A 1-Year Prospective Clinical and Radiographic Study of Early-Loaded Bone Level Implants in the Posterior Maxilla Aleksa Markovic´, DDS, PhD;* Snježana Cˇolic´, DDS, PhD;† Miodrag Šc´epanovic´, DDS, PhD;‡ Tijana Mišic´, DDS, PhD;§ Ana Ðinic´, DDS;¶ Dinesh Sharma Bhusal, DDS, MSc**

ABSTRACT Purposes: The primary aim of the study was to investigate a 1-year success rate of early-loaded bone level implants with a chemically modified sand-blasted, large grit, acid-etched surface (SLActive®, Institut Straumann AG, Basel, Switzerland) in the posterior maxilla. Secondary objectives included stability of these implants and peri-implant bone level. Materials and Methods: Bone level® implants (Institut Straumann AG) inserted into premolar and/or molar maxillary sites were loaded after 6 weeks of healing. The implants were monitored for 1 year using the following outcome measures: implant success, primary and secondary stability, and peri-implant bone level. Results: Out of 37 implants placed in 13 patients, 36 reached sufficient stability and were early loaded, whereas one underwent a delayed loading protocol. One-year success rate of early-loaded implants was 100%. Implant stability at baseline was 71.7 1 5. 6 to be steadily increased thereafter up to 1 year (80.3 1 3.3), except at 2 weeks when a nonsignificant decrease was noticed (71.9 1 3.9). Continuous and significant bone loss was observed, reaching 0.4 1 0.1 mm in the first postoperative year. Conclusion: Bone level implants with the SLActive surface placed into low-density bone and loaded after 6 weeks of healing can predictably achieve and maintain a successful tissue integration. KEY WORDS: bone level implants, early loading, low-density bone, SLActive surface

BACKGROUND

contemporary oral implantology, in the face of patient demands for a shorter treatment time, has been focused on the critical healing time.2 Immediate or early loading of oral implants is a modern and successful treatment concept if some requirements are considered. Sufficient primary implant stability and implant surface characteristics have been recognized as the main factors affecting the treatment success when using immediate or earlyloaded implants for prosthetic treatment of partial or total edentulism.3 A high degree of primary implant stability is hard to achieve in low-density bone (type 4) and/or deficient bone volume potentially found in the posterior maxilla; therefore, these loading protocols are considered particularly challenging in this jaw region.2,3 The introduction of dental implants with adjusted macro design, thread geometry and self-tapping capacity, together with adopted surgical techniques (e.g., undersized drilling, bone condensing) that preserve as much bone volume as possible, provides increased implant stability and

Dental implant treatment that involves a conventional loading protocol providing 3 to 6 months of undisturbed healing is a clinically established treatment modality with very good prognosis.1 Research in

*Professor, Department of Oral Surgery, School of Dentistry, University of Belgrade, Belgrade, Serbia; †professor, Department of Oral Surgery, School of Dentistry, University of Belgrade, Belgrade, Serbia; ‡ assistant professor, Department of Prosthodontics, School of Dentistry, University of Belgrade, Belgrade, Serbia; §doctor, Department of Oral Surgery, School of Dentistry, University of Belgrade, Belgrade, Serbia; ¶doctor, Department of Oral Surgery, School of Dentistry, University of Belgrade, Belgrade, Serbia; **doctor, Department of Oral Surgery, School of Dentistry, University of Belgrade, Belgrade, Serbia Corresponding Author: Dr. Aleksa Markovic´, Department of Oral Surgery, School of Dentistry, University of Belgrade, Dr Subotica 4, 11 000 Belgrade, Serbia; e-mail: [email protected] © 2014 Wiley Periodicals, Inc. DOI 10.1111/cid.12201

1004

Bone Level Implants in the Posterior Maxilla

undisturbed bone healing in the regions with compromised bone quality.4–8 Implant surface is one of the determining factors that influence the biological events in peri-implant healing during the critical early stage of healing.9 Certain surface modifications including grit blasting, acid etching, anodization, plasma spraying, biomimetic calcium phosphate coatings, or incorporation of biologically active agents are able to promote faster bone healing.10 Titanium implants with increased surface roughness enhance cell adhesion, proliferation, and differentiation providing contact osteogenesis and improving the clinical performance to accelerate the bone healing and thereby allowing immediate or early loading protocols in areas with poor quality of bone.11,12 However, implant surface modifications affect not only its roughness but also the hydrophilicity. Two technologies have been commercially available to prepare hydrophilic dental implants: rinsing the titanium surface after the etching process under nitrogen protection, followed by storage in isotonic saline13 or chair-side treatment of dental implants with aqueous sodium hydroxide.14 Although the final histomorphometric outcome is equally and highly satisfactory for both hydrophobic and hydrophilic implant surfaces, a weak tendency toward increased bone apposition on the hydrophilic implant surfaces during early healing phase has been observed on animal and human models.15,16 A comprehensive systematic review including human clinical studies has proved that dental implants with different surface roughness and chemical characteristics placed into type 3 or type 4 bone of the posterior maxilla could be successfully loaded according to the immediate or early protocol.3 Recently introduced, SLActive® surfaces (Institut Straumann AG, Basel, Switzerland) are produced by coarse grit blasting with 0.25 to 0.5 mm corundum grit at five bars, followed by acid etching, afterwards rinsed under nitrogen protection to prevent exposure to air and then stored in a sealed glass tube containing isotonic NaCl solution. This surface treatment results in an Sdr value (surface enlargement due to surface topography as compared with a flat reference area) of 143%, Sa value (average height deviation from a mean plane) of 1.78 μm, and contact angle of 0°. Most in vitro and in vivo studies reported a strong bone response to SLActive implants particularly during early healing phase because of its nanostructure and hydrophilicity.17 Previ-

