SYSTEMATIC REVIEW
Prognosis of dental implants in patients with low bone density: A systematic review and meta-analysis Iman A.-W. Radi, DDS, PhD,a Wafaa Ibrahim, DDS, PhD,b Sylvia M. S. Iskandar, MDSc,c and Nouran AbdelNabi, DDS, PhDd Over 200 million people ABSTRACT worldwide suffer from osteoStatement of problem. Osteoporosis is a risk factor for implant success. Evidence for the prognosis porosis.1 Approximately 30% of dental implants in patients with osteoporosis is still unclear. of all postmenopausal women Purpose. The purpose of this systematic review was to compare implant success in patients with have osteoporosis in the low versus normal bone density and to evaluate special techniques used to enhance implant United States and in Europe.2 success in these patients. Aging populations worldwide Material and methods. Searches were performed electronically in 4 databases (PubMed, LILACS, are also responsible for a major Cochrane, and Grey Literature) through July 2017 and manually to identify studies addressing the increase in the incidence of subject. Randomized and nonrandomized clinical trials and cohort studies were included. low bone density in postResults. Eleven studies met the eligibility criteria, with a total of 1071 participants. Seven studies menopausal women.3 Several compared implant success in low and normal bone density, and 4 compared implant success in studies have shown a positive special and conventional techniques of implant placement. The risk of bias in the assessment of correlation between implant cohort studies was critical; of nonrandomized clinical trials, serious; and of randomized clinical trials, failure and low bone denhigh. The meta-analysis showed no significant difference between implant survival in patients with sity.4-7 Åstrand et al4 and low and normal bone density 5 years after implant placement. Busenlechner et al5 reported Conclusions. Implant survival in patients with low bone density seems to be feasible with special that low bone density seriously precautions. Implant placement using special adopted techniques might provide equivalent affects primary implant stabilimplant stability, survival, and marginal bone loss to normal bone. The quality of evidence is still ity and survival. Similarly, in a unclear. (J Prosthet Dent 2018;-:---) case-control study, Jaffin and Berman8 reported 35% implant loss in Type IV bone findings. A critical summary conducted by Alqutaibi and (Leckholm and Zarb)9 compared with Types I, II, and III, Radi13 reported no clear evidence of the results of the which have shown an implant loss of only 3%. However, Giro et al12 review. Holahan et al10 believe that osteoporosis or osteopenia The increased prevalence of low bone density among were not contraindications for dental implant therapy. de patients introduced modified surgical techniques such as Medeiros et al11 and Giro et al12 conducted systematic undersized drilling, bone condensation, and modified reviews and reported similar success rates in patients implant designs to overcome associated failures. Underwith or without osteoporosis. Unfortunately, de Medeiros sized drilling was said to provide good primary implant et al11 combined studies of different designs in their stability in low bone density,14,15 despite the fact that it meta-analyses, which raised concerns about their resulted in compressive forces in the crestal portion and
a
Professor, Prosthodontics, Faculty of Dentistry, Cairo University and Member of Evidence Based Dentistry Centre, Cairo University, Egypt. Lecturer, Faculty of Dentistry, Delta University for Science and Technology, Egypt. c Assistant Lecturer, Faculty of Dentistry, Misr International University, Egypt. d Lecturer, Faculty of Dentistry, Cairo University, Egypt. b
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Clinical Implications Placing implants in patients with low bone density depends on patient selection and might require bone condensation and/or step osteotomy to enhance success.
