Dental implants, compared to teeth, are less tolerable

Marginal Bone Loss Around Tilted Implants in Comparison to Straight Implants: A Meta-Analysis Alberto Monje, DDS 1 /Hsun-Liang Chan, DDS, MS 2 /Fernando Suarez, DDS 1 / Pablo Galindo-Moreno, DDS, PhD 3 /Hom-Lay Wang, DDS, MS, PhD 4 Purpose: The primary aim of this systematic review was to compare the amount of marginal bone loss around tilted and straight. As the secondary aim, the incidence of biomechanic complications was compared. Materials and Methods: An electronic literature search from five databases, for the years 2000 to 2011, and a hand search in implant-related journals were conducted. Clinical human studies in the English language that had reported marginal bone loss in tilted and straight at 12-months followup or longer were included. Mean marginal bone loss and the number of that were available for analysis were extracted from original articles for meta-analyses. Results: Eight (six prospective and two retrospective) studies were included. One-year data were available in seven articles, which included 1,015 (451 tilted). Three articles provided 3- to 5-year data from 302 (164 tilted). No significant difference in weighted mean marginal bone loss was found between the tilted and straight in the short and medium terms. Three articles reported the incidence of biomechanic complications. There was not enough information to make a comparison. Conclusions: This meta-analysis failed to support the hypothesis that tilted that were splinted for the support of fixed prostheses had more marginal bone loss. Additionally, there was not enough evidence to claim a higher incidence of biomechanic complications in tilted. However, due to the nature of the study design of the included articles, caution should be exercised when interpreting the results of this review. Int J Oral Maxillofac Implants 2012;27:1576 1583 Key words: edentulous, immediate dental implant loading, marginal bone loss, nonaxial loading, splinting, tilted implant Dental, compared to teeth, are less tolerable to traumatic occlusal forces due to the lack of periodontal ligaments. They are more vulnerable to nonaxial forces because of the higher moment, torsional, and shear forces exerted to the surrounding bone that damage the bone-to-implant contact surface. 1 As a result, should be placed in line to the direction of the loading. However, the proximity of anatomical structures, such as the maxillary sinus and 1 Visiting Scholar, Graduate Periodontics, Department of Periodontics and Oral Medicine, University of Michigan, School of Dentistry, Ann Arbor, Michigan, USA. 2 Adjunct Clinical Assistant Professor, Graduate Periodontics, Department of Periodontics and Oral Medicine, University of Michigan, School of Dentistry, Ann Arbor, Michigan, USA. 3 Associate Professor, Department of Oral Surgery, University of Granada, Granada, Spain. 4 Program Director, Professor, Graduate Periodontics, Department of Periodontics and Oral Medicine, University of Michigan, School of Dentistry, Ann Arbor, Michigan, USA. Correspondence to: Hsun-Liang Chan, Adjunct Clinical Assistant Professor and Research Fellow, University of Michigan, 1011 North University Avenue, Ann Arbor, Michigan 48109-1078, USA. Fax: (734) 936-0374. Email: hlchan@umich.edu the inferior alveolar nerve, often preclude standard from being placed axially. Solutions to inadequate ridge height include the use of short, 2 vertical ridge augmentation procedures, 3 or cantilever prostheses. 4 Although having a comparable shortterm survival rate, the long-term performance of short is less understood, especially in the posterior maxilla with lower bone density. 5,6 Vertical augmentation procedures increase patient morbidity and the outcome is unpredictable, especially when performed in the posterior mandible. 7 Cantilever prostheses might incur higher rates of prosthetic complications, such as abutment loosening and denture fracture. 8 10 Due to the unpredictable long-term prognosis associated with the above-mentioned procedures, the use of tilted was proposed. 11,12 The use of tilted could provide several clinical advantages: (1) to allow for the placement of longer, which increases the bone-to-implant contact area as well as implant stability; (2) to create a wider distance between anterior and posterior, which results in better load distribution; (3) to reduce or eliminate the use of cantilevers; and (4) to avoid bone augmentation procedures. 13 One example of using tilted is the All-on-Four technique in 1576 Volume 27, Number 6, 2012

