Correlation between Initial BIC and the Insertion Torque/Depth Integral Recorded with an Instantaneous Torque-Measuring Implant Motor: An in vivo Study Paolo Capparé, MD, MFS;* Raffaele Vinci, MD, MFS, DMD;† Danilo Alessio Di Stefano, DDS;† Tonino Traini, DDS, PhD;‡ Giuseppe Pantaleo, PhD;§ Enrico Felice Gherlone, MD, DMD;¶ Giorgio Gastaldi, MD, DMD**
ABSTRACT Background: Quantitative intraoperative evaluation of bone quality at implant placement site and postinsertion implant primary stability assessment are two key parameters to perform implant-supported rehabilitation properly. A novel micromotor has been recently introduced allowing to measure bone density at implant placement site and to record implant insertion-related parameters, such as the instantaneous, average and peak insertion torque values, and the insertion torque/depth integral. Purpose: The aim of this study was to investigate in vivo if any correlation existed between initial bone-to-implant contact (BIC) and bone density and integral values recorded with the instrument. Materials and Methods: Twenty-five patients seeking for implant-supported rehabilitation of edentulous areas were consecutively treated. Before implant placement, bone density at the insertion site was measured. For each patient, an undersized 3.3 × 8-mm implant was placed, recording the insertion torque/depth integral values. After 15 minutes, the undersized implant was retrieved with a 0.5 mm-thick layer of bone surrounding it. Standard implants were consequently placed. Retrieved implants were analyzed for initial BIC quantification after fixation, dehydration, acrylic resin embedment, sections cutting and grinding, and toluidine-blue and acid fuchsine staining. Correlation between initial BIC values, bone density at the insertion site, and the torque/depth integral values was investigated by linear regression analysis. Results: A significant linear correlation was found to exist between initial BIC and (a) bone density at the insertion site (R = 0.96, explained variance R2 = 0.92) and (b) torque/depth integral at placement (R = 0.81, explained variance R2 = 0.66). Conclusions: The system provided quantitative, reliable data correlating significantly with immediate postinsertion initial BIC, and could therefore represent a valuable tool both for clinical research and for the oral implantologist in his/her daily clinical practice. KEY WORDS: bone density, bone to implant contact, dental implant, histomorphometry, implant stability, insertion torque, primary stability
*Researcher, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; †adjunct professor, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; ‡consultant, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; § associate professor, Faculty of Psychology, Vita-Salute San Raffaele University, Milan, Italy; ¶full professor and chairman, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; **associate professor, Dental School, University of Brescia, Brescia, Italy Corresponding Author: Dr Paolo Capparé, Department of Dentistry, IRCCS San Raffale, Via Olgettina 48, Milan 20132, Italy; e-mail: [email protected]
Conflict of interest: We certify that we have no affiliation with or financial involvement in any organization or entity with direct financial interest in the subject matter or materials discussed in the manuscript and that the material is original and has not been published elsewhere. © 2015 Wiley Periodicals, Inc. DOI 10.1111/cid.12294
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INTRODUCTION Success of dental implants relies on successful osseointegration1 that, in turn, correlates with primary stability at implant placement.2 Mechanical stabilization of implant at insertion ensures the fixture remains strictly in place while a stable bond creates between bone and implant surface. Lack of sufficient primary stability at insertion allows implant micromotion in a range that favors fibrous integration instead of osseointegration3–5 and is linked to early implant failure.6 Primary stability depends on several factors.7 Implant design (implant and threads shape) and surface topography are the most important implant-related factors.8 Bone density and the topographical relationship between cortical and cancellous bone at insertion site are regarded as the most important site-related factors.9–13 Measuring bone density and assessing cortical–cancellous bone distribution at the placement site before implant insertion are therefore of paramount importance. At present, bone density measurement at implant sites relies either on presurgical radiographic evaluation or intraoperatory empirical assessments. Radiographic evaluation through CT or CTCB scans has been shown to provide substantial data about the topographical relation of cortical and cancellous bone at the placement site.14–18 CT may provide reliable information about bone density at the insertion site but only as an averaged value,16 and still, concerns remain about the radiation exposure risk.18 CBCT exposes the patients to a smaller radiation dose, but information it provides on bone density is far from being reproducible19,20 