consequently led to necrosis.16,17 To overcome this disadvantage, a surgical technique was introduced called ‘stepped osteotomy,’ which requires an underpreparation in the apical part of the osteotomy only.18 Lateral bone condensation19 and modified implant designs4,20 were also introduced to enhance both implant stability and survival.21 The length and width of dental implants play significant roles in osseointegration. An increase in either or both of them results in an overall increase in the total surface area.22 Contradictory results of implant survival in patients with low bone density have raised concerns regarding the need for these special techniques to obtain satisfactory survival and have increased the indication for conducting this systematic review. The objectives, therefore, were first to compare implant success in patients with low and normal bone density and second to determine whether special surgical techniques or implant designs used in patients with low bone density could lead to satisfactory success. MATERIAL AND METHODS This systematic review was reported according to Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines. The review was registered on the International Prospective Register of Systematic Reviews (PROSPERO) website, Center for Reviews and Dissemination, University of York on January 12, 2016, with registration number CRD42016050585. The population was adult women and men with low bone density who had dental implants in either the maxillary or mandibular arch. Participants younger than 18 years, those with secondary osteoporosis induced by drugs, or those who received chemotherapy or radiotherapy were excluded. Regarding exposure and intervention, studies comparing implant failure in participants with low and normal bone density were considered eligible. Articles in which special surgical techniques, implant designs, or surface treatments were used in individuals with low bone density were included. Studies that used short implants (<10 mm in length) or mini implants (<3 mm in diameter) or those that required soft and hard tissue grafting, immediate loading, and/or immediate implant placement were excluded. All these factors might affect both implant stability and failure. Considering outcomes, studies reporting implant failure as described by Albrektsson et al23 were considered
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eligible. The outcomes sought by this review were divided into primary and secondary outcomes according to patient relevance. Implant failure in terms of survival/loss, stability, pain/ paresthesia, inflammation/infection, and gingival recession was chosen as a primary outcome because of its effect on the patient. The secondary outcomes were periimplant radiolucency and peri-implant bone changes. These outcomes were radiographically detectable. Studies reporting these outcomes at any time after implant placement were included. Randomized clinical trials (RCTs), nonrandomized clinical trials (NRCTs), and cohort studies were included. Reviews, animal studies, in vitro studies, case series, case reports, case-control studies, cadaveric studies, and correlation studies not comparing normal and low bone density were excluded. Published and unpublished studies reported in the English language only were included. I.A.R., N.A., and S.I. searched 4 electronic databases (PubMed, LILACS, Cochrane, and Grey Literature) and hand-searched 8 journals (International Journal of Prosthodontics, Journal of Prosthodontics, Journal of Clinical Oral Implant Research, Journal of Implant Dentistry, International Journal of Oral and Maxillofacial, Journal of Oral Rehabilitation, British Dental Journal, and Journal of the American Dental Association) in addition to the Egyptian Knowledge Bank until December 2016. The search was updated in July 2017. The detailed search strategy can be seen in Supplemental Table 1. Primary screening of all identified studies by title and abstract was performed by N.A. and S.I. independently and in duplicate to exclude nonrelevant articles. At this stage, article inclusion rather than exclusion was done. Secondary screening by full text was performed by the same reviewers. Disagreements were resolved by discussion or by involvement of a third reviewer (I.A.R.). Inclusion in the meta-analysis was based on a plan to assess the clinical and methodologic heterogeneity of the included studies. The risk of bias assessment was not considered a factor for inclusion in the meta-analysis. A risk of bias assessment was carried out by I.A.R., W.I., and S.I. separately and in duplicate based on the outcome level within and across the studies. When conflicts occurred between the review authors, they were resolved by discussion and voting. The risk of bias of the RCTs was assessed using the Cochrane Risk of Bias tool as illustrated in the Cochrane handbook.24 NRCTs and cohort studies were assessed using the Cochrane ROBINS tool. Unfortunately, fewer than 10 studies were available to assess planned publication bias by funnel plot. I.A.R., N.A., and S.I. were involved in data extraction. The process began with piloting the design of the tables on 3 of the included studies. Where data were unclear or missing, S.I. contacted the authors of the study. Numeric Radi et al
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Identification
Records identified through database searching (n=2621) All included records (n=2638)
PubMed=2258 Cochrane=187 LILACS=176
Eligibility
Screening
Records after duplicates removed by Endnote (n=2580)
Duplicates removed (n=58)
Records screened by title (n=2580)
Records excluded (n=2449)
Eligible records screened by title and abstract (n=131)
Records excluded (n=94)
Full-text articles assessed for eligibility (n=37)
Studies included in qualitative synthesis (n=11)
Included
Additional records identified through hand searching (n=17): 12 records through reference review 2 studies from International Journal of Oral and Maxillofacial Implants 3 studies from International journal of Prosthodontics
Studies included in quantitative synthesis (meta-analysis) (n=3)
Full-text articles excluded (n=26): Bone grafting performed 5,25-28 Short implants used 29-36 Patients received chemotherapy or radiotherapy 36 In vitro study 37 Case report 38 Case series 39 Systematic review 40 Narrative review 41 Irrelevant topic 42-46 Unfound neither full text nor by author’s contact 47-49
Studies excluded from meta-analysis (n=8): Implant stability outcome Different study design 19,50,51,54 Same population 9,50,51,55 Implant survival Different study design 54 Same population 9,55 Marginal bone loss Different follow up periods 4, 54,52 Different objectives 4,52
Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) flow indicating number of studies at different review stages.5,25-57
missing data were clarified by contacting the authors. Otherwise, they were calculated whenever possible. Types I, II, and III described by Lekholm and Zarb,9 D1 and D2 described by Misch,25 a Hounsfield unit 850,25 a score of 1 or 2 for the surgeon’s tactile sense,20 and finally a T score e11 were all assumed equivalent because they were all described as normal
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bone density. Soft bone was assigned to D3, D4 (Misch classification),25 type IV (Leckholm and Zarb),9 Hounsfield unit <850,25 a score of 3 or 4 for the surgeon’s tactile sense,20 and T score
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Table 1. Characteristics of included studies
Study
Setting
Implant Size (Diameter/ I or E Length)
No. of Implants
Chow et al31
Prince Philip Dental 2 per patient Hospital, Hong (N=158) Kong
Lauc et al22
NA
N=92
Jaffin and Berman8
NA
Temmerman et al30
Centers: Leuven, Gothenburg, Wurzburg, and Uppsala
Holahan et al10
C
Habits (Smoking/ Bruxism)
Opposing Arch
Site of Implant Placement
Material and Type of Prosthesis
Low bone density
Normal bone density
Included only patients who could cease smoking for 3 months before implant surgery (52 participants were non-smokers)
Complete denture
Anterior mandible
NA
Low bone density
Normal bone density
NA
NA
Maxilla and Fixed prosthesis mandible, anteriorly and posteriorly
N=1054
NA
Low bone density
Normal bone density
NA
NA
Maxilla and Intermediate mandible, removable anteriorly and prosthesis posteriorly
2-8 splinted implants (N=148)
NA
Low bone density
Normal bone density
Included ex-smokers, NA habitual smokers, occasional smokers and non-smokers
Maxilla
Mayo Clinic N=3224 School of Graduate Medicine, Rochester, Minn.