which the fixed prosthesis is supported by two straight and two tilted in a fully edentulous mandible. 14 Four were splinted together and immediately restored with an acrylic provisional denture, which is replaced with a permanent porcelain prosthesis after 4 to 6 months. The same concept was adopted for the reconstruction of a fully edentulous maxilla and the implant survival rate at 1 year was similar to placed in the mandible (98.36% and 99.73%, respectively). 15 Although biomechanic complications are commonly reported, ranging from 15.6% 15 to 27%, 14 patient satisfaction remained high because any complications can be repaired at chairside. Therefore, combining tilted and straight for supporting fixed prostheses can be considered a viable treatment modality because of the high survival rate. 16 However, the stability of peri-implant tissue and, especially, the marginal bone level for these tilted has not been extensively studied. Unfavorable loading direction could cause more marginal bone loss around these. In vitro studies have suggested accentuated stresses around implant necks that were nonaxially placed. 17,18 In addition, it is not known if angled are associated with a higher incidence of biomechanic complications. For that reason, it is the primary aim of this systematic review to compare marginal bone loss between nonaxially and axially placed. The second aim is to assess whether tilted are related to a higher incidence of prosthetic complications. Materials and Methods A search of five electronic databases, including PubMed, Ovid (MEDLINE), EMBASE, Web of Science, and Cochrane Central for relevant studies published in English from January 2000 until July 2011 was performed by one examiner (AM). The search terms used, where mh represented the MeSH term and tiab represented the title or abstract, were: Mouth, Edentulous [mh] OR Jaw [mh] AND Dental [mh] OR ( Dental [tiab] AND Implants [tiab]) OR Dental Implants [tiab] OR ( Dental [tiab] AND Implant [tiab]) OR Dental Implant [tiab] OR Dental implantation [mh]) OR Immediate dental implant loading [mh] AND Tilted [tiab] OR Angled [tiab] OR Angulated [tiab] OR Offset [tiab] OR Non-axial [tiab] OR Axial [tiab] OR Axially OR Upright"[tiab] OR "Straight"[tiab] OR "All-on-4"[tiab] OR "All-on-four"[tiab]. Additionally, a hand search was carried out in dental and implant-related journals from January 2000 until July 2011, including Clinical Implant Dentistry and Related Research, Journal of Oral and Maxillofacial Implants, Clinical Oral Implants Research, Implant Dentistry, European Journal of Oral Implantology, Journal of Oral Implantology, International Journal of Oral and Maxillofacial Surgery, Journal of Oral and Maxillofacial Surgery, Journal of Dental Research, International Journal of Prosthodontics, Journal of Prosthetic Dentistry, Journal of Clinical Periodontology, Journal of Periodontology and The International Journal of Periodontics and Restorative Dentistry. Furthermore, a search in the references of included papers was conducted for publications that were not electronically identified. Studies were selected if they fulfilled the following inclusion criteria: human clinical studies, either prospective or retrospective, with data on comparison of marginal bone loss between tilted and straight ; a minimum sample size of 10 patients and 10 in each group that had been in function for at least 1 year; and that were placed in a pristine residual ridge with no additional grafting. Animal studies and human trials with insufficient information were excluded. Potential articles were reviewed in full text and confirmed for their eligibility by another examiner (HC). Data extracted from the selected studies and transported to a commercially available software (CMA, Biostat) for meta-analysis included: number of available for analysis and mean value and standard deviation of marginal bone loss. The contributions of each article to the primary outcome were weighed based on sample size and the random effect model was chosen. Publication bias was examined by the funnel plot in which standard deviations of the difference in mean marginal bone loss were plotted against the difference in mean from the included articles. As a second aim, the incidence of biomechanic complications, if reported in the included articles, was recorded separately for straight and tilted and compared. The reporting of this meta-analysis adhered to the PRISMA (Preferred Reporting Items for Systematic Review and Meta-Analyses) statement. 