and may depend on the particular device used.21,22 Surgeons therefore still rely on the empirical bone density classification proposed by Misch,23 later modified by Trisi and Rao.24 In the Misch assessment system, bone density is classified through the subjective operator’s perception while drilling the implant tunnel (being D1 density attributed as the surgeon perceives “harder” bone down to D4, corresponding to the softest), while Trisi and Rao define three classes only. Both classifications suffer from being nonquantitative and subjective, and not reproducible. At present, an easy-to-use and reliable system to preoperatively quantify the bone quality unfortunately does not exist. As the assessment of bone density at placement site is crucial to plan and perform implant placement properly, conditioning choices concerning implant design
and surgical technique for implant placement, evaluating implant primary stability at insertion, provide additional valuable information to decide the loading strategy, allowing the surgeon to decide whether to follow an immediate loading protocol or preferring an early or delayed one.25,26 Primary stability may be measured, in a clinical setting, by recording values at insertion as the peak insertion torque (IT) or – for research purposes only – the removal torque. Instrumental assessment may exploit either the resonance frequence analysis27,28 or the Periotest29,30 methods, both evaluating implant stability by analyzing and interpreting the response a transducer or the implant itself respectively provides when stimulated by ultrasounds or mechanically. It has also been shown, both on animal bone sections and on synthetic bone models, that implant primary stability, assessed with one or more of the methods mentioned above, significantly correlates with immediate postplacement bone-to-implant contact (BIC).31–33 Concerning a possible reliable and objective measurement of bone density at placement site, it has been shown that cutting resistance at threading is a good estimator of bone quality at the placement site by in vitro studies on pig ribs34 and jaw autopsy specimens.35 Recently, a surgical micromotor has been introduced featuring an instantaneous torque measurement system. This feature is exploited to measure bone density at an intermediate step of implant tunnel preparation by means of a proper probe, according to the same principle already highlighted in the previously mentioned studies,34,35 that is, that resistance at cutting (or, as in the case of the device under examination, at probing) correlates significantly with bone density. The device, moreover, allows to record the instantaneous IT and other correlated values at implant placement. It has already been shown, in a study on bovine ribs,36 that the device provides reliable bone density values, significantly correlating with actual histomorphometric bone density. When used in vivo on human subjects, the device allowed distinguishing zones of the jaws presenting different bone densities37 and provided bone density measurements independently on the operator performing them. It has also been shown that the torque/depth function integral the device provides at implant placement correlates with immediate BIC at insertion, suggesting the device allows site-specific intraoperative BIC measuring and provides reliable
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information about the primary stability of the implant placed.36 Correlation between bone density and insertion measurements the device provides with immediate BIC has so far not been investigated in a human study, and such is the aim of the present paper. MATERIALS AND METHODS Twenty-five patients (16 women and nine men, mean age 56.3 years, range 35–71) were enrolled between December 2012 and January 2014. Inclusion criteria were good general health; no chronic systemic diseases; the presence, either in the upper or in the lower jaw, of an edentulous area requiring the placement of at least one dental implant; sufficient bone volume to place a 5.0 × 12.0-mm (diameter × length) fixture; adequate oral hygiene (mean modified Plaque Index score of 1 or lower and mean modified Sulcus Bleeding Index score of 1 or lower38). Exclusion criteria were the presence of any chronic systemic disease, smoking (>10 cigarettes/day), alcohol or drug abuse, and previous or ongoing bisphosphonate therapy. The study was performed at the Department of Dentistry, San Raffaele Hospital, Milan, Italy. All patients signed an informed consent form for the participation in the study. Surgical Protocol One hour prior to surgery, patients received 1 g of amoxicillin (Zimox, Pfizer Italia, Latina, Italy), and they continued to receive 1 g twice a day for a week after the surgical procedure. Surgery was performed under local anesthesia (mepivacaine 20 mg/ml with adrenaline 1:80.000; Optocain, Molteni Dental, Scandicci, Italy). Incisions were made on the top of the alveolar crest, with releasing incisions if needed. A full-thickness flap was elevated, and bone crest was accurately exposed through vestibular and lingual or palatal subperiosteal dissection.
