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 Table of Contents  
Year : 2021  |  Volume : 33  |  Issue : 4  |  Page : 428-434

Association of dental implants success in bone density classification of postmenopausal women with osteoporosis - a clinical and radiographic prospective study

Department of Periodontology, Damascus University, Syria

Date of Submission04-Mar-2021
Date of Decision23-Jun-2021
Date of Acceptance28-Sep-2021
Date of Web Publication27-Dec-2021

Correspondence Address:
Dr. Wasim Alsadi
Department of Periodontology, Damascus University, Damascus
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jiaomr.jiaomr_61_21

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Introduction: Osteoporosis according to postmenopausal women is a major health problem increasing yearly. Thus, there is a growing need to assess the success of dental implants among these patients. Aim: Evaluation of dental implants success between 6 and 12 months follow-up on postmenopausal women with osteoporosis by means of clinical and radiographic assessment. Materials and Methods: A total of 30 female patients aged between 46 and 65 years were diagnosed with osteoporosis and treated with Vitamin D3 and Calcium (Vit D3 and Ca). The sample was divided into two groups: Group 1- 15 female patients diagnosed with osteoporosis (bone density of D2) and treated with (Vit D3 and Ca) and group 2- 15 female patients diagnosed with osteoporosis (bone density of D3) and treated with (Vit D3 and Ca). A total of 60 dental implants were placed in the mandibular posterior area. Implant loading was done after 6 months. Follow up intervals were 6 to 12 months after loading. Results: According to the study, compromised survival was in two implants in the osteoporosis group with a bone type of D2 with a rate of 3.3%, and compromised survival in the osteoporosis group with bone type of D3 was 11 implants with a rate of 18.3%. The success was in 52 implants, with a rate of 86.7%. Conclusion: Placing dental implants in postmenopausal female patients with osteoporosis and treating with (Vit D3 and Ca) is a safe treatment option for missing teeth, despite the bone density type. More researches about implant with osteoporosis patients are recommended.

Keywords: Bone mineral density, dental Implants, osteoporosis, post-menopausal

How to cite this article:
Alsadi W, AbouSulaiman A, AlSabbagh MM. Association of dental implants success in bone density classification of postmenopausal women with osteoporosis - a clinical and radiographic prospective study. J Indian Acad Oral Med Radiol 2021;33:428-34

How to cite this URL:
Alsadi W, AbouSulaiman A, AlSabbagh MM. Association of dental implants success in bone density classification of postmenopausal women with osteoporosis - a clinical and radiographic prospective study. J Indian Acad Oral Med Radiol [serial online] 2021 [cited 2022 Aug 8];33:428-34. Available from: https://www.jiaomr.in/text.asp?2021/33/4/428/333879

   Background Top

Osteoporosis is a systemic skeletal disease characterized as a reduced bone strength that predisposes to an increased risk of fractures.[1] It is a very common disease that affects on about 300 million people around the world.[2],[3] It is most common in females, and its incidence increases with age.[4] It is usually accompanied by destruction of bone microarchitecture with a reduced bone mass, strength and increased fragility.[5]

The resistance reflects the amount of bone density and bone quality. Bone density is determined by the maximum value of bone mass (measured in grams per cm2) and the magnitude of their loss. The diagnosis of osteoporosis was established by basing on the classical values of bone mineral density (BMD) that is achieved in bone densitometry. This method is called dual X-ray absorptiometry for lumbar vertebrae (L1, L2, L3, L4). Osteoporosis was considered when the T-score was less than -2.5 SD. The T number of standard deviation is how much a subject deviates from the average BMD of a population group of healthy young women.[6]

Osteoporosis is classified according to the WHO[7]:

  1. Initial common osteoporosis: that has several types, Type 1: postmenopausal osteoporosis, commonly seen in ladies aged between 41 and 75. Represents a rapid and irregular loss in spongy bone. Type 2: Elderly osteoporosis: mostly common in both genders after the age of 75, and affects spongy and cortical bone. Type 3: idiopathic osteoporosis: affects both elderly and children.
  2. Diseases accompanied by osteoporosis such as calcium deficiencies.
  3. Hereditary connective tissue diseases accompanied by osteoporosis – Ehlers Danlos syndrome and Marfan syndrome.
  4. Idiopathic diseases accompanied by osteoporosis: Arthritis, Epilepsy, Malnutrition, Diabetes, Alcoholism, and Menkes syndrome.