1005

ous studies have shown promising clinical outcome of early-loaded SLActive implants.18,19 The primary aim of this study was to investigate a 1-year success rate of early-loaded bone level® implants (Institut Straumann AG) with a chemically modified sand-blasted, large grit, acid-etched implant (SLActive) in the posterior maxilla. Secondary objectives included implant stability and peri-implant bone level (PBL). MATERIALS AND METHODS The 1-year prospective clinical and radiographic study was conducted at the Clinic of Oral Surgery School of Dentistry, University of Belgrade, from January 2010 to September 2012. The study was approved by the Ethics Committee, School of Dentistry, University of Belgrade (No. 36/10). Eligible patients were between 25 and 70 years of age, unilaterally/bilaterally and partially edentulous in the premolar/molar region of the maxilla, with subantral alveolar ridge height of at least 12 mm, ridge width of 6 mm, bone type 3 or 4 (Lekholm & Zarb classification),20 and natural teeth as antagonists. The following exclusion criteria were set: general conditions that contraindicated implant surgery; pregnancy or lactation; substance abuse; need for bone or soft tissue augmentation procedures; signs of untreated periodontitis or other mucosal and bone tissue lesions; history of radiation therapy in the region of implantation; heavy clenching or bruxism; and poor oral hygiene. Alternative treatments, possible risks, complications, and benefits related to implant surgery were explained to all patients. Written informed consent was obtained from all participants before any study-related procedure was performed. Implant treatment was planned using cone beam computed tomography (CBCT) images (Galileos, Sirona, Bensheim, Germany). Periodontal, endodontal, and open caries lesions were treated prior to implant placement. All patients received careful oral hygiene instruction and training in self-performed plaque control measures. One hour prior to surgery, each patient received 2 g of amoxicillin or 0.6 g of clindamycin (in the case of penicillin allergy).21 The surgical treatment was performed under local anesthesia using 2% lidocaine with 12.5 mg/ml adrenaline (Xylestesin®, 3M ESPE Dental AG, Seefeld, Germany) through a one-stage approach. In the posterior maxilla, a mucoperiosteal flap was raised, and the implant site

1006

Clinical Implant Dentistry and Related Research, Volume 17, Number 5, 2015

was prepared using a pilot drill followed by a series of drills with increasing diameters, in intermittent manner, under copious irrigation of saline at flow rate 100 ml/ min and drill speed 400 rpm, with strict adherence to the manufacturer’s recommended protocol. During drilling, the quality (1–4) of jawbone at recipient site(s) was assessed according to criteria proposed by Lekholm and Zarb.20 Bone level implants with the SLActive surface, 10 mm in length and 4.1 mm in diameter, were inserted using a torque of 35 Ncm. As all patients included in this study had bone class 3 or 4, the implants were inserted in a self-tapping way in accordance with manufacturer’s recommendation. Nonsubmerged healing abutments were placed, and the surgical wounds were closed with interrupted sutures. Postoperatively, analgesics were prescribed, and instructions on diet and oral hygiene were given. The sutures were removed after 1 week. Six weeks after implantation, implants that reached an implant stability quotient (ISQ) value of at least 65 as measured by resonance frequency analysis (RFA, Osstell Mentor®, Integration Diagnostics AB, Göteborg, Sweden) were loaded. All patients were rehabilitated by means of a provisional restoration, temporarily cemented for 4 months. After 4 months, final porcelainfused-to-metal crowns or bridges were made and temporarily cemented for 1 year (Telio® CS Cem Implant, Ivoclar Vivadent, Schaan, Liechtenstein), after which they were definitively cemented. Implants with insufficient stability after 6 weeks needed an additional healing period and were therefore excluded from the study. The primary outcome of this study was implant success defined according to the criteria by Buser and colleagues22 as follows: (1) absence of persistent subjective complaints (pain, foreign body sensation, dysesthesia); (2) absence of recurrent infection; (3) absence of mobility; and (4) absence of continuous radiolucency (evaluated after 6 weeks, 4 and 12 months of implant placement). The secondary outcomes of this study included primary and secondary implant stability as well as vertical PBL. Implant stability was assessed immediately after implant placement (primary stability) and then weekly up to 6 weeks as well as after 4 months and 1 year (secondary stability) by RFA using the Osstell Mentor apparatus. For implant stability measurements following implant loading, restorations were removed from the