19 Results The screening process was presented in Fig 1. Initial screening of the databases using a combination of the above-mentioned key words, in addition to hand searching, yielded a total of 326 articles. After an evaluation of their titles and abstracts, 15 potentially relevant articles were selected for full-text evaluation. Seven articles were excluded because of several reasons: marginal bone loss was not reported, 11,12,20,21 no comparison of marginal bone loss between straight and tilted, 15 inclusion of immediate implant placement, 22 and inadequate sample size 23 (Table 1). Eight articles (numbered 1 to 8, as shown in Tables 2 and 3) fulfilled the inclusion criteria and were included in the meta-analysis. The International Journal of Oral & Maxillofacial Implants 1577

PubMed, Ovid (MEDLINE). EMBASE, Web of science, and Cochrane Central database searching. Limits: English language articles only. 326 records identified through database searching. 15 full-text articles assessed for eligibility. 8 studies included in qualitative synthesis. 8 studies included in quantitative synthesis. 311 records excluded based on exclusion/inclusion criteria. 7 full-text articles excluded: No report on marginal bone loss (n = 4); No marginal bone loss comparison (n = 1); Immediate implant placement (n = 1); Inadequate sample size (n = 1). Table 1 excluded Articles and Their Reasons for Exclusion Excluded article (y) Reason for exclusion Agliardi et al No comparison in marginal bone loss (2010) 15 Bedrossian Insufficient sample size et al (2008) 23 Francetti et al (2010) 22 Krekmanov et al (2000) 11 Inclusion of immediate implant placement No report on marginal bone loss Maló et al No report on marginal (2005) 12 bone loss Maló et al No report on marginal (2006) 20 bone loss Maló et al No report on marginal (2007) 21 bone loss Fig 1 Flow chart of the screening process. Table 2 Characteristics of the Included Studies with Report on Marginal Bone Loss at 1-year Follow-up # Authors (y) Study type No. of (T/S) No. of patients Implant location Degree of angulation of tilted Type of restoration No. of for FF Loading time (mo) 1 Agliardi et al P 42/42 24 Mandible 30 40 FF 4 Immediate (2010) 30 2 Aparicio et al R 40/53 25 Maxilla 35 FP NA 6 8 (2001) 39 3 Calandriello and P 22/32 18 Maxilla 45 75 FF or FP Mean: 5; Immediate Tomatis (2005) 40 range: 3 6 4 Capelli et al P 74/116 65 Mandible; (2007) 13 maxilla 25 35 FF Maxilla: 6; mandible: 4 Immediate 5 Degidi et al P 120/89 30 Maxilla 30 40 FF 7 Immediate (2010) 41 6 Hinze et al P 73/71 37 Mandible 30 FF 4 Immediate (2010) 42 Maxilla 7 Testori et al P 80/161 41 Maxilla 30 35 FF 6 Immediate (2008) 43 T = tilted implant; S = straight implant; P = prospective; R = retrospective; FF = fixed full-arch prosthesis; FP = fixed partial prosthesis; NA = not applicable. Significance level set at P <.05. Table 3 Characteristics of the Included Studies with Data on Marginal Bone Loss for More Than 1 Year No. of (T/S) Degree of angulation of tilted Study Follow up No. of Implant Type of Loading # Authors (y) type period (yr) patients location restoration time (mo) 2 Aparicio et al (2001) 39 R 5 11/12 NA Maxilla 35 FP 6 8 5 Degidi et al (2010) 41 P 3 120/89 30 Maxilla 30 40 FF Immediate 8 Koutouzis and R 5 33/36 38 Mandible (33%); 30 FP 3 6 Wennström (2007) 44 Maxilla (67%) T = tilted implant; S = straight implant; P = prospective; R = retrospective; FF = fixed full-arch prosthesis; FP = fixed partial prosthesis; NA = not applicable. Significance level set at P <.05. 1578 Volume 27, Number 6, 2012

