Abstract
The aim of this study was to determine the influence of patient-related systemic risk factors (systemic disease, genetic traits, chronic drug or alcohol consumption, and smoking status) on peri-implant bone loss at least 1 year after implant installation and prosthetic loading. An electronic search was performed of MEDLINE, EMBASE, and The Cochrane Central Register of Controlled Trials up to January 2012. One thousand seven hundred and sixty-three studies were identified. After applying a three-stage screening process, 17 articles were included in the qualitative analysis, but only 13 in the quantitative analysis, since smoking was a common exposure. The meta-analysis of these 13 studies (478 smokers and 1207 non-smokers) revealed a high level of heterogeneity and that smoking increases the annual rate of bone loss by 0.164 mm/year. Exposure to smoking had a harmful effect on peri-implant bone loss. However, the level of evidence for oral implant therapy in patients with systemic conditions is very low. Future studies should be improved in order to provide more robust data for clinical application.
The achievement of osseointegration is a biological concept already adopted in implant dentistry. The long-term maintenance of bone around an osseointegrated implant is paramount to clinical success, and peri-implant bone remodelling has commonly been expressed in terms of survival rates. It is believed that several factors may affect peri-implant bone resorption: local, surgical, implant, post-restorative, and patient-related risk factors, which include systemic diseases, genetic traits, chronic drug or alcohol consumption, and smoking status. Nevertheless, there is uncertainty around some factors. As an example, the results of a number of in vitro studies that aimed to investigate the association between specific interleukin 1 (IL-1) gene polymorphisms and peri-implant diseases were unclear ; this later generated further methodological problems. On the other hand, other factors have been identified as a risk. It has been observed that smokers have a higher risk of dental implant failure than non-smokers, with an increased risk for patients with a history of treated periodontitis.
Diabetes is considered a relative contraindication for dental implant treatment. The success rates improve by 85–95% with the eradication of co-morbidities (poor oral hygiene, cigarette smoking, and periodontitis), stabilization of glycaemic control (glycated haemoglobin (HbA1c) around 7%), and preventive measures against infection. Implant failure in patients using oral/intravenous bisphosphonates to treat osteoporosis is a subject that remains controversial. In a recent systematic review, only two out of 10 selected papers demonstrated a negative impact of bisphosphonates on implant success. Moreover, no scientific data are available to sufficiently support any specific treatment protocol for the management of bisphosphonate-related osteonecrosis of the jaws (BRONJ). Finally, although the ravages of cancer therapy are well-known, implants can osseointegrate and remain functionally stable in oral cancer patients who have undergone radiotherapy and chemotherapy.
Nevertheless, the current goals of implant therapy include long-term function, the capability to maintain good oral hygiene at home (even in posterior areas of the oral cavity), and overall aesthetics. In cases of implant survival, it is very important to address how much bone is lost over time radiographically. Furthermore, there is a lack of results on peri-implant soft tissue outcomes (bleeding on probing, plaque index, gingival recession, and width of keratinized tissues).
The aim of the present study was to review, in a systematic manner, the influence of systemic risk factors on peri-implant bone loss.
Materials and methods
Study protocol
The recommendations of the PRISMA statement were followed for the review process.
Focused question
The question in focus was ‘In patients undergoing dental implant treatment, what is the influence of systemic risk factors (systemic disease, genetic traits, chronic drug or alcohol consumption, and smoking status) on the occurrence of peri-implant bone loss at least 1 year after implant installation and prosthetic loading?’
Eligibility criteria
The following inclusion criteria were applied: (1) English language publications; (2) randomized controlled clinical trials, controlled clinical trials, cohort studies, case–control studies, and case series with at least five patients (in order to include as many studies as possible); (3) human subjects presenting systemic risk factors (systemic disease, genetic traits, chronic drug or alcohol consumption, and smoking status); (4) intervention involving dental implants and/or immediate loading of dental implants; (5) studies reporting on radiographic peri-implant bone level changes assessed by means of intraoral or panoramic X-rays; and (6) follow-up of at least 1 year after implant placement and prosthetic loading (to avoid the risk of false-positive measurements of peri-implant bone loss due to bone remodelling in the first 3–6 months after implant placement, or early implant loss due to surgical procedures).
The following were exclusion criteria: (1) letters, reviews, and unpublished data; (2) patients with acute medical conditions that could contraindicate implant therapy (acute infection, severe bronchitis or emphysema, severe anaemia, uncontrolled diabetes, uncontrolled hypertension, abnormal liver function, nephritis, severe psychiatric disease, conditions with a severe risk of haemorrhage, endocarditis, and myocardial infarction); and (3) studies reporting only implant failure, survival, and/or success rates.