implants. A transducer (Smart Peg® type 54, Osstell, Integration Diagnostics AB, Göteborg, Sweden) vertically attached to the implant was magnetically stimulated using the probe from two directions: perpendicularly to the jaw line for one measurement and in line with the jaw for the other measurement. The displayed ISQ values ranging from 1 to 100 (lowest to highest stability) reflected the degree of implant stability. The peri-implant vertical bone level was measured immediately after implant placement (baseline) and after 6 weeks, and 4 and 12 months postoperatively from the retroalveolar radiographs. The sulcus formers were attached to the implants prior to every radiographic exposure. In order to provide reproducible projection geometry in the different follow-up points, radiographs were taken using a long-cone paralleling technique and a customized film holder made from a commercial x-ray film holder (Dentsply®, Mölndal, Sweden) and a silicone key (Zeta plus, Zhermack® SpA, Badia Polesine, Italy). Scanned and digitized radiographs were imported in the Ray Mage® (Cefla Group, Imola, Italy) software and calibrated according to the known intraosseous implant length with regard to magnification. The implant shoulder and marginal crestal bone level on the mesial and distal sides of the implant were used as a reference points for the peri-implant vertical bone level measurements. The mean of values measured at mesial and distal aspects was accepted as an authentic value. All measurements were performed by the same independent outcome assessor. Adverse events (allergic reaction, implant mobility, implant fracture, maxillary sinus membrane perforation, severe hematoma, severe swelling, severe pain, hyperplasia, or gingival recession), deviations from the protocol, and withdrawals were also recorded. Statistical analysis was performed using SPSS 18.0 software (SPSS, Chicago, IL, USA). The statistical unit of observation was the implant. Outcome variables were described using measures of central tendency (mean, median) and of dispersion (minimum, maximum, standard deviation, 95% confidence interval). Frequency analysis was performed for PBL. Onesample Kolmogorov–Smirnov test was used to assess the normality of data distribution. The dynamic of changes in implant stability and PBL were analyzed using repeated measures of analysis of variance. p Values of less than 0.05 were considered statistically significant.

Bone Level Implants in the Posterior Maxilla

1007

TABLE 1 Distribution of Implants Used in the Study Patient’s Gender

Bone Density

Jaw Region

Female

Male

Type 3

Type 4

PM1

PM2

M1

M2

11

26

10

27

6

12

15

4

Implants

PM1-first maxillary premolar; PM2-second maxillary premolar; M1-first maxillary molar; M2-second maxillary molar.

RESULTS Thirteen eligible patients with a mean age of 47.1 (range 33–57) years received a total of 37 implants (Table 1). Between one and five implants were inserted per patient according to the prosthetic indication. Deviation from the study protocol was required for one implant (single-tooth replacement) inserted into the region of the second maxillary molar of a male patient aged 55 years with unremarkable medical history as poor stability at baseline (49 ISQ) as well as at 6 weeks (52 ISQ) were recorded. This implant required a two-stage protocol and was therefore excluded from the study and successfully restored using a delayed loading approach (68 ISQ at implant loading). The remaining 36 implants were early loaded after 6 weeks of healing, and all completed the 1-year follow-up. Data from these 36 implants were used for the analysis. Implant Success At the end of the follow-up, all 36 implants fulfilled the success criteria resulting in 100% 1-year success rate. Implant Stability At baseline, the mean ISQ value was 71.7 1 5.6, indicating high primary implant stability (Table 2). Afterwards,

a nonsignificant increase of ISQ was observed in the first postoperative week (72.3 1 4.1) followed by a nonsignificant decrease recorded in the second week (71.9 1 3.9) but with values that did not fall below baseline (Table 2, Figure 1). From the third week, implant stability steadily increased up to 1 year when the highest mean ISQ (80.3 1 3.3) was observed (Table 2, Figure 1). This increase in implant stability over time reached statistical significance 4 and 6 weeks postoperatively as well as after 4 months (Figure 1). ISQ values recorded at each observation time were higher compared with baseline, with a statistically significant difference after 6 weeks (Figure 1). PBL The radiographic analysis performed at loading (6 weeks) indicated a significant mean bone loss of 0.3 1 0.1 mm from baseline (Table 3, Figure 2). Afterwards, continuous and statistically significant bone loss was observed with a mean PBL of −0.3 1 0.0 mm after 4 months and −0.4 1 0.1 after 12 months (Table 3, Figure 2). Frequency analysis of PBL after 1-year follow-up showed bone loss of 0.5 mm or higher around only two implants (Figure 3).

