Nigerian Journal of Clinical Practice

: 2020  |  Volume : 23  |  Issue : 2  |  Page : 147--153

Evaluation of long-term dental implant success and marginal bone loss in postmenopausal women

VE Toy, MO Uslu 
 Department of Periodontology, Faculty of Dentistry, Inonu University, Malatya, Turkey

Correspondence Address:
Dr. M O Uslu
Department of Periodontology, Faculty of Dentistry, Inonu University, Malatya


Aim: The aim of this study was to examine long-term implant success and marginal bone loss (MBL) of dental implants in postmenopausal women with osteoporosis/osteopenia. Materials and Methods: Postmenopausal women who underwent dental implant treatment at least 3 years ago were divided into two study groups [Test (osteoporosis/osteopenia) Group and Control Group] according to bone mineral density (BMD) measurements. Besides clinical periodontal and radiographic examinations, any implant failures were also recorded. Results: A total of 52 patients with a mean age of 59.51 ± 5.66 years (Test Group; 26 patients, mean age: 60.61; Control Group; 26 patients, mean age: 58.42) were included in the study. Implant survival rates were 96.2% and 100% with a mean follow-up 60.84 ± 22.13 and 60.07 ± 20.93 months in Test and Control Groups, respectively (P > 0.05). While peri-implant PI (plaque index) and PD (probing depth) were not different between the groups, BoP (bleeding on probing) was significantly higher in Test Group (P = 0,026). Although MBL in Test Group was higher than Control Group (0.82 ± 0,63 mm and 0.44 ± 0,33 mm respectively), the difference was not found statistically significant (P = 0.069). Conclusion: Within the limits of this retrospective study, it can be concluded that postmenopausal osteoporosis/osteopenia does not affect MBL and long-term implant success. The findings suggest that dental implant therapy is a reliable treatment modality in these patients to improve the quality of life by increasing function and aesthetics.

How to cite this article:
Toy V E, Uslu M O. Evaluation of long-term dental implant success and marginal bone loss in postmenopausal women.Niger J Clin Pract 2020;23:147-153

How to cite this URL:
Toy V E, Uslu M O. Evaluation of long-term dental implant success and marginal bone loss in postmenopausal women. Niger J Clin Pract [serial online] 2020 [cited 2020 Feb 24 ];23:147-153
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Dental implant therapy has become a popular treatment modality for the rehabilitation of missing teeth. Although the long-term success of dental implants has been reported in many studies, several risk factors associated with implant, surgery, and patient-related components may disturb long-term implant survival.[1] Sufficient amount and satisfactory quality of bone at the implant recipient site are absolutely crucial for successful implant osseointegration.

Osteoporosis is a systemic skeletal disease characterized by deterioration of bone microarchitecture with reduced bone mass and strength and increased fragility.[2] It is the most common bone disease in humans, particularly in postmenopausal women (PW) due to reduction in ovarian estrogen production. During postmenopausal osteoporosis (PO) a negative balanced bone turnover causes a continuous reduction in bone volume and quality.[3] Systemic bone loss is the main cause of fractures in PW and may also affect jawbone impairing osseointegration. Therefore, PO is thought to be a possible risk factor for bone healing around implants and the rate of bone-to-implant contact. Little is known about the outcomes of PO on the success of dental implants but it is known that implants placed in low-density bone tissues are more likely to fail.[4] The need for dental implants in elderly women is progressively increasing so more information about the long-term effects of osteoporosis on marginal bone level and dental implant survival is required. The aim of this study was to investigate the effects of osteoporosis/osteopenia on long-term implant success and marginal bone loss (MBL) in PW over 50 years of age.

 Materials and Methods

Female patients, 50 years of age or older, who had been rehabilitated with dental implants placed during 2015 or before at the Department of Periodontology, Faculty of Dentistry, Inonu University were contacted. Patients who agreed to sign informed consent and were willing to attend the study were given a control appointment. The study was approved by the Ethical Committee of Malatya Clinical Researchs, Inonu University (Protocol 2019/39) and was conducted according to the principles of the Helsinki Declaration of 1975, as revised in 2013.