Figure 1 The bone density measurement probe.
whole depth of the cortical bone layer and subsequently used a 2.3-mm bur to drill a first narrow tunnel to 8-mm depth (the desired implant placement depth for the experimental implant). Before enlarging the tunnel to its final width, a bone reamer was used to drill a 3-mm deep, 3-mm wide circular access hole in order to eliminate the first, overdense, cortical bone ridge layer and allow proper bone density measurement. After mounting the probe on the handpiece, and switching it in its measurement mode, the first probe thread was inserted in the access hole. The surgeon proceeded to switch on rotation and let the probe screw itself into the previously prepared tunnel without exerting any additional pressure (Figure 2). The upside-down cone shape of the threads allowed the device to measure the friction encountered by the first thread only. When the device was in its measurement mode, the probe rotated at a given speed (30 rpm) and could reach 35 N × cm maximum torque. While the probe deepened into the tunnel, a digital software performed a high-frequency sample measurement of the instantaneous torque
Bone Density Measurement The center was provided with a TMM2 surgical micromotor (IDI Evolution, Concorezzo, Italy). When a bone density measurement was performed, a measuring probe was mounted on the handpiece (Figure 1). The probe was a 2-mm wide cylinder featuring equally spaced threads, whose width was 3 mm and shape was a 1-degree reverse cone (patented). At tunnel preparation, the surgeons first created a 2.2-mm round hole for the
Figure 2 Bone density measurement. The probe screws into the 2.3-mm wide tunnel. The tunnel will be subsequently enlarged for implant placement according to results of bone density measurement.
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Figure 3 The torque/depth curve displayed by the micromotor during bone density measurement and at implant insertion. The curve is generated by plotting the instantaneous torque measurements as the measuring probe or the implant deepen into the tunnel. The device calculates the average of all recorded torque values, records the peak value, and calculates the area bound by the curve (integral), showing the corresponding parameters on the bottom of the screen (X axis is 0–12 mm in both cases). Cm, average torque; Cp, peak torque; I, integral; P, maximum depth in 0.1 mm.
needed to keep speed constant. The device recorded also the depth the probe had reached, given the fact probe threads were evenly spaced, and their pitch was known. The device, calibrated with high-precision dynamometers, automatically performed a self-calibration routine at each switching on. The device displayed a torque/ depth graph as an output showing how the instantaneous torque had varied according to the probe depth, together with torque peak and average, and the value of the torque/depth curve integral (Figure 3). Istantaneous torque may be regarded as a point-to-point estimator of bone density along the tunnel, the rationale being that the denser the bone is, the greater the friction on the probe thread, and the greater the torque needed to keep rotation speed constant will be. This rationale relies on previous studies on cutting resistance at threading34,35 and on the observation, in a study on bovine ribs,36 that the device torque measurements at probing significantly correlated with actual histomorphometric bone density. Average torque at probing, therefore, may be regarded as an estimate of average bone density along the whole tunnel. After recording these data, surgeons proceeded to insert an undersized 3.3 × 8-mm (diameter × length) experimental implant (IDI Evolution). Again, the device allowed recording the average and peak torque, the torque/depth curve, and its integral at insertion. The latter provides the area bound by the torque/depth curve and represents the cumulative contribution of the whole implant surface to the instantaneous torque measurement (Figure 3). Data collection was supervised by a single operator trained in the detection method and was recorded in the device solid-state memory to be downloaded later to a personal computer for statistical analysis. The inserted implant was left in place for 15 minutes in order to allow the surrounding bone tissue to adapt
through its elastic response. Afterwards, the surgeon retrieved a core containing the implant, surrounded by a 0.5-mm thick adhering bone layer, with a trephine (Figure 4). A 5.0 × 12-mm (diameter × length) implant (IDI Evolution) was then inserted in the core collection site after preparing it according to the manufacturer implant placement protocols. Specimen Processing Retrieved specimens were fixed in 10% pH 7.0-buffered formalin for 10 days and then transferred to 70% ethanol solution. Dehydration followed in ascending concentration of ethanol up to 100%. Specimens were then infiltrated and embedded in a hydrophilic acrylic resin (LR White, London Resin Company, Berkshire, England). Nondecalcified, 50-μm thick longitudinal sections were prepared by using a cutting and grinding TT system (TMA2, Grottammare, Italy) and slide mounted separately. Sections were double stained with toluidine blue and acid fuchsine. BIC Measurement through Transmitted Light Microscopy Data Recording and Analysis Data for BIC measurement were recorded with a transmitted bright-field light microscope (Axiolab, Zeiss,
Figure 4 The undersized implant is collected after 15 minutes, with a 0.5-mm thick layer bone surrounding it.