TABLE 2 Descriptive Statistics of Implant Stability during 1-Year Follow-Up ISQ Descriptive Statistics Time

Baseline 1 week 2 weeks 3 weeks 4 weeks 5 weeks 6 weeks 4 months 6 months 1 year

Mean

Median

SD

Min

Max

95% CI

71.7 72.3 71.9 73.0 74.1 74.8 75.9 78.3 79.5 80.3

74 73 73 73 74 75 76 79 80 80

5.6 4.1 3.9 4.0 4.1 3.9 3.7 3.5 3.2 3.3

58 60 62 64 65 66 67 67 70 73

80 80 80 81 81 82 83 85 85 85

69.8–73.7 70.8–73.7 70.6–73.3 71.6–74.4 72.7–75.5 73.4–76.1 74.6–77.2 77.1–79.4 78.4–80.6 79.2–81.4

CI = confidence interval; ISQ = implant stability quotient; SD = standard deviation.

1008

Clinical Implant Dentistry and Related Research, Volume 17, Number 5, 2015

Figure 1 Changes in implant stability during the first year. Line represents mean, error bars represent 95% CI of mean. Asterisks indicate a statistically significant difference between two consecutive weeks: *p 2 0.0005 (95%CI: −1.7 to −0.4 ); **p 2 0.0005 (95%CI: −1.7 to −0.6); ***p = 0.014 (95%CI: −4.4 to −0.3). Crosses indicate a statistically significant difference to baseline (implant placement): +p = 0.001 (95%CI: −7.1 to −1.2); ++p 2 0.0005 (95%CI: −9.2 to −3.8); +++p 2 0.0005 (95%CI: −11.0 to −4.4); ++++p 2 0.0005 (95%CI: −12.1 to −5.0).

DISCUSSION In the present study, bone level implants with the SLActive surface were placed in the bone type 3 or 4 of posterior maxilla and loaded 6 weeks after surgery. At the end of the 1-year follow-up, all 36 implants fulfilled

Figure 2 Changes in peri-implant bone level during the first year. Line represents mean; asterisks indicate a statistically significant difference between two consecutive time points: *p 2 0.0005 (95%CI: 0.2 to 0.3); **p 2 0.0005 (95%CI: 0.1 to 0.1); ***p 2 0.0005 (95%CI: 0.1 to 0.1). Crosses indicate a statistically significant difference to baseline (implant placement): +p 2 0.0005 (95%CI: 0.2 to 0.3); ++p 2 0.0005 (95%CI: 0.3 to 0.4); +++p 2 0.0005 (95%CI:0.4 to 0.5).

the success criteria, resulting in implant survival rate of 100%, indicating successful functional early loading without an increased risk of failure inspite of lowdensity bone. Similarly, Roccuzzo and Wilson reported a 100% 1-year implant survival rate of early-loaded SLActive implants in posterior maxilla.19 In the prospective randomized 3-year study of Nicolau and colleagues,23 early loading of 178 SLActive implants, of which 40.3% was placed into bone type 3/4, resulted in 96.7% implant survival rate and no implant failures in bone type 4 suggesting that bone quality had no significant effect on survival rate of nanostructured and

TABLE 3 Descriptive Statistics of PBL during 1 Year Follow-Up PBL Descriptive Statistics Time

6 weeks 4 months 1 year

Mean

Median

SD

Min

Max

95% CI

−0.3 −0.3 −0.4

−0.3 −0.4 −0.4

0.0 0.0 0.1

−0.4 −0.4 −0.5

−0.2 −0.2 −0.3

−0.3 to 0.3 −0.4 to 0.3 −0.4 to 0.4

CI = confidence interval; PBL = peri-implant bone level; SD = standard deviation.

Bone Level Implants in the Posterior Maxilla

1009

Figure 3 Frequency analysis of peri-implant bone level during the first year.

hydrophilic implants. The survival rates for early-loaded bone level SLActive implants are in line with those reported for other implant systems with different macro design and surface properties.3 Sullivan and colleagues24 published a 5-year survival rate of 99.19% for 123 Osseotite implants (Biomet, Warsaw, IN, USA) loaded 2 months after placement into posterior maxilla. Turkyilmaz and colleagues25 presented a 4-year implant survival rate of 95.2% for 21 TiUnite implants (Nobel Biocare AB, Göteborg, Sweden) placed into premolar and molar maxillary regions and early loaded (6 weeks). Results of multicenter study of Cochrane and colleagues26 including 990 SLA implants placed into posterior maxilla and loaded after 6 weeks revealed a 5-year survival rate of 99.3%. Clinical studies in healthy patients have shown superior osteogenesis, angiogenesis, and histomorphometric characteristics of the nanostructured and hydrophilic SLActive surface compared with its predecessor, microstructured and hydrophobic SLA implant surface, during the critical early period of osseointegration.16,17,27 This biological response to the increased roughness and wettability of the implant surface results in enhanced stability of SLActive implants that can be successfully used in either