NA
Low bone density
Normal bone density
Smokers included
NA
Maxilla and NA mandible, anteriorly and posteriorly
Holahan et al32
Mayo Clinic N=2867 School of Graduate Medicine, Rochester, Minn.
NA
Low bone density
Normal bone density
Smokers included
NA
Maxilla and NA mandible, anteriorly and posteriorly
Åstrand et al4
Multiple centers in Sweden
N=240
Diameter of Mark IV implants 3.8 mm in the in low bone apical part and density 4 mm in the cervical part
Mark II implants in normal bone density
Smokers excluded
NA
Maxilla
Fixed prosthesis
Markovic et al27
University of Belgrade, Serbia.
N=48
4.1-mm diameter and 10-mm length
Bone condensation in self-tapping and noneselftapping implants
Conventional drillings in self-tapping implants
Smokers excluded
NA
Maxilla
NA
Markovic et al28
University of Belgrade, Serbia.
N=102
4.1-mm diameter and 10-mm length
Bone condensation in self-tapping and noneself-tapping implants
Conventional drillings in self tapping implants.
Smokers excluded
NA
Maxilla
NA
VonWowern NA and Gotfredson29
N=2
NA
Ball and bar Ball and bar NA attachment in attachment in low bone density normal bone density
Complete denture
Anterior mandible
Acrylic overdentures with bar and ball attachment
Alghamdi et al20
27 implants in maxilla and 25 in mandible
4.1-mm diameter and 12-mm length
Undersized drilling in low bone density
NA
NA Maxilla and mandible, anteriorly and posteriorly
NA
3.75-mm diameter and various lengths
I/C or E/C
Standard drilling in normal bone density
Excluded patients having parafunctional habits (bruxers and clenching patients)
Metal reinforced acrylic overdentures with magnet or Locator attachments
Screw-retained permanent restoration(s) or bar-attached overdentures
C, comparator; E, exposure; I, intervention; NA, not available.
homogenous with similar comparisons and outcomes at similar time periods. Risk ratios (RRs) were combined for dichotomous data using random effects or a fixed effect model. A review manager (RevMan, v5.3; The Nordic Cochrane Centre) was used to perform meta-analysis. The 95% confidence interval (CI) was calculated simultaneously with the effect size estimate. Statistical heterogeneity was assessed by I2 and s2. Whenever s2 was >0, the random effects model was chosen. For each outcome and comparison, the body of evidence was assessed by I.A.R. and S.I. using the Grading of Recommendations Assessment,
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Development and Evaluation of group methodology (GRADE) tool.26 RESULTS By searching the electronic databases, 2621 references were retrieved in addition to 17 references identified through hand search, which resulted in a total of 2638 articles. The number of articles identified at the different review stages can be seen in the PRISMA flowchart (Fig. 1). The 11 included studies comprised 5 interventional and 6 observational studies. The interventional studies were either RCTs of parallel design (studies by
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Åstrand et al,4 Markovic et al,27,28 and Von Wowern and Gotfredson29) or an NRCT (study by Alghamdi et al20). The observational studies were 4 prospective cohort studies, (studies by Jaffin and Berman,8 Lauc et al,22 Temmerman et al,30 Chow et al31) and 2 retrospective cohort studies (studies by Holahan et al10,32). Seven studies compared low and normal bone densities, namely, all cohort studies and 1 RCT (study by Von Wowern and Gotfredson29), which compared different attachment systems in participants with low and normal bone density subgroups. Alghamdi et al20 compared undersized drilling in low bone density with standard drilling in normal bone density. Åstrand et al4 compared 2 implant designs, namely, the Brånemark System Mark II in normal bone density (placed in test and control groups) with the Brånemark System Mark IV in low bone density (placed in test group only). Markovic et al27,28 compared lateral bone condensation and standard drilling in individuals with low bone density. For Markovic et al,28 the effect size and its measure of dispersion for the following 3 interventions were calculated: bone condensation in self-tapping implants, bone condensation in noneself-tapping implants, and conventional drillings in self-tapping implants. The 3 interventions were considered as 1 special treatment and were compared with conventional drilling in noneself-tapping implants as a control group. The total number of participants in the 10 included studies was 1071. None of the included studies reported calculating sample size. The mean age of participants included in this systematic review was 62.4 years based on the average age of participants in the 10 studies that reported participants’ ages. Studies in this review included both sexes, except the Holahan et al10,32 and Temmerman et al30 studies, which were performed on a total