Initially, 280 women with minimum one dental implant being in function for at least 3 years were called and asked to bring their dual-energy X-ray absorptiometry (DXA) measurements. Information about their age, osteoporotic diagnosis based on T-score, duration of follow-up, smoking habits, systemic conditions, medication, data concerning implant insertion, and prosthetic rehabilitation and any implant failures were provided using their medical and dental records. Subjects unaware of their bone status, because of not having bone mineral density (BMD) assessment, were excluded from the study. Patients who had systemic diseases that may affect implant success such as uncontrolled diabetes, heavy parafunctions (e.g., bruxism), with a history of bone augmentation and/or sinus lift and smoking habit were also excluded. The patients' osteoporotic status was determined according to T-scores based on The World Health Organization (WHO) criteria [Table 1]. Subjects meeting all of the inclusion and neither of the exclusion criteria were divided into two study groups regarding each subject's lowest T-score.{Table 1}

Inclusion criteria

Being postmenopausal woman over 50 years of age with BMD measurements,Having been rehabilitated by dental implants in 2015 or before,Not having any systemic diseases,Not smoking,Being volunteer to participate in the study.

Exclusion criteria

Lack of BMD measurements,Having been rehabilitated by dental implants after 2015,Presence of systemic diseases that may affect implant success such as uncontrolled diabetes,Smoking,History of bone grafting and/or sinus lift,Severe parafunctional habits such as bruxism.

While Control Group included subjects with a T-score ≥ -1, Test Group (osteoporosis/osteopenia group) included subjects with a T-score [5]

Standardized orthopantomograms were taken with a digital X-ray machine (PlanmecaProline XC 2013; Helsinki, Finland) and marginal bone levels were assessed using an image analysis software (Planmeca, Romexis 3.5.1.R). A researcher blinded to the BMD status of the patient (V.E.T.) took the measurements on radiographs and known implant lengths were used for calibration. Marginal bone levels were measured as the linear distance between the reference point, implant-abutment junction, and the most coronal point of bone-to-implant contact, both mesially and distally. The average of mesial and distal measurements was calculated to determine a single value for each implant. Orthopantomograms taken at the time of implant insertion were regarded as baseline and MBL was calculated as the difference between the marginal bone level at baseline and the follow-up appointment. For every patient in the study, all of the measurements were averaged into one. Duration of follow-up was calculated from the date of implant insertion to the date of recall visit. Finally, the study was completed with a total of 52 patients with 244 implants.

Statistical analysis

Sample size was calculated by power analysis at the beginning of the study (α = 0.05, 1-β (power) = 0.80). It was estimated that at least 21 volunteers for each group would be enough to find a difference of 0.35 mm amount of mean MBL between the groups. The obtained data were analyzed using SPSS 22.0 package program (SPSS Inc., Chicago, IL, USA). A descriptive analysis was performed using mean ± standard deviation (SD) and median with 95% confidence interval (CI). Only ages of the subjects showed normal distribution and were presented as means and SDs of means and compared between the groups by using Independent-samples t test. Analysis of other parameters (T-score, number of implants, follow-up period, PI, PD, BoP and amount of MBL) did not show normal distributions. Therefore, the data for those parameters were presented as means and SDs of means, and median values with minimum/maximum. The differences between the groups were analyzed using Mann-Whitney U test. Fisher's Exact Chi-square Test was used for comparing implant survival rates between the groups on a patient basis. A P value <0.05 was considered statistically significant.


A total of 52 women with 244 dental implants who met the inclusion criteria were included in the study. Patient demographics are listed in [Table 2]. While Test Group included 26 subjects with a mean T-score of -2,55 ± 0,53; Control Group included 26 subjects whose mean T-score was -0,98 ± 1,69, being significantly lower than Test Group (P = 0,001). The mean age of the subjects in Test and Control Groups were determined as 60,61 ± 5,96 and 58,42 ± 5,23, respectively and there was no statistically significant difference between the groups [Table 2].{Table 2}