immediate or early loading treatment protocols, even in low-density bone.17,18,28–30 As implant stability has been recognized as a prerequisite for the success of dental implant therapy, many methods have been developed for measuring it. Some of these techniques, such as cutting torque resistance analysis and reverse torque test, can be used only intra or postoperatively, so they are not suitable for long-term evaluation of implant stability. Additionally, reverse torque test is found to be destructive31 and unable to quantify degree of osseointegration, so its use is mainly confined to experimental studies.32 RFA is a noninvasive diagnostic method that analyzes the first resonance frequency of a small transducer attached to an implant fixture or an abutment.33 RFA evaluates implant stability as a function of the stiffness of the implant-bone interface, and it can supply clinically relevant information about the state of the implant-bone interface at any stage of the treatment or at follow-up examinations.34 In the present study, we used RFA measurements as an indicator of healing events in periimplant bone department to clinically monitor the course of osseointegration next to hydrophilic SLActive implants in low-density bone. ISQ values increased from baseline through the follow-up period, except

1010

Clinical Implant Dentistry and Related Research, Volume 17, Number 5, 2015

between the weeks 1 and 2 when decrease was nonsignificant. Previous experimental research demonstrated that in areas of primary mechanical stability at the pitch of the implant threads, osseointegration first occurred after bone resorptive processes, thereby disrupting mechanical stability for a short period of time.35 Previous studies also reported an initial decrease in ISQ values for the implants with hydrophobic surface within the first 3 to 4 weeks of healing,36–38 which could be explained by bone remodeling processes in the peri-implant region. Interesting finding is the time frame in which this breakpoint (change from decreasing to increasing stability) occurs. We identified the breakpoint in the second postoperative week indicating that afterwards, formative processes predominated over the resorptive one within bone remodelling. This result suggests that nanostructured and hydrophilic SLActive implant surface promotes enhanced bone formation during the early stage of osseointegration. Our clinical result has been supported by experimental findings of Buser and colleagues13 who has shown that increased surface roughness as well as wettability and surface-free energy significantly increase the bone-toimplant contact (BIC value) as early as after 2 weeks following implant placement providing reduced healing time. In addition, Ferguson and colleagues39 reported higher implant stability during the critical early weeks of osseointegration of the nanostructured and hydrophilic SLActive implants compared with microstructured and hydrophobic implants using removal torque test in adult miniature pigs. These results suggest benefits of SLActive implant surface regarding accelerated achievement of implant stability required for early loading protocol. Histometric study of Lang and colleagues16 using a human model demonstrated significantly higher BIC values for SLActive compared with SLA implants after 2 and 4 weeks of healing with a BIC of 62% in 4 weeks, indicating degree of osseointegration sufficient to fully carry functional load. However, after 6 weeks of healing, both implant surfaces expressed similar and favorable histomorphometric outcome suggesting conditions for early loading.16 In addition to our study focusing on nanostructured and hydrophilic SLA surface, several clinical studies proved successful implantation of immediate or early loading protocol for hydrophobic implant surfaces with microtopography in demanding clinical situations such as low-density bone.3

In the literature, ISQ values between 60 and 65 were recommended for sufficient stability to initiate the restoration of an implant, whereas an ISQ value of 45 or below was a “warning sign” indicating implant failure and requiring an additional healing time.40 We set the threshold implant stability of 65 ISQ at the time of loading for single, nonsplitting implant. After 6 weeks of healing, we measured implant stability between 67 and 83 ISQ (mean 75.9, SD 3.7). Thirty-six out of 37 implants were loaded after they reached stability of at least 65 ISQ. Achievement of these high RFA values in the present study might be explained by the mutual effect of the nanotopography and enhanced surface-free energy as well as hydrophilicity of the SLActive implant surface and the bone level implant design.41 Similarly, previous research reported high ISQ values after a 6-week long observation period, which was a reliable criterion for early loading of SLActive implants.29 Our results showed a statistically significant increase in ISQ values between 3 and 4 weeks, as well as between 5 and 6 weeks and between 6 weeks and 4 months after surgery. These changes of RFA values over time can be explained by the osseointegration and remodeling process occurring around the peri-implant bone.36,40 A similar outcome was reported in another study where a significant change in the pattern of implant stability was noted after 3 weeks.36 In contrast to the present findings, a previous study reported no statistically significant structural changes of RFA values in measurement intervals, although the typical RFA course (decrease and a subsequent increase) was noted.42 Furthermore, in the present study, a statistically significant difference in ISQ values from baseline was observed after 6 weeks (at the loading time) and 4, 6, and 12 months after surgery. In previous clinical research, authors also reported that mean RFA values of SLActive implants at the loading stage were significantly higher than RFA values at the surgical stage,42 but in this study, loading in the maxilla was performed after 12 weeks of healing. Bornstein and colleagues43 monitored early-loaded SLActive implants placed into posterior mandible of 40 partially edentulous patients using the RFA method. They recorded steady increase of ISQ values from 74.3 at the time of implant placement to 83.8 at week 26. A lack of decreasing trend in their study might be explained by the selected time points for RFA measurements as the first two measurements occurred on day 0 and week 3,