of 794 women. The overall male-to-female ratio in this systematic review was 113:940, reflecting a higher prevalence of women. In one study8 the number of participants, their average age, and the male-to-female ratio were not reported. Instead, the number of jaws was reported (n=246). The total dropout calculated in this review was 158 participants, with a total of 97 implants in 7 studies4,10,20,22,28-32; 3 studies showed no dropouts.19,21,29 All included studies used delayed loading except that of Markovic et al,27,28 who used early loading and a 1-stage surgical protocol. None mentioned the type of teeth or occlusal concept used. Study characteristics of the included studies are shown in Table 1 and Supplemental Table 1. The results of implant stability, implant survival, and marginal bone loss are shown in Tables 2-4. Only 3 studies were included in 3 meta-analyses, namely, Lauc et al,22 Jaffin and Berman,8 and Chow et al.31 The remaining articles were not included in any metaanalysis for the reasons listed in Figure 1. Of all sought Radi et al
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outcomes, only 3 were reported in the included articles, namely, implant stability, implant survival/loss, and marginal bone loss. Implant stability was measured in the included articles with a resonance frequency instrument (Osstelll ISQ; Osstell) or with a torque wrench. Units of measurements are reported in Table 2. Temmerman et al30 found no significant difference between implant stability in low and normal bone density 15 months after implant placement (P=.163). Markovic et al27,28 found a significant difference between special and conventional techniques applied in participants low bone density. This was observed 0-12 weeks after implant placement (P<.001). Alghamdi et al20 reported no significant difference between undersized drilling in low bone density and standard drilling in normal bone density at the time of implant placement (P=.165 for the implant stability quotient (ISQ), and P=.685 for the insertion torque). The results of implant survival reported in 10 studies are presented in Table 3. Seven compared low and normal bone density.8,10,22,27,28,30,32 Three interventional trials compared special and conventional techniques.4,20,33 A significant difference in implant survival of participants with low and normal bone density was reported by Jaffin and Berman8 at 3 years and by Holahan et al32 (using the surgeon’s tactile sense and T score) 1, 3, 5, and 10 years after implant placement (P<.001). This difference was absent in Holahan et al10 (bone mineral density score), Von Wowern and Gotfredson,29 Temmerman et al,30 Lauc et al,22and Chow et al31 (per protocol analysis and best and worst case scenario). Markovic et al27 reported no significant difference between implant survival of special versus conventional techniques at a follow-up period of 6 months (P=1). Åstrand et al4 placed Mark II Brånemark dental implants in both the control group and the dense regions of the test group. Mark IV dental implants were placed in low bone density regions of the test group. The survival results of Mark II implants placed in the dense regions of the test group were not considered with the results of Mark II in the control group because this would have violated the randomization performed by the authors. The importance of implant design was reported by Åstrand et al4 and of undersized drilling by Alghamdi et al20; however, no significant difference was found between conventional techniques in normal bone density and special techniques in patients with low bone density 12 months after implant insertion (P=.180 and P=1, respectively). Marginal bone loss was reported in 4 studies: Chow et al,31 Temmerman et al,30 Åstrand et al,4 and Von Wowern and Gotfredsen.29 Temmerman et al30 (P=.01) and Von Wowern and Gotfredson29 (P=.013) reported a significant difference between marginal bone loss in participants with low and normal bone density 15 months
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Table 2. Results of implant stability (0, 4, 8, and 12 weeks) 0 Weeks I /E
4 Weeks
C P
8 Weeks
I /E
C
I /E
Mean ±SD
Mean ±SD
P
d
d
d
12 Weeks
C
I /E
C
P
Mean ±SD
Mean ±SD
d
70.6 ±8.8
73.8 ±6.5
Study/Unit of Measure
Mean ±SD
Mean ±SD
Temmerman et al30 (ISQ)
65.8 ±10.2
69.2 ±7.7
Markovic et al27 (ISQ)
74.03 ±3.53 61.20 ±1.63 <.001* 68.37 ±1.65 60.77 ±0.90 <.001*
Markovic et al28 (ISQ)
71.15 ±3.55 61.20 ±1.63 <.001*
Alghamdi et al20 (ISQ)
68.58 ±4.81 66.69 ±5.41 .165
d
d
d
d
d
Alghamdi et al20 (Ncm)
35.19 ±4.79 34.62 ±5.83 .685
d
d
d
d
d
.205
66.8 ±2.99
Mean ±SD Mean ±SD d
60.77 ±0.90 <.001*
d
d
d
d
d
69.99 ±1.9
66.03 ±0.4
<.001*
71.2 ±1.83
d
P .163 d
67.10 ±0.32 <.001*
C, comparator; I/E, intervention/exposure; ISQ, implant stability quotient (Osstell); SD, standard deviation. *Significant difference.