One hundred and twenty implants were placed in 26 osteoporosis/osteopenia subjects and 124 were placed in 26 control subjects; with an average of 4,61 ± 3,29 and 4,76 ± 2,14 implants per patient respectively. Distribution of the implants according to arch locations is listed in [Table 3]. The mean follow-up period was 60,84 ± 22,13 (min. 36-max. 102) and 60,07 ± 20,93 (min. 36-max. 104) months in Test and Control Groups respectively. All of the implants were followed for at least 36 months. No statistically significant differences were observed between the groups in terms of implant related factors [Table 3].{Table 3}

Data regarding peri-implant soft tissue status and MBL are summarized in [Table 4]. There were no significant differences for PI, PD values, and the amount of MBL between the groups. Although the mean MBL in Test Group (0.82 ± 0,63 mm) was higher than Control Group (0.44 ± 0,33 mm), the difference was not found statistically significant (P = 0.069). Only BoP percentage of Test Group was significantly higher than Control Group (70,57 ± 35,05% and 54,92 ± 30,07% respectively).{Table 4}

The only implant failure was detected in a patient in Test Group resulting an overall implant survival rate of 98.1% on subject level at the 5-year follow-up [Table 5]. The implant supported a mandibular overdenture and was inserted in the region of the left mandibular canine. It was lost 2 years after implant placement and a new implant was successfully inserted 3 months after failure and no additional complication was encountered. No statistically significant difference was observed between the groups regarding the implant survival rates (96,2% versus 100% in Test and Control Groups, respectively; P = 0,313).{Table 5}


Since the average life expectancy is progressively increasing, patients need more dental implants. Long-term success and survival rates of osseointegrated implants have been reported in a number of studies but it is controversial regarding the patients with osteoporosis.[6] Many studies have suggested a possible relationship between periodontal disease and osteoporosis.[7] Although knowledge about the correlation between skeletal and mandibular/maxillary BMD in osteoporotic patients is scarce and an association between implant failure and osteoporosis has not been proved, osteoporosis has been proposed as a risk factor for implant failure.[8] It has been considered to reduce the rate of bone-to-implant contact and the bone support because of decreased cancellous bone volume.[9] On the other hand, there are studies reporting contrary results too.[10],[11] As a better understanding was required, this study was conducted to evaluate the effects of osteoporosis/osteopenia on long-term survival rates of dental implants and MBL in PW. In this retrospective study, after a mean follow-up of 60,46 ± 21,33 months, 1,9% of all implants placed and 3,8% of implants in Test Group failed. MBL was 0.82 ± 0,63 mm and 0.44 ± 0,33 mm for Test and Control Groups respectively with no significant differences between the groups.

Osteoporosis has been defined as a decrease in bone mass and density and an increased risk of fracture. Type 1 osteoporosis generally appears in PW aged over 50 as a result of decrease in estrogen levels and causes women to be susceptible to fractures.[2],[3] WHO has defined diagnostic criteria for osteoporosis based on BMD measurements determined by DXA.[12] It is diagnosed as osteoporosis if the T-score, defined according to the BMD measurements at the hip or lumbar spine, is less than or equal to 2.5 standard deviations (SDs) below the mean of a young-adult reference population (T-score ≤2.5). When the T-score is between −2.5 and −1, then a diagnosis of osteopenia is made [Table 1]. Although DXA imaging has been proposed as the “gold standard” for diagnosis of osteoporosis, WHO definition has been criticized since it does not regard male T-scores and the T-scores of the skeletal bones in other parts of the body. So updated guidelines recommend the use of BMD at both proximal femur and lumbar spine and choosing the lower one.[13] While determining the osteoporotic status of patients, we used the lowest T-scores either of femur or lumbar spine in order to increase the susceptibility of WHO definition.