Bone Level Implants in the Posterior Maxilla

skipping the gap at critical week 2. Slightly higher ISQ values reported in their study compared with the present one could be because of the higher bone density of the posterior mandible than posterior maxilla with formerly providing superior bone anchorage. In the present study, mean PBL was significantly different between each consecutive time point during the evaluation time. A statistically significant difference from baseline was also demonstrated after 6 weeks, and 4 and 12 months. Similar outcomes were reported in another study despite implants being loaded after a reduced healing period of only 21 days.44 The present results showed that mean PBL in the loading stage was −0.3 1 0.1 mm, decreasing to −0.4 1 0.1 mm after 1 year, which was similar to the results reported in the previous clinical trial.42 Higher mean PBL (0.6 1 1.0 mm) after 12 months was obtained in earlier research where SLActive implants were used, and early loading after 28 to 34 days was performed.18 Similar results were previously reported from 5-month follow-up data of the same study cohort.30 The results of the present research demonstrated that only 1% of the implants had periimplant bone loss higher than 0.5 mm after 1 year. In one of the earlier studies, no implant showed a bone loss greater than 1 mm, but there were seven implants with bone resorption between 0.6 and 1 mm.44 Also, in another study, 3.2% of the implants with bone loss higher than 2 mm were identified.18 The interim results of the same study cohort also reported a low frequency of bone loss higher than 2 mm.30 Other clinical trials also reported little bone loss for the bone level implant design. A recent multicenter study reported mean marginal bone loss of 0.5 1 0.6 mm in a 1-year analysis, which is consistent with the findings of this clinical research.43 Another study reported mean marginal bone loss of 0.2 1 0.2 mm after 3 years.45 Other commercially available dental implants with various macro design and surface properties when placed into maxilla and early loaded demonstrated marginal bone loss within the scope of a successful outcome as well. Fischer and colleagues46 reported mean marginal bone loss of 1.1 1 1.0 mm for 53 oxidized tapered implants of which 23 were placed into type 3 or 4 bone of maxilla and loaded within 16 days. Roccuzzo and Wilson47 revealed marginal bone loss of 0.5 1 0.6 mm based on 36 SLA implants inserted into maxillary molar regions and early loaded.

1011

In conclusion, the results of this prospective, 1-year study suggest that Straumann bone level implants can predictably achieve and maintain successful tissue integration in low-density bone after undergoing an early loading protocol. Additional clinical studies with a larger sample size and a longer observation period are needed to confirm these findings. ACKNOWLEDGMENTS The authors acknowledge Institut Straumann AG, Basel, Switzerland who kindly supplied the materials used in this research (KCA60). The authors declare no conflict of interests and have no affiliations to the products or companies mentioned in this article. REFERENCES 1. Branemark PI, Hansson BO, Adell R, et al. Osseointegrated implants in the treatment of the edentulous jaw. Experience from a 10-year period. Scand J Plast Reconstr Surg Suppl 1977; 16:1–132. 2. Esposito M, Grusovin MG, Willings M, Coulthard P, Worthington HV. The effectiveness of immediate, early, and conventional loading of dental implants: a Cochrane systematic review of randomized controlled clinical trials. Int J Oral Maxillofac Implants 2007; 22:893–904. 3. Roccuzzo M, Aglietta M, Cordaro L. Implant loading protocols for partially edentulous maxillary posterior sites. Int J Oral Maxillofac Implants 2009; 24(Suppl):147– 157. 4. Markovic A, Calvo-Guirado JL, Lazic Z, et al. Evaluation of primary stability of self-tapping and non-self-tapping dental implants. A 12-week clinical study. Clin Implant Dent Relat Res 2013; 15:341–349. 5. Markovic A, Calasan D, Colic S, Stojcev-Stajcic L, Janjic B, Misic T. Implant stability in posterior maxilla: bonecondensing versus bone-drilling: a clinical study. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2011; 112:557– 563. 6. Wu SW, Lee CC, Fu PY, Lin SC. The effects of flute shape and thread profile on the insertion torque and primary stability of dental implants. Med Eng Phys 2012; 34:797– 805. 7. Ostman PO, Hellman M, Wendelhag I, Sennerby L. Resonance frequency analysis measurements of implants at placement surgery. Int J Prosthodont 2006; 19:77–83, discussion 84. 8. O’Sullivan D, Sennerby L, Meredith N. Measurements comparing the initial stability of five designs of dental implants: a human cadaver study. Clin Implant Dent Relat Res 2000; 2:85–92.

