification of about x160. Mean and standard deviation of the histometric variable values were calculated for both slides of each implant and then for each group.
Results
Information about patient age, gender, time of loading, etc., is presented in Tables 1 and 2. The main reason for removal was mechanical complications for 45% of the 22 histologically evaluated implants. All implants included in this study were clinically stable.
The histologic evaluation revealed bone tissue in the threads of the retrieved implants, with variations in the percentage of bone-to-implant contact for the implants retrieved from both groups (osteoporosis and control). The bone tis-sue surrounding the implants was healthy for both groups (Figs. 2 and 3). The pris-tine bone was mostly mature bone and/or lamellar and compact, and numerous osteocytes were observed in the lacunae, although areas of woven bone could be distinguished. In some specimens, there were areas of newly formed bone exhibit-ing different degrees of maturation and remodeling (Figs. 4 and 5).
Occasionally, osteoblasts were con-nected to the newly formed bone, indicat-ing ongoindicat-ing bone formation. Inside the implant threads, a variable apposition of bone could be found. Some samples
showed a lack of connecting bridges between the thin bone trabeculae and the implant surface. On the sandblasted acid-etched surface implants, a thin layer of bone trabeculae was interposed between the old bone and the implants. The areas close to the surfaces showed a thin layer of dense connective tissue between the bone and the implants. In some sections, blood vessels were detected close to the retrieved implant surface (Fig. 6).
Some sections presented surface debris or particle inclusions in the surrounding tissue close to the bone area. Some sec-tions displayed inflammatory cells (lym-phocytes, macrophages and giant cells) near the implant surface, mainly in the implants retrieved due to peri-implantitis (Figs. 7 and 8). No foreign body reaction was found in the area of bone-to-implant contact, although epithelial downgrowth was observed at the interface. The evalua-tion of bone-to-implant contact revealed Table 1. Patients with osteoporosis: retrieved implant data
Patient Age (years)/ Gender Implant surface topography Time in situ (months) Loading time (months) Implant length diameter (mm) Implant position Indications of implant Bone-to-implant contact (%mean SD) % Length of remaining osseointegration Claimed reason for removal 1 61/f Machined 66 60 10 4.0 Mandible Single tooth 51.25 3.16 100 Mechanical 2 66/f Machined 59 52 10 3.75 Mandible Full denture 50.08 2.01 85 Mechanical 3* 76/f Machined 55 50 13 3.75 Maxilla FDP 27.89 2.22 24 Bone Loss 4 59/f Machined 69 63 10 4.0 Maxilla FDP 37.95 1.25 75 Mechanical 5 63/f SAS 48 43 11 4.0 Mandible Full denture 52.43 1.91 19 Bone Loss 6 61/f Machined 76 70 10 3.75 Mandible FDP 62.51 1.96 100 Mechanical 7 62/f Machined 55 48 10 3.50 Mandible Full denture 39.89 0.65 15 Bone Loss
*
Therapy with estrogen; f: female; SAS: sandblasted acid-etched surface; FPD: fixed partial denture.
Fig. 2. A) Ground section of the retrieved implant from patient with osteoporosis depicted in Fig. 1. B) Ground section of the retrieved implant from a patient without osteoporosis. Acid fuchsin and toluidine blue, original magnification x16.
similar means for the two groups (Fig. 9): 46.00 11.46% and 47.84 14.03% for the osteoporosis group and control group, respectively.
Discussion
The percentages of bone-to-implant con-tact presented in this article were, with few exceptions, similar for both osteoporosis and non-osteoporosis patients. Although some clinical investigations have sug-gested that osteoporosis is not always a risk factor for osseointegration of dental implants, osteoporosis is now regarded as a relative contraindication for oral rehabi-litation using dental implants1,2,5,9,13. Sev-eral studies point to the role of local and systemic factors in the long-term success of dental implants, but less is known about factors affecting the stability of oral implants after the abutment placement process and occlusal load17,24.
In this retrospective histologic study, it was possible to evaluate the bone-to-implant contact in patients classified as type 1 osteoporosis (postmenopausal osteoporosis) according to criteria estab-lished by the World Health Organization. It is important to note that, according to patient anamnesis, the diagnosis of osteo-porosis was made mainly after implant placement. In addition, is important to note that the control group was character-ized according to their anamnesis and clinical evaluation, since these patients have no bone densitometry. However, our retrospective histologic study may offer an idea about the histology of peri-implant bone retrieved from patients with osteoporosis. Some authors2,10, based on several lines of evidence from human and animal studies7,8,20,22, revised their classi-Fig. 3. Presence of cement lines (arrows) and blood vessel (arrowhead) in ground section of
implant retrieved because of mechanical failure from patient without osteoporosis. Acid fuchsin and toluidine blue, original magnification x100.