Table 3. Results of implant survival (1, 3, 5, and 10 years) 1 Year Poor Bone
3 Years
Normal Bone
Poor Bone
Normal Bone
5 Years Poor Bone
10 Years
Normal Bone
Poor Bone
Normal Bone
AR
P
AR
AR
P
AR
AR
P
AR
AR
P
Jaffin and Berman8 (Lekholm and Zarb)
d
d
d
d
d
d
66/102
923/952
<.001*
d
d
d
Lauc et al22 (Lekholm and Zarb)
d
d
d
d
d
d
83/92
86/92
.420
d
d
d
Chow et al31 (16 patients omitted, T score)
d
d
d
d
d
d
105/106
19/20
.422
d
d
d
Chow et al31 (16 patients with normal bone, T score)
d
d
d
d
d
d
105/106
51/52
.645
d
d
d
Chow et al31 (16 patients with osteoporotic patients, T score)
d
d
d
d
d
d
137/138
19/20
.395
d
d
d
50/51
85/85
d
d
d
d
d
d
d
AR
Study (Condition)
Temmerman et al30 Holahan et al32 (Surgeon’s sense)
.430
d
148 /168 2612/2695 <.001*
140/168
2557/2695 <.001* 68/168
d
2538/2695 <.001*
Holahan et al32 (T score)
d
d
d
1893/1998
804/865
.075
d
d
d
Holahan et al10 (BMD score)
d
d
d
d
d
d
d
d
d
68/168
2496/2695 <.001*
d
d
d
3204/3224 3207/3224 .620
Von Wowern and Gotfredson29
14/14
8/8
>.999
d
d
d
14/14
8/8
>.999
d
d
d
Åstrand et al4
94/97
51/51
.180
d
d
d
d
d
d
d
d
d
Markovic et al27 (Special technique versus conventional technique in low bone density)
24/24 24/24
d
>.999
d
d
d
d
d
d
d
d
d
Alghamdi et al20 (Undersized drilling in low bone density and standard drilling in normal bone density)
26/26
26/26
>.999
d
d
d
d
d
d
d
d
d
AR, absolute risk; BMD, bone mineral density. *Significant difference.
Table 4. Results of marginal bone loss (1, 5, and 7 years) 1 Year
Study (Type of Comparison) Chow et al31
5 Years
Low Bone Density M ±SD (mm)
Normal Bone Density M ±SD (mm)
d
d
P
Low Bone Density M ±SD (mm)
Normal Bone Density M ±SD (mm)
d
d
d
7 Years
P
Low Bone Density M ±SD (mm)
Normal Bone Density M ±SD (mm)
P
d
0.3 ±0.7
0.50 ±0.27
.855
Temmerman et al30
e0.11 ±0.49
0.05 ±0.52
.013
d
d
d
d
d
d
Åstrand et al4 (Radiographic picture; Mark IV implant in low bone density versus Mark II [Nobel Biocare AB, Gothenburg, Sweden] in normal bone density)
e0.29 ±0.10
e0.22 ±0.11
.130
d
d
d
d
d
d
d
d
d
0.47 ±0.22
0.01 ±0.15
.010*
d
d
d
Von Wowern and Gotfredson29 (Ball and bar)
M, mean in mm; SD, standard deviation. *Significant difference.