Although it is caused by several factors as calcium and vitamin D deficiency, sedentary and genetic factors, postmenopausal estrogen deficiency is the major known etiology.As estrogen regulates bone remodeling, the cessation of estrogen production induces a bone remodeling imbalance with bone resorption exceeding bone formation, leading to bone fragility and increased risk of fracture.[8]

Currently, the BMD is only considered as a risk factor that must be assessed in the context of age, sex, smoking, body weight, family history, etc.[9] The management of osteoporosis patients is done by medication such as bisphosphonates (Alendronate-Risendronate), glucose, calcium 5001000 mg, and vit D3 (600 units).[5]

Previous animal studies using an ovariectomy model of osteoporosis induction with implants inserted in rats have shown that estrogen deficiency results in lower bone turnover rate, bone-to-implant contact, bone/implant interface biomechanical competence, and bone density on cancellous bone. Therefore, it has been reported as a systemic alteration possibly related as a risk factor to osseointegration process, and some authors suggested that the predictability of dental implant success may be seriously impaired when patients present osteoporosis or osteopenia.[10]

Despite this evidence, from a clinical perspective, the literature findings on the topic are sparse and contradictory. According to a recent systematic review, osteoporotic subjects presented higher rates of implant loss, however, there is lower evidence to strengthen or refute the hypothesis that osteoporosis may have detrimental effects on bone healing. Consequently, conclusions regarding the effect of osteoporosis in dental implant therapy cannot be made at this time.[11]

Thus, the aim of this study was to determine the relationship between osteoporosis in postmenopausal women and the success of dental implants using cone-beam computed tomography (CBCT), according to the bone density type classification by Zarb and Lekholm.[12]

   Materials and Methods Top

This prospective clinical study lasted for 24 months from September 2017 to October 2019. A total of 60 implants were done for 30 patients aged between 46 and 64 (mean age 54.5) diagnosed with osteoporosis at least 5 years according to the WHO diagnosing criteria and dual-energy X-ray absorptiometry (DXA) imaging.

Sample size Estimation

The sample was divided into two groups and the sample size was calculated with G*Power 3.1.9 software (University of Kiel, Germany). The significance level was set at 0.05, the statistical power was set at 80%.Based on a student t-test and previous studies , an estimated 15 patient in each group were required to demonstrate an effect size (0.4).

Group 1:A total of 15 female patients with a bone density of D2 according to Zarb and Lekholm scale[12] using Hounsfield units[13] and treated with (vitamin D3 and Calcium) for a period no less than 2 years.

Group 2: A total of 15 female patients with a bone density of D3 according to Zarb and Lekholm scale[14] using Hounsfield units[11] [Table 1], and treated with (vitamin D3 and Calcium) a period of time no less than 2 years.
Table 1: Hounsfield units

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The patients consulted the orthopedic clinic in Damascus university hospital and were directed to the periodontology department in Damascus university where this study took place. Medical and dental history was recorded for each patient using a designated study form, and a complete periodontal chart was obtained for each patient. The written consent was taken from patients after being informed about the nature of the study and its objective. This research was reviewed by the ethics board at Damascus University and was assigned an ethical approval number 3392 dated 20/08/2017. The study was conducted according to the principles of the Helsinki Declaration of 1975, as revised in 2000.