According to the American Academy of Periodontology, osseointegration is defined as a direct structural and functional contact without having a fibrous tissue between living bone tissue and an implant surface under loading.[14] Given that the amount and quality of bone at the implant recipient site is very important for a successful osseointegration, the effects of osteoporosis on implant success has been investigated in many studies up to now. In the studies performed by Alsaadi et al.[15],[16] osteoporosis was found to be significantly associated with early but not late implant failures. Trullenque-Eriksson et al.[17] assessed long-term outcomes of osseointegrated dental implants and factors that may have influenced implant survival and MBL. They concluded that patients with osteopenia/osteoporosis presented implant failure more frequently. In this study 105 patients with 342 dental implants were included in the study but how many of them were diagnosed as osteopenia or osteoporosis is unknown so the power of the study is questionable. A recently conducted systematic review with meta-analysis presented that while there was no difference in implant survival rate between patients with and without osteoporosis, MBL around implants revealed a significant difference.[18]

On the other hand, there are studies reporting opposite results. In a review on osteoporosis, the evidence for an association between osteoporosis and implant failure was reported to be weak.[19] In another review, it was reported that osteoporosis has been shown to influence osseointegration in preclinical models but not in clinical studies.[20] Holahan et al.[6] demonsrated that osteoporotic status had not affected the survival rate of implants and osteoporosis was not regarded as a contraindication for implant therapy. In another study it was suggested that osteoporotic status and systemic BMD were not associated with local jawbone quality.[21] Dvorak et al.[22] assessed the success rate of dental implants in PW and concluded that PO was not a risk factor for implant loss and periimplantitis. It was also shown that reduced skeletal BMD did not affect survival rate of implants supporting mandibular overdentures.[23] The high survival rate found in this study was attributed to exclusion of patients with risk factors such as smoking, uncontrolled diabetes and alveolar deficiencies as in our study. In the prospective study performed by Temmerman et al.,[24] PW with osteoporosis/osteopenia were followed at 6 months and 1 year after functional loading. While the cumulative survival rates were not significantly different between the groups, there was a significant difference in MBL, being higher in osteoporosis/osteopenia group, after 1 year of functional loading. All of these results, except Temmerman's findings, are consistent with the results found in our study. Although amount of MBL in Test Group was higher than control subjects in our study, it was not statistically significant.

The effects of osteoporosis on implant implantation and on the osseointegrated implants should be considered as two separate topics. In this study, we examined the long-term implant success of dental implants inserted at least 3 years ago in PW retrospectively. Therefore we both evaluated the effects of osteoporosis/osteopenia on implant implantation and on the osseointegrated implants. Besides date of insertion and functional loading, any implant failures were also recorded. When regarding the implant survival rates, the only failed implant was lost 2 years after implant placement so it can be concluded that osteoporotic status did not affect implant implantation or, in other words, osseointegration. On the other hand, although an implant was lost in Test Group resulting an overall implant survival rate of 98.1% on subject level, no statistically significant difference was observed between the groups. It can also be concluded that osteoporotic status did not affect osseointegrated implants too.

Success of dental implants is generally described by implant survival but progressing MBL could risk the long-term survival. A surviving implant does not absolutely mean the maintenance of well-being, only shows that it has not been lost. Implant success criteria, regarding MBL and other parameters, are considered as the gold standard for implant success.[1] To evaluate the long-term prognosis of an implant, it is mandatory to calculate the amount of MBL for a follow-up period. So, in our study, along with survival rates, we evaluated the amounts of MBL which was less than the amount defined by Albrektsson et al.[5] as implant success criteria.

Currently approved medications for the treatment of PO are calcium, vitamin D, bisphosphonates (BPs), hormone replacement therapy, selective estrogen receptor modulators, calcitonin, parathyroid hormone, denosumab, and strontium ranelate. Oral BPs are commonly prescribed pharmacological agents in the treatment of osteoporosis. Osteonecrosis of the jaw (ONJ) has been reported due to oral surgery, including dental implants in patients using BPs in many studies.[25] The likelihood of ONJ may vary depending on the dose, duration, route of administration and the type of BP. Oral BP usage for less than 5 years has been reported to be reliable for dental procedures, particularly for dental implants. It was stated that especially intravenously administered BPs should be considered as a contraindication for dental implant therapy.[26] In the literature, it was reported that more than 90% of the ONJ cases had been seen in patients receiving intravenous BP, while cases in patients using oral BP were scarce. The American Association of Oral and Maxillofacial Surgeons has suggested to stop usage of BPs 3 months before and after oral surgery in patients using BPs for more than 3 years.[27] Only a few of the subjects, six of 26 patients in Test Group (23.07%) in the present study were treated with BPs. Three of them have been rehabilitated with implants after they had given up using the drug. Two of the subjects started BP therapy after implant installation and only one patient was on BP treatment during surgery. All of the subjects using BP were orally administered. Six of the remaining patients were treated with calcium supplementation, one with vitamin D and calcium and one with calcium, vitamin D and denosumab. Since two patients told that they did not receive any treatment and the rest was unknown, pharmacologic agents were not considered and not included in statistics in this study. The only one subject in Test Group who lost one implant was using calcium, vitamin D and denosumab which is a human monoclonal antibody. Although denosumab has been reported to be associated with ONJ,[28] the association of this new therapy is unclear so it is questionable to attribute the only detected failure to the medication used by the patient. Perhaps this failure might be due to the type of prosthetic superstructure since higher implant failure for overdentures, that are generally preferred in complex cases, was reported.[29]