SE 0.0 0.1 0.2 0.3 0.4 2.0 1.5 1.0 0.5 0.0 0.5 1.0 1.5 2.0 Difference in means (mm) Fig 2 Assessment of publication bias for short-term studies showed symmetrical distributions. Implant survival rate (%) (T/S) Marginal bone loss (mm) (T/S) P 100/100 0.80 ± 0.50/0.90 ±0.40 >.05 100/96.5 0.57 ± 0.50/0.43 ± 0.45 >.05 96.3/97 0.34 ± 0.76/0.82 ± 0.86 <.05 (favored tilted ) 98.6/98.2 0.82 ± 0.57/0.95 ± 0.50 >.05 100/100 0.63 ± 0.38/0.60 ± 0.33 >.05 94.6/96 0.76 ± 0.49/0.82 ± 0.31 >.05 98.8/98.8 0.80 ± 0.50/0.90 ± 0.40 >.05 Implant survival rate (%) (T/S) Marginal bone loss (mm) (T/S) P 95.2/96.3 1.21 ± 0.68/0.92 ± 0.55 >.05 100/100 1.03 ± 0.69/0.92 ± 0.75 >.05 NA 0.50 ± 0.95/0.40 ± 0.97 >.05 Characteristics of the Included Articles Study Design and Length of Follow-up. Of the eight articles included in the present study, six were prospective controlled studies (no. 1, 3, 4, 5, 6, and 7) and two were retrospective controlled studies (no. 2 and 8). In addition, three studies (no. 2, 5, and 8) provided data after a study period of 3 to 5 years. To further investigate the effect of time on marginal bone loss of tilted, two meta-analyses were performed for shortterm (1-year) and medium-term (3 to 5 years) results. Sample Size. The number of subjects that was available for data analysis ranged from 18 (no. 3) to 65 (no. 4). For short-term results, 1,015 were analyzed, in which 451 (44.43%) and 564 (55.57%) were tilted and straight, respectively. For comparison at 3- to 5-years follow-up, 164 (54.30%) tilted and 138 (45.70%) straight were analyzed, for a total of 302. Prosthesis Type, Loading Protocol, and Inclination of Implants. All were designed to support fixed prostheses. In other words, the tilted were splinted with straight. Five articles (no. 1, 4, 5, 6, and 7) studied full-arch prostheses only, another two (no. 2 and 8) included partial-arch prostheses only, and the last study (no. 5) had both types of prostheses. For full-arch reconstruction, four (two straight and two tilted) were used in the mandibles (no. 1, 4 and 6); in the maxilla, the number of ranged from four (no. 6), five (no. 3), six (no. 4 and 7) and seven (no. 5). Regarding the loading protocol, in six studies (no. 1, 3, 4, 5, 6, and 7) were loaded immediately; in the other two studies (no. 2 and 8), a conventional loading protocol was adopted. All tilted presented a similar angulation, ranging from 25 to 40 degrees, except in one study (no. 3), where the had a higher inclination of 45 to 75 degrees. Results of Meta-analyses The short-term results (Table 4) showed that the weighted mean difference in marginal bone loss between the tilted and straight was 0.054 mm (95% CI = 0.138 to 0.030 mm), favoring the tilted implant group; however, the difference did not reach statistical significance (P =.207). The funnel plot (Fig 2) showed overall symmetrical distribution, suggestive of no publication bias. For the medium-term results (Table 5), the weighted mean difference was 0.129 mm (95% CI = 0.041 to 0.298 mm), favoring the straight implant group, but was also not statistically significant (P =.137). Biomechanic Complications Only three articles (no. 2, 6, and 7) reported biomechanic complications (Table 6). Abutment screw loosening was the most commonly encountered The International Journal of Oral & Maxillofacial Implants 1579

Table 4 Forest Plot for the Comparison of Marginal Bone Loss between Tilted and Straight Implants at 1-Year Follow-up Sample size Statistics for each study Author (y)* Tilted Straight Difference in means (mm) SE Lower limit Upper limit Agliardi et al (2010) 30 42 42 0.100 0.100 0.296 0.096 Aparicio et al (2001) 39 40 53 0.140 0.100 0.056 0.336 Calandriello and 22 32 0.480 0.220 0.911 0.049 Tomatis (2005) 40 Capelli et al (2007) 13 74 116 0.130 0.080 0.287 0.027 Degidi et al (2010) 41 120 89 0.030 0.050 0.068 0.128 Hinze et al (2010) 42 73 71 0.060 0.070 0.197 0.077 Testori et al (2008) 43 80 161 0.100 0.060 0.218 0.018 Total 451 564 0.054 0.043 0.138 0.030 *Seven articles were included for meta-analysis and the mean difference was 0.054 mm (P =.207). SE = standard error. Table 5 Forest Plot for the Comparison of Marginal Bone Loss between Tilted and Straight Implants at Longer than 1-Year Follow-up Sample size Statistics for each study Author (y) Tilted Straight Difference in means (mm) SE Lower limit Upper limit Aparicio et al (2001) 39 11 12 0.290 0.260 0.220 0.800 Koutouzis and 33 36 0.100 0.230 0.351 0.551 Wennström (2007) 44 Degidi et al (2010) 41 120 90 0.110 0.100 0.086 0.306 Total 164 138 0.129 0.086 0.041 0.298 *Three articles were included for meta-analysis and the mean difference was 0.129 mm (P =.137). SE = standard error. Table 6 incidence of Biomechanic Complications on Tilted and Straight Implants # Type of prosthesis Prosthetic complication (%) Comparison