Inclusion criteria for both bone density groups:

  1. Being postmenopausal, aged over 50 years, and suffering from osteoporosis for a period of not less than 5 years, with Bone Mineral Density measurements.
  2. No history of periodontal/periimplant disease.
  3. Osteoporosis with a T-score δ -2.5 according to the WHO guideline.[3] [Table 2]
  4. Being treated with bisphosphonates, glucose, calcium 500–1000 mg, and vit D3 (600 units) for not less than 2 years.
Table 2: WHO osteoporosis guideline

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Exclusion criteria for both bone density groups:

  1. Presence of systemic diseases that may affect implant success.
  2. Presence of deleterious habits that may affect implant success (smoking, alcohol intake. etc.).
  3. History of bone grafting and/or sinus lift,
  4. Severe parafunctional habits such as bruxism.

   General Radiographic Examination Top

DXA measurements were taken in Damascus university Hospital with a (Lunar -DPX) device that shows bone density, mineral amounts in bone, and T-score.

   Clinical and Radiographical Periodontal Examination Pre-implantation Top

The patients were given full instructions regarding their oral health. A complete periodontal chart was obtained for each patient. Cone-beam computed tomography (CBCT) was taken to evaluate periimplant tissues and the future places to insert the implants. [Figure 1]
Figure 1: (a) A CBCT showing the tissues pre-implementation and the anatomical landmarks adjacent to the implants site. (b) a CBCT showing the bone diameters in order to receive the implant

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Bone height was also evaluated on the same radiographs with 8.5 mm height and above which was appropriate for implantation.

   Surgical Stage: Preparing the Implant Place Top

Full-thickness flap was raised to eliminate the incisions to reveal the active area by using a 15-straight blade size and a periosteum. A hole was drilled using a rounded locator drill with enough irrigation and a surgical motor by Osstem (Suni Max). Twist drills were used with a torque (825 rpm) to expand the diameter until it is (1–2 mm) less than the diameter required to ensure the initial stability, and an Osstem GS2 implant was inserted. Two implants were placed in the posterior mandible area for each patient.

With heights of (8.5, 10, 11.5, 13) and diameters of (3.5, 4, 4.5).

Buccal and lingual flaps were sutured using a 3-0 silk thread. [Figure 2]a, [Figure 2]b, [Figure 2]c, [Figure 2]d.
Figure 2: (a) Initial stage. (b) preparing the implants placement site. (c) placing the implants. (d) final stage

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   Post-Surgery Follow Up Top

The patients were recalled after 10–15 days to remove surgical threads and ensure the healing of periimplant soft tissues and the level of oral health.

Prosthetic stage

All prostheses were done for all the patients after extending the healing period of 1 year to ensure the osseointegration process.

A full-thickness flap was raised over the implant and the poly ethelyne plug was removed. The implant's retention was tested with (GAU03) by osstem with a torque of 30 N clockwise, and the healing abutment was placed for 15 days period.

Impressions and wax bites were taken for patients who were using (kohler) impression material. Contiguous implants were restored with a porcelain fused metal fixed bridge, no implants were connected to any tooth.

Occlusion loading on implants was avoided, and occlusal forces were distributed evenly on the implants.

   Follow up Stage Top

The follow-up period was 6 to 12 months after implant loading and periodontal indexes were taken. Cone-beam computed tomography (CBCT) was made.

   Clinical Assessment Top

A complete periodontal chart was obtained for each patient. Each implant was examined individually. The presence of pain during vertical and horizontal percussion, history of pus during the follow-up stage, and the presence of any movement was taken. Bleeding on probing index and plaque index was also taken. All results were recorded on a special chart.

Bleeding on probing index was also taken in four places (mesial, distal, lingual, and buccal) around the implant using a plastic periodontal probe.

   Radiographic Assessment Top

A Cone-beam computed tomography (CBCT) was done at the baseline and 6 months intervals to measure the bone resorption both horizontally and vertically and to measure the bone density for all patients after loading. The CBCT Cranex 3D (Soredex, Tuusula, Finland) with 90 kVp and 0.2mm voxel size and FOV: 6×8 cm2, mA: 10,T: 12.6s, Rotation time: 20s were used in this study.