Study selection
Information sources and the search strategy are available in the Supplementary Material, available online.
A three-stage screening process was performed independently by two reviewers (MC and PHOR). Initially, all titles were screened to eliminate non-related publications and reviews. During the second stage, all selected abstracts were analyzed and the full-text articles were consequently retrieved. Then, all reference lists of the selected studies, relevant reviews, and studies from the ‘grey literature’ were screened for additional papers that might meet the eligibility criteria of this systematic review. In the third stage, selected articles were analyzed. Any disagreements between the two reviewers were resolved after additional discussion with a third reviewer (LC). The inter-reviewer reliability of the data extraction was calculated by determining the percentage of agreement and the correlation coefficient (kappa, 5% level of significance). In addition, study authors were contacted for incomplete or missing data when necessary.
Heterogeneity of the outcome
In order to evaluate the heterogeneity of the outcome between the selected studies, the following factors were recorded: (1) study design; (2) duration of follow-up; (3) number, mean age (range), and gender of subjects; (4) numbers and types of dental implants; (5) type of prosthetic unit; (6) systemic risk factor affecting the study population; (7) measurement of bone level changes (in mm); and (8) peri-implant soft tissue outcomes (bleeding on probing, plaque index, gingival recession, and width of keratinized tissues).
Risk of bias
Two reviewers (MC and PHOR) assessed the methodological quality using the forms ‘quality assessment of a cohort study’ and ‘quality assessment of a randomized clinical trial’, combining the proposed criteria of the MOOSE statement, STROBE statement, and PRISMA. These two validity tools consist of eight and nine items, respectively, which have to be scored with a plus, a minus, or a question mark. In accordance with Telleman et al., it was decided that studies scoring four or more plusses were methodologically acceptable. The two observers, who were blinded to the author, institute, and journal, independently generated a score for the articles. Any disagreement was resolved with a third reviewer (LC).
Data analysis and synthesis
The meta-analysis was based on the DerSimonian and Laird method. The weighted mean difference (WMD) was expressed for bone loss under a randomized effects model. WMD estimations were accompanied by the 95% confidence interval (95% CI) of the standard error and the P -value of the distinction of a null effect of the smoking factor (WMD = 0) for the solution of the meta-analysis, including the statistical value of association Q A . The statistical Q H value for heterogeneity and the relative P -value for the χ 2 test were both included. At the same time, the index I 2 was also calculated, considered as representative of the total variation due to heterogeneity. A forest plot was obtained for better visualization of the results, and a funnel plot was drawn to assess potential publication bias. The software used to perform this meta-analysis was Sinergy 3.2 (Biometrics Department, GlaxoSmithKline). All analyses were conducted with a 5% level of significance.
Results
Study selection
The search identified 1763 references up to January 2012. A further 160 references were retrieved from other sources and cross-checked references, giving a total 1923 studies. After duplicates were removed, 1824 references were available for screening. Of these, 254 publications fulfilled the eligibility criteria; however a further 237 studies were excluded, as most of them did not report on peri-implant bone loss. After qualitative assessment of the 17 selected studies (16 cohort studies and one randomized controlled trial (RCT)), only 13 studies were included in the quantitative synthesis (meta-analysis) ( Fig. 1 ). Agreement in study selection between the reviewers was 89.53% (kappa value = 0.46).
Study characteristics
Table 1 gives a detailed description of the studies included, which were published from 1996 to 2011; most reported between 2 and 5 years of follow-up (range 6 months to 20 years ). A total of 1883 patients and 5730 implants were analyzed. Cigarette and tobacco smoking were the most prevalent exposures (identified as single factors in 11 studies). The others were osteoporosis, IL-1 gene polymorphisms, diabetes, endocrine diseases, cardiac diseases, and arthritis, and Sjögren’s syndrome. Radiographic bone loss was evaluated by means of intraoral apical X-rays in 11 studies, panoramic X-rays in four studies, and both methods were used in two studies. Only a few studies reported soft tissue outcomes (bleeding on probing, plaque index, gingival recession, and width of keratinized tissues). Bleeding on probing was considered in one study, the plaque index in three studies, and the pocket probing depth in three studies. No study reported data for peri-implant gingival recession or width of keratinized tissues.