and 5 years after implant placement. Åstrand et al4 and Chow et al31 reported no significant difference in marginal bone loss of patients with normal and low bone density 1 year and 7 years after implant placement (P>.05). The 3 meta-analyses done in this systematic review were concerned with implant survival after 5 years in low
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versus normal bone density, where the RR was used to report the effect size between the different groups. They included 3 prospective cohort studies: Lauc et al,22 Jaffin and Berman,8 and Chow et al.31 In the study by Chow et al,31 data for implant survival were available for all 79 participants. The authors reported the failure of only 1 Radi et al
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Low Bone Density Total Events 105 106 66 102 83 92
Study or Subgroup Chow et al Jaffin and Berman Lauc et al Total (95% Cl)
Normal Bone Density Events Total 19 20 923 952 86 92
300
Risk Ratio Weight IV, Random, 95% Cl 33.8% 1.04 (0.94, 1.15) 31.7% 0.67 (0.58, 0.77) 34.5% 0.97 (0.89, 1.05)
1064
100.0%
Total events 1028 254 Heterogeneity: τ2=0.04; χ2=25.98, df=2 (P<.00001); I2=92% Test for overall effect: Z=1.10 (P=.27)
Risk Ratio IV, Random, 95% Cl
0.88 (0.70, 1.10)
0.5 0.7 1 Favors Normal Bone
1.5 2 Favors Low Bone
Chow 2016 (boss loss) Temmerman 2017 (boss loss) Alghamdi 2011 (implant survival and stability) Figure 3. Risk of bias summary: review authors’ judgments about each risk of bias item for each cohort study and nonrandomized clinical trial on outcome level.
implant in each group (low and normal bone density). For 16 patients, data on their classifications were not available, as reported by the authors when contacted. I.A.R. and S.I. decided to omit these patients once and to add them one time to the low bone density group and another time to the normal bone density group. Therefore, 3 meta-analyses were conducted for the same studies to examine the sensitivity of the results to adding those data. The results of the meta-analyses showed no significant differences between implant survival in the low and normal bone density
Radi et al
–
–
Astrand 2003 (implant survival)
?
?
+
+
–
+
–
Astrand 2003 (marginal bone loss)
?
?
?
?
–
+
–
Markovic 2011 (implant stability)
?
?
+
+
+
–
?
Markovic 2013 (implant stability)
–
?
+
+
–
–
?
von Wowern 2001 (implant survival)
?
?
+
+
+
+
?
von Wowern 2001 (marginal bone loss)
?
?
–
–
+
+
? Other bias
Temmerman 2017 (implant survival and stability)
–
Selective reporting (reporting bias)
Holsbso 2011 (implant survival)
+
Incomplete outcome data (attrition bias)
Holahan 2008 (implant survival)
+
Blinding of outcome assessment (detection bias)
Jaffin 1991 (implant survival)
?
Blinding of participants and personnel (performance bias)
Lauc 2000
?
Allocation concealment (selection bias)
Chow 2016
Astrand 2003 (implant stability)
Random sequence generation (selection bias)
Overall bias
Bias in selection of reported result
Bias in measurement of outcomes
Critical risk of bias
Bias due to missing data
Serious risk of bias
Bias due to confounding
Moderate risk of bias
Bias due to deviation from intended interventions
No information
Bias in classification of interventions
Low risk of bias
Bias in selection of participants into the study
Figure 2. Forest plot of implant survival after 5 years (data omitted). CI, confidence interval; IV, inverse variance test.
Figure 4. Risk of bias summary: review authors’ judgments about each risk of bias item for each randomized clinical trial on outcome level.
groups 5 years after implant placement before and after adding the missing data to the 2 studied groups: P=.27, RR=0.88, and 95% CI=0.70-1.10 when omitting the data; P=.17, RR=0.88, and 95% CI=0.73-1.06 when adding missing data to the normal bone density group; and P=.28, RR=0.88, and 95% CI=0.70-1.11 when adding missing data to the low bone density group. Because of the heterogeneity, the random effects model was used (Fig. 2). A risk of bias assessment of each domain for every included study on the outcome level is presented in Figures 3 and 4. In general, the 11 included studies showed
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Table 5. Implant survival in low versus normal bone density 5 years after implant placement Quality Assessment No. of Studies
Study Design
Risk of Bias
No. of Patients
Inconsistency Indirectness Imprecision
Normal Bone
Effect Size
Other Considerations
Poor Bone
RR (95% CI)
AR (95% CI)
All plausible residual confounding would reduce the demonstrated effect
245/300 (81.7%)
1028/1064 RR 0.88 (96.6%) (0.70 to 1.10)
116 fewer Very Low Critical per 1,000 (from 97 more to 290 fewer)
Strong association 254/300 all plausible (84.7%) residual confounding would reduce the demonstrated effect
1060/1096 RR 0.88 (96.7%) (0.73 to 1.06)
116 fewer Very Low Critical per 1,000 (from 58 more to 261 fewer)
1028/1064 RR 0.88 (96.6%) (0.70 to 1.11)
116 fewer Very Low Critical per 1,000 (from 106 more to 290 fewer)
Quality Importance
Implant survival: mean follow-up =5 years (omitted data), assessed with binary 3
Observational Very studies serious
Very serious
Not serious
Serious
Implant survival: mean follow-up =5 years (missing data normal bone density), assessed with binary 3
Observational Very studies serious
Very serious
Not serious
Serious
Implant survival: mean follow up =5 years (missing data low bone density), assessed with binary 3
Observational Very studies serious
Very serious
Not serious
Serious
Strong association 286/332 all plausible (86.1%) residual confounding would reduce the demonstrated effect
AR, absolute risk; CI, confidence interval; RR, risk ratio. Classification of bone density with different measurement techniques. Different prosthetic options, fixed or removable, provided in different articles. Implant systems and positions also different.