between tilted and straight 2 FP Gold screw loosening (17.2); abutment screw loosening (48.3); abutment screw fracture (6.8); occlusal material fracture (6.8) 6 FF Acrylic provisional veneer fracture (10.8); definitive prosthesis fracture (3.7); Loosening of the screw access hole restoration (9.5) Screw loosening (6) No difference in % of screw loosening; no report on other type of complications No report 7 FF Provisional screw loosening (17.5) 3 tilted/4 axial #1, 3, 4, 5, 8: no report on the incidence of prosthetic complications. FP = fixed partial prosthesis; FF = fixed full-arch prosthesis. complication, occurring in 48.3% of the total number of prostheses (no. 2). Other prosthetic complications included screw fracture (6.8%) (no. 2), either provisional (10.8%) or permanent prosthesis fracture (3.7%) (no. 2 and 6), and loosening of the screw access hole restoration (9.5%) (no. 6). Regardless, no evidence from these three articles suggested that tilted incur a higher biomechanic complication rate. 1580 Volume 27, Number 6, 2012

Statistics for each study Relative weight P (%).317 11.59.162 11.59.029 3.39.104 14.99.549 21.96.391 17.07.096 19.41.207 100 Statistics for each study Relative weight P (%).265 11.06.664 14.14.271 74.80.137 100 Discussion Difference in means and 95% CI 1.0 0.5 0.0 0.5 1.0 Favor tilted Difference in means and 95% CI 1.0 0.5 0.0 0.5 1.0 Favor tilted Favors straight Favors straight In this systematic review, marginal bone loss was not statistically higher for tilted compared to straight in the short and medium terms. However, tilted lost more marginal bone in the medium term, contrary to the finding observed from the short-term data. Interestingly, one short-term study (no. 3) showed significantly less bone loss in tilted (0.34 ± 0.76 versus 0.82 ± 0.86, P =.03). These results suggested that tilted may have had continuous bone loss. A 10-year follow-up study 24 was recently published for evaluation of the All-on- Four concept; however, no data on marginal bone loss was available. Further studies are needed to look into the long-term performance of tilted. Theoretically, tilted could receive higher stresses resulting in more marginal bone loss. From computer-simulation studies, 17,18 higher stresses were found around the neck of tilted. Under vertical loading, the compressive stresses were five times higher around the angled implant. 17 In addition, tensile stresses were concentrated on the opposite side of the inclination. 25 As such, angled displayed oblique, nonhomogenous stress patterns to the polymeric model. 26 Animal studies 27,28 have shown that non-axial loading elicits a more dynamic remodeling of surrounding cortical bone and, in particular, trabecular bone. However, the hypothesis that there was more marginal loss around tilted was not supported by this meta-analysis, perhaps for the following reasons: (1) the length of the used was long and (2) the splinting effect. To engage more bone to maximize implant stability, most included studies utilized with a length of at least 10 and up to 20 mm (no. 2). With increasing implant length, more effective stress distributions for cancellous bone were found. 29 Another finite element study 30 suggested that longer distributed stress better, resulting in reduced gap distances between bone and implant. A prospective study 31 did report that long (14 to 16 mm) had significantly less marginal bone loss than average length (12 mm) at 1-year postloading. The comparable marginal bone loss for tilted could have been partially due to their long length. A more probable method to reduce stress around the neck of a tilted implant is splinting and reduction of the cantilever length rather than increasing the implant length. 