| Author, year (Ref.) | Title | Design/setting | Follow-up time | Number of patients | Number of implants | Single or multiple prosthetic unit | Systemic factor | Peri-implant bone loss (mm) | Soft tissue outcomes |
|---|---|---|---|---|---|---|---|---|---|
| Haas et al., 1996 | The relationship of smoking on peri-implant tissue: a retrospective study | Retrospective Smokers with dental implants Non-smokers with dental implants BS, IMZ implants (both groups) |
S = 22.4 months NS = 21.9 months |
S = 107 NS = 314 |
S = 366 NS = 1000 |
FPD, OD (both groups) | Cigarette smoking | Mean values (peri-apical) S = 3.95 Max, 1.97 Mand NS = 1.64 Max, 1.32 Mand |
Mean values (Max/Mand): S: PI 0.96/1.12; BI 1.75/0.70; PPD 4.32/2.31; MI 1.0/0.46 NS: PI 0.60/1.1; BI 0.85/0.89; PPD 2.78/2.37; MI 0.38/0.47 |
| Isidor et al., 1999 | Outcome of treatment with implant-retained dental prostheses in patients with Sjögren syndrome | Case series BS dental implants (6 per patient) Dental arches with poor denture retention/stability |
4 years | 8 | 54 | Multiple OD, complete, FSP |
Sjögren’s syndrome | Mean radiographic bone loss (peri-apical) < 1.0 (0–4 years) | PI (1 year): 0.4 PI (4 years): 0.3 |
| Carlsson et al., 2000 | Long-term marginal peri-implant bone loss in edentulous patients | Prospective Duplicated data from Lindquist et al. (1996 and 1997) |
15 years | 44 | 273 | FxMd prostheses (15 mm = bilateral cantilever) | Cigarette smoking | Mean values (peri-apical), Max/Mand S = 1.0/1.25 NS = 0.7/0.63 |
No report |
| Geurs et al., 2001 | Retrospective radiographic analysis of sinus graft and implant placement procedures from the Academy of Osseointegration Consensus Conference on Sinus Grafts | Retrospective Sinus grafts (7 types) and implant placement Selected patients, digitized panoramic radiographs |
3 years | 100 (145 sinus grafts) | S = 55 NS = 266 |
No report | Tobacco smoking | Mean loss in sinus graft height on panoramic radiographs S = 1.75 NS = 1.36 |
Not possible (only radiographs were analyzed) |
| von Wowern and Gotfredsen, 2001 | Implant-supported overdentures, a prevention of bone loss in edentulous mandibles? A 5-year follow-up study | Prospective follow-up AST, two-stage implant placement Mandibular OD 11 patients (bar attachment) 11 patients (ball attachment) |
5 years | 22 (18 women) OP: S = 2, NS = 5 NOP: S = 6, NS = 5 |
44 (2 per patient) | OD | Osteoporosis Cigarette smoking |
MBL (standard, peri-apical radiographs) OP = 0.47 NOP = 0.01 |
GI: OP = 0.29, NOP = 0.57 PI: OP = 0.07, NOP = 0.20 |
| Feloutzis et al., 2003 | IL-1 gene polymorphism and smoking as risk factors for peri-implant bone loss in a well-maintained population | Retrospective Heavy smokers, moderate smokers, previous smokers, non-smokers IL-1A (+4845) and IL-1B (+3954) |
5.6 years | HS = 14 MS = 14 FS = 23 NS = 39 |
119 IL-1-neg 56 IL-1-pos |
No report | IL-1 polymorphisms Cigarette smoking |
ABL: IL-1-neg = 0.45; IL-1-pos = 0.215 Peri-apical, long-cone ABL (median values): HS = 1.98; MS = ?; FS = 0.24; NS = 0.18; NS = 0.07 IL-1-pos, 0.36 IL-1-neg |
Reported, but not divided by smoking groups |
| Gruica et al., 2004 | Impact of IL-1 genotype and smoking status on the prognosis of osseointegrated implants | Retrospective Smokers (light, heavy), non-smokers, former light smoker, former heavy smoker IL-1A (+4845) and IL-1B (+3954) |
8 years | 53 127 (64 = IL-1-pos) |
292 | No description | IL-1 polymorphisms Cigarette smoking |
Mean change (1–8 years) (peri-apical radiographs) NS = 0.21; FLS = 0.13; FHS = −0.014; LS = 0.38; HS = 0.08 |
No report |
| Peñarrocha et al., 2004 | Radiologic study of marginal bone loss around 108 dental implants and its relationship to smoking, implant location, and morphology | Retrospective Single or partial tooth loss in maxilla and mandible Solid ITI dental implants (SLA) |
1 year | 42 (total) S = 16 NS = 26 |
S = 47 (total) G1: n = 18 G2: n = 18 G3: n = 11 NS = 61 |