Implant Motor and BIC
Oberchen, Germany, or BX 41, Olympus Co, Tokyo, Japan) equipped with a high-resolution digital camera (FinePix S2 Pro, Fuji Photo Film Co. Ltd., Minato-Ku, Japan). Image recording and analysis were performed with a dedicated software (Image-Pro Plus 6.0, Media Cybernetics Inc., Bethesda, MD, USA). BIC for each section was calculated as the ratio between the length of the implant section in contact with bone and the perimeter of the implant body, at a ×25 magnification. At each measurement, the software was calibrated using the diameter or length of the implant as a reference. Measurements were performed by a single researcher. Intraexaminer variability was controlled by carrying out two measurements; if the difference between the two values was greater than 5%, the measuring was repeated. Statistical Analysis In order to investigate the correlation between initial BIC and average torque at probing, measuring bone density at placement site, a linear regression analysis was performed. Again, a linear regression analysis was performed to investigate the correlation between initial BIC and values of the torque/depth integral at insertion. In both cases, the Pearson R coefficient was calculated, and results were regarded as significant when p < .05. All results are provided as mean 1 standard deviation. All statistical analyses were performed by means of a dedicated software program (SPSS 11.5.0, SPSS, Chicago, IL, USA). RESULTS All patients healed uneventfully. Average torque at probing and integral values of the torque/depth curve at insertion recorded at each placement site are shown in Table 1. Table 1 shows also initial BIC values measured for each implants. Average torque at probing was 8.68 1 7.14 N × cm, a value that may be regarded as an estimate of average bone density, considering all placement sites. Average torque at insertion was 10.68 1 7.47 N × cm. Average integral at insertion was 7.0 1 4.5 N × cm2. This value may be regarded as an estimate of the average cumulative contribution of all implants to the instantaneous torque measurements for each of them. Average BIC at insertion was 41.1 1 21.3%. Linear regression graphs are shown in Figure 4. A significant linear correlation was found between immediate BIC at insertion and bone density at the placement site (R = 0.96, explained variance R2 = 0.92; Figure 5),
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TABLE 1 Data Collected for Each Patient Patient #
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
Cm (N × cm)
I (N × cm2)
BIC (%)
1 2 5 15 3 14 3 19 20 29 1 1 9 9 3 11 14 11 9 7 12 11 4 4 0
1.8 2.1 4.0 10.8 3.3 9.9 2.1 15.0 7.8 12.3 0.9 1.2 9.3 10.1 3.4 10.8 12.5 13.4 3.1 8.8 11.2 10.8 4.3 5.4 0.7
21 19 39 68 19 66 19 68 83 83 12 17 41 45 21 50 51 50 43 39 50 51 33 28 11
BIC = bone-to-implant contact; Cm = average torque; I = torque/depth curve integral.
and between immediate BIC at insertion and integral of the torque/depth curve at placement (R = 0.81, explained variance R2 = 0.66, Figure 5). All linear correlations were significant (p < .05). In both cases, residual analysis was coherent with the hypothesis of the linear model being consistent. DISCUSSION The final aim of any prosthetic rehabilitation plan in implantology is to provide an effective, long-lasting recovery of the edentulous patient’s masticatory function and aesthetics. Success of implant-supported prostheses begins with proper diagnosis. Among the many patient-related factors affecting the success of the rehabilitation plan, bone quality at implant placement site is of paramount importance. The oral surgeon, in fact, will take crucial decisions about the type of implant(s) to be placed, the surgical technique to adopt, and – partially –
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Figure 5 Correlation between BIC at insertion and average torque at bone density measurement and integral of the torque/depth curve at insertion. Left: BIC values (Y axis) versus the corresponding average torque at probing (Cm, X axis), for each implant, correlating BIC at insertion with the corresponding placement site bone density estimate (R = 0.96). Right: BIC values (Y axis) versus the corresponding torque/depth integral value (I, X axis), correlating BIC at insertion with the cumulative contribution each implant whole surface provided to the instantaneous torque measurement for that implant (R = 0.81).