poor quality of evidence. The Lauc et al,22 Jaffin and Berman,8 Temmerman et al,30 and Chow et al31 studies were at critical risk, and the Holahan et al,10 Holahan et al,32 and Alghamdi et al20 studies were at serious risk. The Åstrand et al4 and Markovic et al27,28 studies were at high risk. The Von Wowern and Gotfredson29 study was assessed as being at high risk for marginal bone loss and at unclear risk for implant survival. DISCUSSION In this review, a quantitative comparison of implant survival in participants with low and normal bone density showed no significant difference 5 years after implant placement (P>.05). Descriptive analysis showed controversy regarding implant survival in individuals with low versus normal bone density. Merheb et al34 reported 100% implant survival in 3 groups of patients, osteoporotic, osteopenic, and healthy, and found no significant difference among them. Similar findings were reported in recent systematic reviews by Giro et al12 and de Medeiros et al.11 In a retrospective study with a 7-year follow-up,6 a higher implant failure rate was shown in patients with osteoporosis; 2 implants failed in 1 participant treated with oral bisphosphonates. Similarly, Becker et al7 found that sites with moderate to poor bone quality (D3 or D4) had 3.7 times greater implant loss versus sites with good bone quality (D1 or D2). Implant survival findings are further strengthened by the results of the marginal bone loss, where a significant difference between both exposure and control groups exists 5 years after implant placement (P=.01) and disappears 7 years later. Special
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techniques studied in this review (undersized drilling and implant design) seem to reduce the difference between low and normal bone density regarding implant stability, marginal bone loss, and implant survival 1 year after implant placement (P>.05). Regarding implant stability, only Temmerman et al30 reported no significant difference between participants with low and normal bone density in their prospective cohort study. Similarly, Merheb et al34 stated that the difference in stability was not significant among patients with osteopenia and osteoporosis and healthy individuals at the time of implant placement. This contradicts the findings of Turkyilmaz et al,35 who showed a statistically significant correlation between bone density and implant stability (r=0.882, P<.001). Their different findings could be attributed to discrepancies in the study design (retrospective cohort), implant site, and age and sex of the participants. Stability in patients with low bone density improved significantly with bone condensation if compared with conventional drilling (P<.001), especially in the first 3 months, when the lack of implant micromotion is an essential requirement for osseointegration. The quality of evidence regarding the special techniques is based on descriptive synthesis and is, therefore, unclear. The quality of evidence of the meta-analyses was assessed using GRADE, as shown in Table 5. The very low quality of evidence could be due to factors such as study design, critical risk of bias, wide CIs, and marked heterogeneity. The last could be attributed to the difference in how bone density was measured in the 3 included studies. Confounders like implant systems, their
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positions and prosthetic options, and materials also increased heterogeneity among studies. Limiting the language to English only might have caused language bias. Assessment of publication bias was also not possible; therefore, the risk of reporting bias remains unclear. Marked heterogeneity together with the wide CIs decreases certainty about the results and weakens the strength of recommendations. CONCLUSIONS Based on the findings of the 5-year implant survival meta-analysis, the following conclusions were drawn: 1. Implant therapy in patients with low bone density seems feasible with special precautions. 2. Implant placement using special techniques in low bone density regions might enhance implant stability. 3. The quality of evidence is still unclear. REFERENCES 1. Kanis JA, Burlet N, Cooper C, Delmas PD, Reginster JY, Borgstrom F, et al. European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 2008;19:399-428. 2. Lindsay R, Christiansen C, Einhorn TA, Hart DM, Ljunghall S, Mautalen CA, et al. Who are candidates for prevention and treatment for osteoporosis? Osteoporos Int 1997;7:1-6. 3. Reginster JY, Burlet N. Osteoporosis: a still increasing prevalence. Bone 2006;38:S4-9. 4. Åstrand P, Billström C, Feldmann H, Fischer K, Henricsson V, Johansson B, et al. Tapered implants in jaws with soft bone quality: a clinical and radiographie 1-year study of the Brånemark System Mark IV fixture. Clin Implant Dent Relat Res 2003;5:213-8. 