The amount of bone resorption was measured by using the profile tool attached with CBCT software (OnDemand 3D Dental version 1 year after loading in the mesial and distal for each implant, and the mean value was taken. Measurements were taken from a reference point, defined as a junction of the roughened and machined beveled surface, to the most coronal point of the implant. [Figure 3]a, [Figure 3]b.
Figure 3: (a) A CBCT showing the resorption around the implants after 1 year. (b) a CBCT showing the reference point and the amount of resorption around the implants

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Statistical study

The data were computerized by using SPSS 13th edition with proper statistical tables.

Independent un-paired T-student test was run to study the differences in T-Score values between failed implants, compromised survival, survival, and success in P < 0.05. Chi square test was used to evaluate statistical differences between the D2 osteoporosis group and the D3 osteoporosis group and determine if there is any statistical difference.

   Results Top

A total of 60 implants were done for 30 female patients between 46 and 64 years age (mean age 54.5) diagnosed with osteoporosis. Implant success rate and clinical indices and peri-implant bone resorption were compared between the two groups.

Implant success was evaluated according to the Health Scale Dental Implant and was categorized into four domains as following: (Success, Survival, Compromised Survival, and Failure).

There was no failure noticed in group 1. However, two implants in group 2 were considered a failure.

There was no statistical difference between both groups with regards implant success. (P > 0.05). [Table 3] and [Table 4]
Table 3: Inter-group comparison between two groups for implantation success after 6 and 12 months of loading.

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Table 4: Inter-group comparison between two groups for implantation success after 6 and 12 months of loading

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Peri implant bone resorption radiographic results

  • After 6 months: The mean value of resorption was 1.07 mm with a standard deviation of 0.89 in the first group (D2 group), and the mean value of the D3 osteoporosis group was 2.25 mm with a standard deviation of 0.82 with a P value > 0.05, so that there was no statistical difference between the two groups.
  • After 12 months: The mean value of resorption was 0.97 mm with a standard deviation of 0.73 in the first group (D2), and the mean value of the D3 osteoporosis group was 2.25 mm with a standard deviation of 0.84 with a P value > 0.05, so that there was no statistical difference between the two groups. [Table 5] shows the resorption between the two groups in 612 months follow- up period.
Table 5: Inter-group comparison between two groups for radiographic success

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   Discussion Top

Many studies have suggested a possible relationship between periodontal disease and Osteoporosis.[3],[4],[5] Although the correlation between skeletal and mandibular/maxillary BMD in osteoporotic patients is scarce and the association between implant failure and Osteoporosis has not been proved, osteoporosis has been proposed as a risk factor for implant failure.[15],[16],[15],[16],[17] It has been considered to reduce the rate of bone-to-implant contact and the bone support because of decreased cancellous bone volume.[18],[19],[20]

Our study included placing 60 dental implants for 30 females (15 having been diagnosed and treated osteoporosis according to the World Health Organisation criteria with a bone density of D2, and 15 with osteoporosis and a bone type of D3 according to Lekholm and Zarb scale[14]). The average value of T-score = -2.5. The periodontal indexes and oral health were adjusted in all the female patients. The lower jaw was selected on which the procedure was performed so that to unify all criteria and adjust the specimen because the density of the lower jaw is more than the one of the upper jaw. The occlusion load on the implants was minimized in order to avoid occlusion trauma. The patients with acute osteoporosis were excluded to avoid jeopardizing the female patients to fracture of the lower jaw and to ensure the osseointegration. The period of osseo integration was extended to 12 months in order to increase the chance of osseo integration in the osteoporotic bone.