1012

Clinical Implant Dentistry and Related Research, Volume 17, Number 5, 2015

9. Palmquist A, Omar OM, Esposito M, Lausmaa J, Thomsen P. Titanium oral implants: surface characteristics, interface biology and clinical outcome. J R Soc Interface 2010; 7(Suppl 5):S515–S527. 10. Le. Guehennec L, Soueidan A, Layrolle P, Amouriq Y. Surface treatments of titanium dental implants for rapid osseointegration. Dent Mater 2007; 23:844–854. 11. Novaes AB Jr, de Souza SL, de Barros RR, Pereira KK, Iezzi G, Piattelli A. Influence of implant surfaces on osseointegration. Braz Dent J 2010; 21:471–481. 12. Sennerby L, Gottlow J. Clinical outcomes of immediate/early loading of dental implants. A literature review of recent controlled prospective clinical studies. Aust Dent J 2008; 53(Suppl 1):S82–S88. 13. Buser D, Broggini N, Wieland M, et al. Enhanced bone apposition to a chemically modified SLA titanium surface. J Dent Res 2004; 83:529–533. 14. Tugulu S, Lowe K, Scharnweber D, Schlottig F. Preparation of superhydrophilic microrough titanium implant surfaces by alkali treatment. J Mater Sci Mater Med 2010; 21:2751– 2763. 15. Vasak C, Busenlechner D, Schwarze UY, et al. Early bone apposition to hydrophilic and hydrophobic titanium implant surfaces: a histologic and histomorphometric study in minipigs. Clin Oral Implants Res 2013. DOI: 10.1111/ clr.12277 16. Lang NP, Salvi GE, Huynh-Ba G, Ivanovski S, Donos N, Bosshardt DD. Early osseointegration to hydrophilic and hydrophobic implant surfaces in humans. Clin Oral Implants Res 2011; 22:349–356. 17. Wennerberg A, Galli S, Albrektsson T. Current knowledge about the hydrophilic and nanostructured SLActive surface. Clin Cosmet Investig Dent 2011; 3:59–67. 18. Ganeles J, Zollner A, Jackowski J, ten Bruggenkate C, Beagle J, Guerra F. Immediate and early loading of Straumann implants with a chemically modified surface (SLActive) in the posterior mandible and maxilla: 1-year results from a prospective multicenter study. Clin Oral Implants Res 2008; 19:1119–1128. 19. Roccuzzo M, Wilson TG Jr. A prospective study of 3 weeks’ loading of chemically modified titanium implants in the maxillary molar region: 1-year results. Int J Oral Maxillofac Implants 2009; 24:65–72. 20. Lekholm U, Zarb GA. Patient selection and preparation. In: Branemark PI, Zarb GA, Albrektsson TS, eds. Proceedings of the Tissue-Integrated Prosthesses: Osseointegration in clinical dentistry. Chicago: Quintessence, 1985:199–210. 21. Esposito M, Worthington HV, Loli V, Coulthard P, Grusovin MG. Interventions for replacing missing teeth: antibiotics at dental implant placement to prevent complications. Cochrane Database Syst Rev 2010; Jul:CD004152. DOI: 10.1002/14651858.CD004152.pub3