Single and multiple prosthetic units | Cigarette smoking | Mean bone loss (peri-apical radiographs) G1: 1–10 cig/day, 0.59 G2: 11–20 cig/day, 0.91 G3: >20 cig/day, 0.89 NS = not reported |
No report |
| Galindo-Moreno et al., 2005 | Influence of alcohol and tobacco habits on peri-implant marginal bone loss: a prospective study | Prospective BS, IMTEC (TPS), Calciteck (HA) |
3 years | 185 S = 63 NS = 122 |
514 S = ? NS = ? |
Fixed prosthesis, OD, single crowns | Tobacco smoking | MBL (digital panoramic radiographs) S = 1.36 NS = 1.25 |
No report |
| Nitzan et al., 2005 | Impact of smoking on marginal bone loss | Retrospective Different implants used |
S = 42.9 months NS = 48.4 months |
S = 59 NS = 102 |
S = 271 NS = 375 |
No report | Cigarette smoking | MBL (panoramic radiographs) S = 0.15 NS = 0.047 |
No report |
| DeLuca and Zarb, 2006 | The effect of smoking on osseointegrated dental implants. Part II: peri-implant bone loss | Retrospective Consecutive complete or partially edentulous patients BS implants |
20 years | 235 | 767 | Single, multiple, and OD | Endocrine diseases, cardiac diseases, and arthritis Cigarette smoking |
Mean bone loss (peri-apical), following the first year of clinical loading S2 = 0.07 NS2 = 0.04 |
No report |
| Norton, 2006 | Multiple single-tooth implant restorations in the posterior jaws: maintenance of marginal bone levels with reference to the implant–abutment microgap | Retrospective Missing posterior teeth, some cases with sinus grafts AST dental implants |
3 years | S = 7 NS = 47 |
173 S = ? NS = ? |
Multiple, freestanding prostheses | Smoking | Mean bone loss (peri-apical) S = 0.77 (0.1–1.6) NS = 0.63 (0–2.7) |
Purulent exudate (1 implant) Apical infection (2 implants) |
| Herzberg et al., 2006 | Implant marginal bone loss in maxillary sinus grafts | Retrospective Patients with the need of a dental implant and maxillary sinus grafts cpTi and HA-coated dental implants |
6–56.5 months (mean 21.7 months) | 60 | S = 56 NS = 104 |
No report | Cigarette smoking | Mean bone loss (panoramic or intraoral) S = 0.24/year NS = 0.09/year |
Two patients with swelling and sinus membrane perforations |
| Sanna et al., 2007 | Immediately-loaded CAD–CAM manufactured fixed complete dentures using flapless implant placement procedures: a cohort study of consecutive patients | Prospective At least 1 completely edentulous arch BS (TiUnite) immediately loaded dental implants |
5 years (mean 2.2 years) | S = 13 NS = 17 |
212 | Multiple Complete, fixed supported prostheses |
Cigarette smoking | Mean bone loss after 4 years (digital panoramic radiographs) S = 2.6 (25 implants) NS = 1.3 (22 implants) |
No report |
| Tandlich et al., 2007 | Removable prostheses may enhance marginal bone loss around dental implants: a long-term retrospective analysis | Retrospective BioCom, rough-surface dental implant |
≥30 months | S = 17 NS = 65 |
265 | Single ( n = 63); multiple ( n = 52); OD (ball) ( n = 22) | Osteoporosis Diabetes Cigarette smoking |
BLRate (panoramic or peri-apical): S = 0.065 NS = 0.05 |
No report |
| Sánchez-Pérez et al., 2007 | Tobacco as a risk factor for survival of dental implants | Retrospective Consecutive patients Screw-taped, sandblasted, acid-etched dental implants (Bis) |
5 years | S = 40 NS = 26 |
S = 95 NS = 70 |
No report | Cigarette smoking | Retroalveolar radiographs, parallel technique MBL1: S = 2.7; NS = 2.78 MBL2: S = 2.41; NS = 3.13 |
PPD S = 3.0 NS = 2.5 |
| Stoker et al., 2012 | Long-term outcomes of three types of implant-supported mandibular overdentures in smokers | Randomized controlled clinical trial 36 patients (2IBA group) 37 patients (2ISB group) 37 patients (4ITB group) One-stage ITI/Bonefit dental implants |
8.3 years | 110 baseline 103 for analysis after follow-up |
256 | OD | Smoking | Mean bone loss (long-cone) S: 2IBA = 1.53; 2ISB = 1.17; 4ITB = 2.46 NS: 2IBA = 0.7; 2ISB = 0.83; 4ITB = 1.24 |
PPD (overall) 2IBA: 3.1 2ISB: 3.5 4ITB: 3.6 |
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