We have found the dental implantation for women with osteoporosis according to the health implant scale was 93.3%. This percentage of success is close to the study of Becker et al.[21] carried out on 49 implants where the successful implants were 95%. In our study, it was also close to the percentage of success in the study of Vetoy et al.[22] which included 52 patients with a mean age of 59.51 ± 5.66 years. Implant survival rates were 96.2% and 100% with a mean follow-up of 60.84 ± 22.13 and 60.07 ± 20.93 months. Where the percentage of success in the lower jaw was 97%. The researcher applied a long monitoring period, and the implants were placed in several places of the lower jaw (posterior and anterior).

Our study was compatible also with the studies of FCF de Medeiros et al.[23] who used PubMed\Medline web of sciences and Cochrane library. Fifteen studies involved 8859 patients, and 29,798 implants were included. The main outcome of the meta-analysis indicated that there was no difference in implant survival rate between the patients with and without osteoporosis, either at the implant level (RR 1.39, 95% CI 0.93-2.08; P = 0.11) or at the patient level (RR 0.98, 95% CI 0.50-1.89; P = 0.94). However, the meta-analysis for the secondary outcome revealed a significant difference in marginal bone loss around the implants between the patients with and without osteoporosis (0.18 mm, 95% CI 0.050.30, P = 0.005). The data heterogeneity was low. Temmerman et al.[21] included two groups of osteoporosis patients – group O (osteoporosis) and group C (control group). A total of 148 implants were placed in 48 patients (mean age 67 years). Sixty three implants were placed in 20 patients (group O) and 85 implants in 25 patients (group C).

After 5 years, the survival rate was 96.5% according to the implant and 95.7% according to the patient. The bone loss was observed in the osteoporosis patients group, and the implant therapy in those patients was efficient with a high success rate. This study was a new approach to dental implants in bone densities of D2 and D3. Our study was close and also compatible with the study of Luke chow et al.[24] which recruited 79 patients in the study, the survival rate of the implant was 98.7%. Sixty-three patients (79.7%) were finally available for data collection and statistical analyses. The mean follow up time was 62.9 (SD = 15.2) months with the mean marginal bone loss (MBL) 0.65 mm (SD = 0.67) and the mean GBL 1.25 mm (SD = 0.83), respectively. The average BOP and PI of patients were 49.6% (SD = 30.8) and 47.4% (SD = 37.4) but was different from it in MBL levels where skeletal BMD was not associated with the marginal MBL (mean MBL: r = -0.094, P = 0.466; mean GBL: r = 0.04, P = 0.761).

In this study, we evaluated the relationship between bone density and the results of successful and failed implants. We did not find statistically significant differences between the shortage of total metal bone density and the results of the dental implantation in the posterior lower jaw, which agrees with the study of Temmerman et al.[25] On the upper jaw, no significant difference was seen statistically in implant integration and survival after 1 year of functional loading. The reason for that may be attributed to the small number of specimen individuals and the short monitoring period.

The percentage of cases where no bone absorption occurred around the dental implants was 80%. This corresponds with the percentage of clinical success. On the other hand, 20% of the dental implants had bone absorption, which was compatible with the study of Joe Merheb et al.[26] In implant placement, primary stability was in a lower average in the osteoporosis group (63.3 ± 10.3 ISQ) than in osteopenia group (65.3 ± 7.5 implant stability quotient (ISQ)), and group C (66.7 ± 8.7 ISQ). At abutment placement, a similar trend was observed.The osteoporosis group (66.4 ± 9.5 ISQ) scored lower than group osteopenia (70.7 ± 7.8 ISQ), whereas the highest average was for group C (72.2 ± 7.2 ISQ). The difference between osteoporosis and Group C was significant. Implant length and diameter did not have a significant effect on the implant stability as measured with RFA. A significant correlation was found between the local bone density and the implant stability for all regions of interest. The bone resorption and implant stability were influenced by the local and skeletal densities. The occurrence of bleeding when probing around the implants where bone absorption happened may indicate that the periodontitis was a result of the noncompliance of some female patients with the oral care instructions.