about the following loading strategy (delayed, early, or immediate) to follow, on the basis of data about bone density and the spatial relationship between cortical and cancellous bone at implant placement site. While bone quantity may be assessed preoperatively with precision through CT or CBCT radiographs, tomographic tests do not allow for a quantitative, site-specific reproducible assessment of bone density, and still, concerns remain about the radiation risk their application exposes patients to. So, evaluation of bone density still relies on subjective, empirical methods. Such methods, beyond suffering from being not reproducible, do not allow for intraoperatory refinement of the surgical technique as they provide information at a too late stage of the implant placement procedure. The surgeon, therefore, bases his/her intraoperative choices on nonquantitative, subjective evaluations. A more accurate evaluation of bone quality would allow, instead, for the development of specific, quantitativebased, rationales for implant placement. The device used in the present study was shown, in a study on bovine ribs, to provide average torque values at probing that significantly correlated with histologic bone density data.36 Such result is in strict accordance with previous in vitro studies on pig ribs34 and autopsy jaw specimens35 where it had been shown that cutting resistance measurements at threading correlated significantly with bone density values collected through microradiographs of the threading sites. The device was also shown to distinguish predefined zones with different bone densities in a study involving 1,254 bone density measurements in 464 patients.37 Bone density estimates the
device provides are operator independent.36 In the present study, a statistically significant correlation (R = 0.96) was found between initial BIC after insertion and average torque values measured with the specific probe at the placement site before insertion, showing that bone density at the site of insertion correlates significantly with the initial BIC (as shown also by bench experiments33). In other words, the present study shows that the device allows the surgeon to quantitatively assess a parameter (average torque at probing) correlated with bone density,36 which in turn correlates to a postinsertion parameter as initial BIC is. The surgeon can, therefore, modulate its intraoperative behavior according to the initial instrument readings. The device, moreover, provided a site-specific graphical representation of the point-to-point instantaneous density and IT variation along the tunnel length (Figure 3). This may be regarded very helpful for the clinician because it showed up the areas of greater or lesser resistance along the surgical site by their degree of corticalization (crestal, intermediate, and apical). This could be of further help in the preparation of the implant site defining if any undersizing of the implant tunnel and/or bone compaction is necessary, assisting in the choice of the most appropriate implant system for the anatomy of the implant site (macro and micromorphology of the implant surface) of a one-stage or twostage protocol, with or without the use of taps and cortical drills. CONCLUSIONS Results of present study show, moreover, a significant (R = 0.81) correlation exists also between the IT/depth
Implant Motor and BIC
integral and the initial BIC rate at insertion. It is known that initial BIC at insertion is correlated with primary stability31–33,39 and that topographical features of the implant and surgical implant placement technique may modulate such correlation.8,40–42 Assessment of the initial BIC after implant insertion may provide valuable – and, above all, quantitative – information about the interaction between the implant just inserted with the surrounding bone. These information may be regarded both as an intraoperatory assessment of the consistency of choices done (implant shape, site preparation, etc.) and as a postoperatory primary stability assessment, useful to plan the loading strategy properly. Availability of such quantitative information, moreover, may allow to define rationales to plan and perform any loading strategy through targeted clinical studies. Studies on immediate loading, where primary stability is known to play a fundamental role in the success of rehabilitation43 and especially on immediate loading on single implants could, in particular, benefit of such possibility. In the present protocol, intraoperative site-specific measurements of bone density recorded with the system under testing at placement site and the integral of the torque/depth curve correlated significantly with initial BIC. Within the limitations of this study, the system under testing could provide quantitative, reproducible, and reliable data about bone density at the site of insertion and about immediate postinsertion BIC, and could represent a valuable tool both for the oral implantologist in his/her daily clinical practice and for the clinical researcher in planning and performing clinical research protocols in implant surgery. REFERENCES 1. Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983; 50:399–410. 2. Davies JE. Mechanisms of endosseous integration. Int J Prosthodont 1998; 11:391–401. 3. Brunski JB. Biomechanical factors affecting the bone-dental implant interface. Clin Mater 1992; 10:153–201. 4. Brunski JB. Avoid pitfalls of overloading and micromotion of intraosseous implants. Dent Implantol Update 1993; 4:77–81. 5. Szmukler-Moncler S, Salama H, Reingewirtz Y, Dubruille JH. Timing of loading and effect of micromotion on bone-dental implant interface: review of experimental literature. J Biomed Mater Res 1998; 43:192–203. Summer.