32 34 In all cases included in the present review, tilted were splinted into a fixed prosthesis, either for a partial or full arch. The reduction of the cantilever span by tilted and the rigidity of the prostheses could have helped to reduce stress. Some recent three-dimensional finite element studies 33 36 suggested that tilted could benefit stress distribution by reducing cantilever length and, therefore, may be a viable option. These computersimulation studies could have partially explained the favorable marginal bone level around tilted. Prosthetic complications increase costs, treatment time, and frustration to patients as well as clinicians and should be avoided whenever possible. Due to the possibility of unfavorable loading conditions for tilted, it was hypothesized that tilted incurred higher biomechanic complications. Nevertheless, the present review did not have enough evidence to claim this statement because only three included articles reported prosthetic complication rates. Interestingly, one study (no. 2) reported an overall higher abutment loosening rate (48.3%) compared with the other two studies (no. 6 and 7), although no differences were found between tilted and straight. The type of restoration could be The International Journal of Oral & Maxillofacial Implants 1581

one explanation, ie, in that specific study, fixed partial prostheses were used, which do not provide the same cross-arch stability as fixed full prostheses. Implant marginal bone loss is primarily assessed by radiographs and the quality of radiographic methods could potentially influence the accuracy of the results. From the eight included articles, four (no. 4, 5, 7, and 8) performed standardized periapical radiographs exclusively. One article (no. 1) used standardized periapical radiographs whenever possible and panoramic films as an alternative. Another article (no. 6) only used panoramic radiographs and the remaining two articles did not mention if the periapical radiographs were standardized. Standardized periapical radiographs are generally desired because their accuracy can be within a range of 0.2 mm from the true measurement. 37 Panoramic radiographs are generally less preferred due to low resolution and an average distortion rate of 25%. 38 However, it is understandable that taking periapical radiographs could be difficult for edentulous patients with a shallow vestibule. Nevertheless, when interpreting the results, the radiographic methods used could pose an experimental limitation and should be taken into consideration. Conclusions Marginal bone loss around tilted that were splinted to support fixed prostheses was not significantly different from straight for the shortand medium-term reviews. However, tilted had slightly more marginal bone loss at the medium-term review. Long-term results are required to verify this finding. No evidence suggested that tilted are associated with a higher incidence of biomechanic complications. There is a potentially high risk of bias for this systematic review because none of the included articles was a randomized clinical trial. Therefore, precautions should be exercised when interpreting the results of this review. Acknowledgments The authors would like to acknowledge Mr Kerby A. Shedden, Associate Professor, Department of Statistics, University of Michigan, for his guidance in conducting meta-analyses, and Mr Mark MacEachern, a liaison services librarian in the Taubman Health Sciences Library, University of Michigan, for providing consultations on the literature search. The authors reported no conflicts of interest related to this study. This paper was partially supported by the University of Michigan Periodontal Graduate Student Research Fund. References 1. Kim Y, Oh TJ, Misch CE, Wang HL. Occlusal considerations in implant therapy: Clinical guidelines with biomechanical rationale. Clin Oral Implants Res 2005;16:26 35. 2. Fugazzotto PA. 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21. Malo P, de Araujo Nobre M, Lopes A. The use of computer-guided flapless implant surgery and four placed in immediate function to support a fixed denture: Preliminary results after a mean follow-up period of thirteen months. J Prosthet Dent 2007;97 (suppl 6):S26 S34. 22. Francetti L, Romeo D, Corbella S, Taschieri S, Del Fabbro M. Bone level changes around axial and tilted in full-arch fixed immediate restorations. Interim results of a prospective study. Clin Implant Dent Relat Res 2012 Oct;14:646-654. 23. Bedrossian E, Sullivan RM, Fortin Y, Malo P, Indresano T. Fixed-prosthetic implant restoration of the edentulous maxilla: A systematic pretreatment evaluation method. J Oral Maxillofac Surg 2008;66: 112 122. 24. Malo P, de Araujo Nobre M, Lopes A, Moss SM, Molina GJ. A longitudinal study of the survival of All-on-4 in the mandible with up to 10 years of follow-up. J Am Dent Assoc 2011;142:310 320. 25. Watanabe F, Hata Y, Komatsu S, Ramos TC, Fukuda H. 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