5. Busenlechner D, Fürhauser R, Haas R, Watzek G, Mailath G, Pommer B. Long-term implant success at the Academy for Oral Implantology: 8-year follow-up and risk factor analysis. J Periodontal Implant Sci 2014;44: 102-8. 6. Niedermeier R, Stelzle F, Riemann M, Bolz W, Schuh P, Wachtel H. Implantsupported immediately loaded fixed full-arch dentures: evaluation of implant survival rates in a case cohort of up to 7 years. Clin Implant Dent Relat Res 2017;19:4-19. 7. Becker W, Hujoel PP, Becker BE, Willingham H. Osteoporosis and implant failure: an exploratory case-control study. J Periodontol 2000;71: 625-31. 8. Jaffin RA, Berman CL. The excessive loss of Branemark fixtures in type IV bone: a 5-year analysis. J Periodontol 1991;62:2-4. 9. Lekholm U, Zarb GA. Patient selection and preparation. Tissue integrated prostheses: osseointegration in clinical dentistry. Chicago: Quintessence Pub Co; 1985. p. 199-209. 10. Holahan 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. 11. de Medeiros FC, Kudo GA, Leme BG, Saraiva PP, Verri FR, Honório HM, et al. Dental implants in patients with osteoporosis: a systematic review with meta-analysis. Int J Oral and Maxillofac Surg 2017;17:31484-8. 12. Giro G, Chambrone L, Goldstein A, Rodrigues JA, Zenóbio E, Feres M, et al. Impact of osteoporosis in dental implants: a systematic review. World J Orthop 2015;6:311-5. 13. Alqutaibi AY, Radi IA. No clear evidence regarding the effect of osteoporosis on dental implant failure. J Evid Based Dent Pract 2016;16:124-6. 14. Al-Marshood MM, Junker R, Al-Rasheed A, Al Farraj Aldosari A, Jansen JA, Anil S. Study of the osseointegration of dental implants placed with an adapted surgical technique. Clin Oral Implants Res 2011;22:753-9. 15. Degidi M, Daprile G, Piattelli A. Influence of underpreparation on primary stability of implants inserted in poor quality bone sites: an in vitro study. J Oral Maxillofac Surg 2015;73:1084-8. 16. Fanuscu MI, Chang TL, Akça K. Effect of surgical techniques on primary implant stability and peri-implant bone. J Oral Maxillofac Surg 2007;65: 2487-91.
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45. de Souza JG, Neto AR, Dalago HR, de Souza JJ, Bianchini MA. Impact of local and systemic factors on additional peri-implant bone loss. Quintessence Int 2013;44:415-24. 46. Heo D, Heo YK, Lee JH, Lee JJ, Kim B. Comparison between cortical drill and cortical tap and their influence on primary stability of macro-thread tapered implant in thin crestal cortical bone and low-density bone. Implant Dent 2017;26:711-7. 47. Deporter DA, Todescan R, Nardini K. Use of a tapered, porous-surfaced dental implant in combination with osteotomes to restore edentulism in the difficult maxilla. Implant Dent 1999;8:233-9. 48. Bass SL, Triplett RG. The effects of preoperative resorption and jaw anatomy on implant success: a report of 303 cases. Clin Oral Implants Res 1991;2: 193-8. 49. Slagter KW, Raghoebar GM, Vissink A. Osteoporosis and edentulous jaws. Int J Prosthodont 2008;21:19-26. 50. Elsubeihi ES, Zarb GA. Implant prosthodontics in medically challenged patients: the University of Toronto experience. J Can Dent Assoc 2002;68:103-9. 51. Farré-Pagès N, Augé-Castro ML, Alaejos-Algarra F, Mareque-Bueno J, Ferrés-Padró E, Hernández-Alfaro F. Relation between bone density and primary implant stability. Med Oral Patol Oral Cir Bucal 2011;16:e62-7. 52. Munjal S, Hazari P, Mahajan H, Munjal A, Mehta DS. Evaluation of specifically designed implants placed in the low-density jaw bones: a clinicoradiographical study. Contemp Clin Dent 2015;6:40-3.
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53. Trullenque-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. 54. Fuh LJ, Huang HL, Chen CS, Fu KL, Shen YW, Tu MG, et al. Variations in bone density at dental implant sites in different regions of the jaw bone. J Oral Rehabil 2010;37:346-51. 55. Gay IC, Tran DT, Weltman R, Parthasarathy K, Diaz RJ, Walji M, et al. Role of supportive maintenance therapy on implant survival: a university-based 17 years retrospective analysis. Int J Dent Hyg 2016;14:267-71. 56. Toffler M. Site development in the posterior maxilla using osteocompression and apical alveolar displacement. Compend Contin Educ Dent 2001;22: 775-90. 57. Bustillo F, Kosinski T, Bachtell R. A preliminary study of 37 subperiosteal implant candidates with atrophic mandibles. J Oral Implantol 1985;12:218-27. Corresponding author: Dr Iman Abd-Elwahab Radi 11 ElSaraya St, ElManial 11553 EGYPT Email:
[email protected] Copyright © 2018 by the Editorial Council for The Journal of Prosthetic Dentistry.
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