Table 2. Patients without osteoporosis (control group): retrieved implant data
Patient Age (years)/ Gender Implant surface topography Time in situ (months) Loading time (months) Implant length diameter (mm) Implant position Indications of implant Bone-to-implant contact (%mean SD) % Length of remaining osseointegration Claimed reason for removal 1* 54/f Machined 110 102 13 3.75 Mandible Full denture 21.46 1.45 24 Peri-implantitis 2 45/m SAS 66 60 12 4.0 Mandible FPD 43.75 0.55 100 Mechanical 3 65/f Machined 47 41 13 3.75 Maxilla FPD 49.00 1.56 98 Mechanical 4 53/f Machined 74 68 10 3.75 Maxilla Full denture 37.31 2.01 19 Bone Loss 5 49/f SAS 16 12 10 4.0 Mandible Single tooth 63.33 0.98 100 Iatrogenic 6 66/m Machined 98 90 10 3.75 Mandible FDP 39.63 1.63 18 Bone Loss 7 74/f Machined 105 98 13 3.75 Maxilla Full denture 38.71 1.74 19 Bone Loss 8 59/f Machined 54 47 10 4.0 Mandible FDP 41.01 0.71 64 Mechanical 9* 54/f Machined 81 75 10 3.75 Mandible FDP 46.74 2.10 26 Peri-implantitis 10 66/f TPS 77 70 11 4.0 Maxilla Full denture 39.01 0.56 20 Peri-implantitis 11 59/f Machined 120 112 10 3.75 Maxilla FDP 79.56 1.12 100 Mechanical 12 63/m Machined 96 90 10 3.75 Mandible FDP 46.66 0.06 13 Bone Loss 13 59/m Machined 126 120 13 3.75 Maxilla FDP 58.69 1.74 54 Mechanical 13 59/m Machined 126 120 13 4.0 Maxilla FDP 64.89 1.65 76 Mechanical 14 71/f Machined 87 80 8.0 3.75 Maxilla FDP 47.96 0.98 22 Bone Loss
*Smoker; m: male, f: female; SAS: sandblasted acid-etched surface; TPS: titanium plasma spray; FPD: fixed partial denture.
Fig. 4. Ground section from patient of osteoporosis group depicting mostly compact pristine bone and some osteocytes present in the lacunae. Osteoid layer with osteoblasts (arrows). Acid fuchsin and toluidine blue, original magnification x100.
fication and proposed a unitary model for the pathophysiology of involutional osteo-porosis, because estrogen deficiency is responsible for bone loss in both postme-nopausal women and aging men. Conse-quently, in osteoporosis, the decreased net bone volume, as well as the reduced ability to withstand optimal load may be affected by a combination of modulated cellular activities, influenced by lower levels of estrogen in postmenopausal osteoporo-sis20. Bone-to-implant integration gradu-ally increases, and once it is established the accumulated rate of bone attachment to implants is maintained. Unlike regular bone remodeling that occurs in the trabe-cular area, this phenomenon is not accom-panied by apparent turnover or resorption bone18.
Reports on histometric evaluations of retrieved oral implants of the same design are rare3. Previous studies3,4,11,21 evalu-ated the quality and quantity of peri-implant bone around several retrieved implants with different designs, host con-ditions, implant surfaces and causes of failure. Direct comparison with the pre-sent study is therefore difficult. It must be emphasized that the histometric evalua-tion performed in our study considered only the patient group (control or osteo-porosis) of the retrieved implants without taking into account the implant surface topography or reason for implant removal. The main difference among the retrieved implants was not the host’s con-dition (osteoporosis or non-osteoporosis) but the presence of an inflammatory infil-trate in the peri-implant tissue, as well as the presence of bacteria on the coronal part of the retrieved implants, because of peri-implantitis. Another important aspect was the time of loading. All implants were loaded at least 1 year before their removal, and they were stable at the time of removal. This condition could explain the higher mean bone-to-implant contact when compared with previous studies3,21. In some clinical investigations, factors such as patient gender and age were not correlated with long-term failures5,12. This may suggest that once bone-to-implant integration is established, there may be not a significant number of clinical fail-ures1. The presence of the dental implant may create a distinct and unique cellular environment, and a scaffold for bone-mar-row osteogenic cells to form new bone tissue6, mainly in the earlier stages, depending on the microstructure of the implant surface topography6,14,23, loading time and force17.
Implant-supported prostheses in the jawbone are affected not only by systemic Fig. 5. Ground section of implant from osteoporosis patient. Presence of cavity with
multi-nuclear giant cell (arrows) in contact with implant surface. Acid fuchsin and toluidine blue, original magnification x100.
Fig. 6. Ground section of control group depicting close contact between mature compact bone and implant surface. Note the presence of nerve bundles and blood vessels. Acid fuchsin and toluidine blue, original magnification x100.
Fig. 7. Presence of bacteria in implant soft tissue in implant retrieved because of peri-implantitis. Acid fuchsin and toluidine blue, original magnification x100.
factors but also by many local factors, such as the periodontal condition of the remaining teeth, number and distribution of dental implants in the arch, occlusion and bite forces. There may be some dif-ferences in bone healing and remodeling between the long bones and the jawbones after dental implant placement22,24. According to several investigations, in patients with postmenopausal osteoporo-sis the rate of trabecular bone loss is greater, despite the rate of cortical bone loss being only slightly above normal.
In conclusion, the results of this retro-spective histomorphometric study suggest that osteoporosis may not present a contra-indication for implant placement, at least once osseointegration has been estab-lished. These results should be considered with caution, and further prospective stu-dies are needed with a larger sample of patients with disorders such as postmeno-pausal and/or senile osteoporosis.
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Address:
Prof. Jamil Awad Shibli Centro de Po´s-graduac¸a˜o Pesquisa e Extensa˜o – CEPPE Universidade Guarulhos-UnG R. Dr. Nilo Pec¸anha 81 – Pre´dio U – 68 Andar 07011-040 Guarulhos SP Brazil Fax: +55 11 64641758 E-mail:jashibli@yahoo.com