One of the limitations of this study was that all subjects were not diagnosed as osteoporosis; a larger number of patients with osteoporosis rather than osteopenia would be beneficial. Seventeen of the subjects were diagnosed as osteoporosis and nine of them were diagnosed as osteopenia according to their T-scores. Since T-scores of the subjects did not show normal distributions, the data for this parameter was presented as means and SDs of means, and median values with minimum/maximum. While mean value was −2,55 ± 0,53; minimum and maximum values were −1,20 and − 3,40, respectively. Information about the duration of being daignosed as osteoporosis/osteopenia is unfortunately not enough. We only know the duration of 15 subjects and the rest is unknown. The average duration of being osteoporosis/osteopenia for these patients is 10 years. Another limitation was the lack of knowledge about the medications used by the subjects. Pharmacologic agents, that are often prescribed in osteoporotic patients, may have an effect on the peri-implant bone. Since we could not obtain sufficient information about the medications, pharmacologic agents were not considered.


The main objective of this study was to determine if dental implant therapy were a safely preferable treatment option for patients with osteoporosis/osteopenia. The present study shows that PO and reduced BMD does not affect long-term success of implants. Based upon the results of this retrospective study and congruent with recent studies, it can be concluded that dental implant therapy is a preferable option and a diagnosis of osteoporosis/osteopenia is not a contraindication in these patients.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.