The relationship between the failure of dental implants and the occurrence of bone absorption indicates that the cause of failure of female patients with osteoporosis is not the shortage of bone density, but rather it is because of disease around the implants. Our study agreed with the study of F R Rozema, 2020[27] which concluded that placing implants in patients with osteoporosis is not contraindicated and the implant survival rate, marginal bone loss, and mucosal parameters do not behave differently from they do in the healthy group of patients.

Limitations and Future Prospects

Future studies about implantation in women with osteoporosis presenting with D 4 type of bone must be conducted. It is also recommended to select the appropriate dentures on the implants with the observation of extending the healing period (Osseointegration) to 6 months in the lower jaw.

   Conclusion Top

Our study was a new approach to dental implantation in patients with osteoporosis that compared two types of bone densities. It also showed an acceptable success of dental implants in female patients with osteoporosis in the lower jaw with D2 and D3 bone types, despite the period of treatment with vit D3 and Ca.Oral care should be taken and general healthy state of the female patients should be ensured before the implantation, during the healing, and after the implantation period.


Damascus University funded this study.

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.

   References Top

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Al-Ekrish, Asma'A. A, Gerlig Widmann, Sara A. Alfadda, Asma'A. A. Al-Ekrish. “Revised, Computed Tomography-Based Lekholm and Zarb Jawbone Quality Classification.” International Journal of Prosthodontics 31, no. 4 (2018).  Back to cited text no. 12
Lekholm U,Zarb GA. Patient selection and preparation. In: Branemark PI, Zarb GA, Alberktsson T. Tissue-integrated Protheses: Osseointegration in vlinical Dentistry. Chicago Quintessence Publishing Company, 1985:199-209.  Back to cited text no. 13
Lotz EM, Cohen DJ, Ellis RA, Wayne JS, Schwartz Z, Boyan BD. Ibandronate treatment before and after implant insertion impairs osseointegration in aged rats with ovariectomy induced osteoporosis. JBMR Plus 2019;3:e10184.  Back to cited text no. 14
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Nguyen VH. Smoking Status on Bone Health and Osteoporosis Prevalence. Osong Public Health Res Perspect 2018;9:213-4.  Back to cited text no. 17
Poxleitner P, Steybe D, Kroneberg P, Ermer MA, Yalcin-Ülker GM, Schmelzeisen R, et al. Tooth extractions in patients under antiresorptive therapy for osteoporosis: Primary closure of the extraction socket with a mucoperiosteal flap versus application of platelet-rich fibrin for the prevention of antiresorptive agent-related osteonecrosis of the jaw. J Craniomaxillofac Surg 2020;48:444-51.  Back to cited text no. 18
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Sadat-Ali M, Al-Dakheel DA, Azam MQ, Al-Bluwi MT, Al-Farhan MF, AlAmer HA. Reassessment of osteoporosis-related femoral fractures and economic burden in Saudi Arabia. Arch Osteoporos 2015;10:37.  Back to cited text no. 20
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Temmerman A, Rasmusson L, Kübler A, Thor A, Merheb J, Quirynen M, A prospective, controlled, multicenter study to evaluate the clinical outcome of implant treatment in women with osteoporosis/Osteopenia: 5-Year Results. J Dent Res 2019;98:84-9.  Back to cited text no. 23
Luke Chow, Tak Wah Chow, John Chai Nikos Mattheos , Bone stability around implants in elderly patients with reduced bone mineral density - a prospective study on mandibular overdentures, Clin Oral Implants Res. 2017 Aug;28(8):966-973. doi: 10.1111/clr.12907.  Back to cited text no. 24
Joe Merheb, Andy Temmerman, Lars Rasmusson, Alexander Kübler, Andreas Thor, Marc QuirynenInfluence of Skeletal and Local Bone Density on Dental Implant Stability in Patients with Osteoporosis clinical implant dentistry and related research.2016;18:253-60.  Back to cited text no. 25
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  [Figure 1], [Figure 2], [Figure 3]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]


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