22. Buser D, Mericske-Stern R, Bernard JP, et al. Long-term evaluation of non-submerged ITI implants. Part 1: 8-year life table analysis of a prospective multi-center study with 2359 implants. Clin Oral Implants Res 1997; 8:161– 172. 23. Nicolau P, Korostoff J, Ganeles J, et al. Immediate and early loading of chemically modified implants in posterior jaws: 3-year results from a prospective randomized multicenter study. Clin Implant Dent Relat Res 2013; 15:600–612. 24. Sullivan D, Vincenzi G, Feldman S. Early loading of Osseotite implants 2 months after placement in the maxilla and mandible: a 5-year report. Int J Oral Maxillofac Implants 2005; 20:905–912. 25. Turkyilmaz I, Avci M, Kuran S, Ozbek EN. A 4-year prospective clinical and radiological study of maxillary dental implants supporting single-tooth crowns using early and delayed loading protocols. Clin Implant Dent Relat Res 2007; 9:222–227. 26. Cochran D, Oates T, Morton D, Jones A, Buser D, Peters F. Clinical field trial examining an implant with a sand-blasted, acid-etched surface. J Periodontol 2007; 78:974–982. 27. Donos N, Hamlet S, Lang NP, et al. Gene expression profile of osseointegration of a hydrophilic compared with a hydrophobic microrough implant surface. Clin Oral Implants Res 2011; 22:365–372. 28. Oates TW, Valderrama P, Bischof M, et al. Enhanced implant stability with a chemically modified SLA surface: a randomized pilot study. Int J Oral Maxillofac Implants 2007; 22:755– 760. 29. Markovic A, Colic S, Drazic R, Gacic B, Todorovic A, Stajcic Z. Resonance frequency analysis as a reliable criterion for early loading of sandblasted/acid-etched active surface implants placed by the osteotome sinus floor elevation technique. Int J Oral Maxillofac Implants 2011; 26:718–724. 30. Zollner A, Ganeles J, Korostoff J, Guerra F, Krafft T, Bragger U. Immediate and early non-occlusal loading of Straumann implants with a chemically modified surface (SLActive) in the posterior mandible and maxilla: interim results from a prospective multicenter randomizedcontrolled study. Clin Oral Implants Res 2008; 19:442–450. 31. Meredith N. Assessment of implant stability as a prognostic determinant. Int J Prosthodont 1998; 11:491–501. 32. Atsumi M, Park SH, Wang HL. Methods used to assess implant stability: current status. Int J Oral Maxillofac Implants 2007; 22:743–754. 33. Meredith N, Alleyne D, Cawley P. Quantitative determination of the stability of the implant-tissue interface using resonance frequency analysis. Clin Oral Implants Res 1996; 7:261–267. 34. Sennerby L, Meredith N. Implant stability measurements using resonance frequency analysis: biological and biomechanical aspects and clinical implications. Periodontol 2000 2008; 47:51–66.

Bone Level Implants in the Posterior Maxilla

35. Berglundh T, Abrahamsson I, Lang NP, Lindhe J. De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res 2003; 14:251–262. 36. Huwiler MA, Pjetursson BE, Bosshardt DD, Salvi GE, Lang NP. Resonance frequency analysis in relation to jawbone characteristics and during early healing of implant installation. Clin Oral Implants Res 2007; 18:275–280. 37. Han J, Lulic M, Lang NP. Factors influencing resonance frequency analysis assessed by Osstell mentor during implant tissue integration: II. Implant surface modifications and implant diameter. Clin Oral Implants Res 2010; 21:605–611. 38. Valderrama P, Oates TW, Jones AA, Simpson J, Schoolfield JD, Cochran DL. Evaluation of two different resonance frequency devices to detect implant stability: a clinical trial. J Periodontol 2007; 78:262–272. 39. Ferguson SJ, Broggini N, Wieland M, et al. Biomechanical evaluation of the interfacial strength of a chemically modified sandblasted and acid-etched titanium surface. J Biomed Mater Res A 2006; 78:291–297. 40. Glauser R, Sennerby L, Meredith N, et al. Resonance frequency analysis of implants subjected to immediate or early functional occlusal loading. Successful versus failing implants. Clin Oral Implants Res 2004; 15:428–434. 41. Rupp F, Scheideler L, Olshanska N, de Wild M, Wieland M, Geis-Gerstorfer J. Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces. J Biomed Mater Res A 2006; 76: 323–334. 42. Karabuda ZC, Abdel-Haq J, Arisan V. Stability, marginal bone loss and survival of standard and modified

43.

44.

45.

46.

47.

1013

sand-blasted, acid-etched implants in bilateral edentulous spaces: a prospective 15-month evaluation. Clin Oral Implants Res 2011; 22:840–849. Bornstein MM, Hart CN, Halbritter SA, Morton D, Buser D. Early loading of nonsubmerged titanium implants with a chemically modified sand-blasted and acid-etched surface: 6-month results of a prospective case series study in the posterior mandible focusing on peri-implant crestal bone changes and implant stability quotient (ISQ) values. Clin Implant Dent Relat Res 2009; 11:338–347. Morton D, Bornstein MM, Wittneben JG, et al. Early loading after 21 days of healing of nonsubmerged titanium implants with a chemically modified sandblasted and acid-etched surface: two-year results of a prospective two-center study. Clin Implant Dent Relat Res 2010; 12:9–17. Buser D, Wittneben J, Bornstein MM, Grutter L, Chappuis V, Belser UC. Stability of contour augmentation and esthetic outcomes of implant-supported single crowns in the esthetic zone: 3-year results of a prospective study with early implant placement postextraction. J Periodontol 2011; 82:342–349. Fischer K, Backstrom M, Sennerby L. Immediate and early loading of oxidized tapered implants in the partially edentulous maxilla: a 1-year prospective clinical, radiographic, and resonance frequency analysis study. Clin Implant Dent Relat Res 2009; 11:69–80. Roccuzzo M, Wilson T. A prospective study evaluating a protocol for 6 weeks’ loading of SLA implants in the posterior maxilla: one year results. Clin Oral Implants Res 2002; 13:502–507.