1Schwartz-Arad D, Herzberg R, Levin L. Evaluation of long-term implant success. J Periodontol 2005;76:1623-28.
2Raisz LG. Pathogenesis of osteoporosis: Concepts, conflicts, and prospects. J Clin Invest 2005;115:3318-25.
3Riggs BL, Parfitt AM. Drugs used to treat osteoporosis: The critical need for a uniform nomenclature based on their action on bone remodeling. J Bone Miner Res 2005;20:177-84.
4Goiato MC, Dos Santos DM, Santiago JF Jr, Moreno A, Pellizzer EP. Longevity of dental implants in type IV bone: A systematic review. Int J Oral Maxillofac Surg 2014;43:1108-16.
5Albrektsson T, Zarb G, Worthington P, Eriksson AR. The long-term efficacy of currently used dental implants: A review and proposed criteria of success. Int J Oral Maxillofac Implants 1986;1:11-25.
6Holahan CM, Koka S, Kennel KA, Weaver AL, Assad DA, Regennitter FJ, et al. Effect of osteoporotic status on the survival of titanium dental implants. Int J Oral Maxillofac Implants 2008;23:905-10.
7Martinez-Maestre MA, Gonzalez-Cejudo C, Machuca G, Torrejon R, Castelo-Branco C. Periodontitis and osteoporosis: A systematic review. Climacteric 2010;13:523-9.
8Calciolari E, Donos N, Park JC, Petrie A, Mardas N. A systematic review on the correlation between skeletal and jawbone mineral density in osteoporotic subjects. Clin Oral Implants Res 2015;27:433-42.
9Keller JC, Stewart M, Roehm M, Schneider GB. Osteoporosis-like bone conditions affect osseointegration of implants. Int J Oral Maxillofac Implants 2004;19:687-94.
10Becker W, Hujoel PP, Becker BE, Willingham H. Osteoporosis and implant failure: An exploratory case-control study. J Periodontol 2000;71:625-31.
11Amorim MA, Takayama L, Jorgetti V, Pereira RM. Comparative study of axial and femoral bone mineral density and parameters of mandibular bone quality in patients receiving dental implants. Osteoporos Int 2007;18:703-9.
12National Osteoporosis Foundation: Clinician's Guide to Prevention and Treatment of Osteoporosis. Washington, DC: National Osteoporosis Foundation; 2014.
13Kanis JA, McCloskey EV, Johansson H, Cooper C, Rizzoli R, Reginster JY. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 2013;24:23-57.
14Glossary of Periodontal Terms. 4th ed. Chicago, IL: The American Academy of Periodontology; 2001.
15Alsaadi G, Quirynen M, Komarek A, van Steenberghe D. Impact of local and systemic factors on the incidence of oral implant failures, up to abutment connection. J Clin Periodontol 2007;34:610-7.
16Alsaadi G, Quirynen M, Komarek A, van Steenberghe D. Impact of local and systemic factors on the incidence of late oral implant loss. Clin Oral Implants Res 2008;19:670-6.
17Trullenque-Eriksson A, Guisado-Moya B. Retrospective long-term evaluation of dental implants in totally and partially edentulous patients. Part I: Survival and marginal bone loss. Implant Dent 2014;23:732-7.
18de Medeiros FCFL, Kudo GAH, Leme BG, Saraiva PP, Verri FR, Honorio HM, et al. Dental implants in patients with osteoporosis: A systematic review with meta-analysis. Int J Oral Maxillofac Surg 2018;4:480-91.
19Bornstein MM, Cionca N, Mombelli A. Systemic conditions and treatments as risks for implant therapy. Int J Oral Maxillofac Implants 2009;24(Suppl):12-27.
20Mellado-Valero A, Ferrer-García JC, Calvo-Catalá J, Labaig-Rueda C. Implant treatment in patients with osteoporosis. Med Oral Patol Oral Cir Bucal 2010;15:52-7.
21Holahan CM, Wiens JL, Weaver A, Assad D, Koka S. Relationship between systemic bone mineral density and local bone quality as effectors of dental implant survival. Clin Implant Dent Relat Res 2011;13:29-33.
22Dvorak G, Arnhart C, Heuberer S, Huber CD, Watzek G, Gruber R. Peri-implantitis and late implant failures in postmenopausal women: A cross-sectional study. J Clin Periodontol 2011;38:950-5.
23Chow L, Chow TW, Chai J, Mattheos N. Bone stability around implants in elderly patients with reduced bone mineral density-a prospective study on mandibular overdentures. Clin Oral Implants Res 2017;28:966-73.
24Temmerman A, Rasmusson L, Kubler A, Thor A, Quirynen M. An open, prospective, nonrandomized, controlled, multicentre study to evaluate the clinical outcome of implant treatment in women over 60 years of age with osteoporosis/osteopenia: 1-year results. Clin Oral Implants Res 2017;28:95-102.
25Chadha GK, Ahmadieh A, Kumar S, Sedghizadeh PP. Osseointegration of dental implants and osteonecrosis of the jaw in patients treated with bisphosphonate therapy: A systematic review. J Oral Implantol 32013;9:510-20.
26Madrid C, Sanz M. What impact do systemically administrated bisphosphonates have on oral implant therapy? A systematic review. Clin Oral Implants Res 2009;20(Suppl 4):87-95.
27Allen MR, Ruggiero SL. A review of pharmaceutical agents and oral bone health: How osteonecrosis of the jaw has affected the field. Int J Oral Maxillofac Implants 2014;29:45-57.
28Aghaloo TL, Felsenfeld AL, Tetradis S. Osteonecrosis of the jaw in a patient on denosumab. J Oral Maxillofac Surg 2010;68:959-63.
29Berglundh T, Persson L, Klinge B. A systematic review of the incidence of biological and technical complications in implant dentistry reported in prospective longitudinal studies of at least 5 years. J Clin Periodontol 2002;29(Suppl 3):197-212.