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6. Sakka S, Baroudi K, Nassani MZ. Factors associated with early and late failure of dental implants. J Investig Clin Dent 2012; 3:258–261. 7. Javed F, Ahmed HB, Crespi R, Romanos GE. Role of primary stability for successful osseointegration of dental implants: factors of influence and evaluation. Interv Med Appl Sci 2013; 5:162–167. 8. Chong L, Khocht A, Suzuki JB, Gaughan J. Effect of implant design on initial stability of tapered implants. J Oral Implantol 2009; 35:130–135. 9. Friberg B, Jemt T, Lekholm U. Early failures in 4,641 consecutively placed Brånemark dental implants: a study from stage 1 surgery to the connection of completed prostheses. Int J Oral Maxillofac Implants 1991; 6:142–146. 10. Johansson B, Back T, Hirsch JM. Cutting torque measurements in conjunction with implant placement in grafted and nongrafted maxillas as an objective evaluation of bone density: a possible method for identifying early implant failures. Clin Implant Dent Relat Res 2004; 6:9–15. 11. Meredith N. Assessment of implant stability as a prognostic determinant. Int J Prosthodont 1998; 11:491–501. 12. Sennerby L, Roos J. Surgical determinants of clinical success of osseointegrated oral implants: a review of the literature. Int J Prosthodont 1998; 11:408–420. 13. Roos J, Sennerby L, Albrektsson T. An update on the clinical documentation on currently used bone anchored endosseous oral implants. Dent Update 1997; 24:194– 200. 14. Hatcher DC, Dial C, Mayorga C. Cone beam CT for presurgical assessment of implant sites. J Calif Dent Assoc 2003; 31:825–833. 15. Shahlaie M, Gantes B, Schulz E, Riggs M, Crigger M. Bone density assessments of dental implant sites: 1. Quantitative computed tomography. Int J Oral Maxillofac Implants 2003; 18:224–231. 16. Turkyilmaz I, Tözüm TF, Tumer C. Bone density assessments of oral implant sites using computerized tomography. J Oral Rehabil 2007; 34:267–272. 17. De Oliveira RC, Leles CR, Normanha LM, Lindh C, Ribeiro-Rotta RF. Assessments of trabecular bone density at implant sites on CT images. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008; 105:231–238. 18. Norton MR, Gamble C. Bone classification: an objective scale of bone density using the computerized tomography scan. Clin Oral Implants Res 2001; 12:79–84. 19. Shapurian T, Damoulis PD, Reiser GM, Griffin TJ, Rand WM. Quantitative evaluation of bone density using the Hounsfield index. Int J Oral Maxillofac Implants 2006; 21:290–297. 20. Valiyaparambil JV, Yamany I, Ortiz D, et al. Bone quality evaluation: comparison of cone beam computed tomography and subjective surgical assessment. Int J Oral Maxillofac Implants 2012; 27:1271–1277.
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21. Mah P, Reeves TE, McDavid WD. Deriving Hounsfield units using grey levels in cone beam computed tomography. Dentomaxillofac Radiol 2010; 39:323–335. 22. Nomura Y, Watanabe H, Honda E, Kurabayashi T. Reliability of voxel values from cone-beam computed tomography for dental use in evaluating bone mineral density. Clin Oral Implants Res 2010; 21:558–562. 23. Misch CE. Density of bone: effect of treatment planning, surgical approach, and healing. In: Misch CE, ed. Contemporary implant dentistry. St Louis, MO: Mosby Year-Book, 1993:469–485. 24. Trisi P, Rao W. Bone classification: clinicalhistomorphometric comparison. Clin Oral Implants Res 1999; 10:1–7. 25. Prosper L, Crespi R, Valenti E, Cappare P, Gherlone E. Fiveyear follow-up of wide-diameter implants placed in fresh molar extraction sockets in the mandible: immediate versus delayed loading. Int J Oral Maxillofac Implants 2010; 25:607–612. 26. Crespi R, Capparé P, Gherlone E, Romanos GE. Immediate versus delayed loading of dental implants placed in fresh extraction sockets in the maxillary esthetic zone: a clinical comparative study. Int J Oral Maxillofac Implants 2008; 23:753–758. 27. 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. 28. Friberg B, Sennerby L, Meredith N, Lekholm U. A comparison between cutting torque and resonance frequency measurements of maxillary implants. A 20-month clinical study. Int J Oral Maxillofac Surg 1999; 28:297–303. 29. Olive J, Aparicio C. Periotest method as a measure of osseointegrated oral implant stability. Int J Oral Maxillofac Implants 1990; 5:390–400. 30. Teerlinck J, Quirynen M, Darius P, van Steenberghe D. Periotest: an objective clinical diagnosis of bone apposition toward implants. Int J Oral Maxillofac Implants 1991; 6:55– 61. 31. Degidi M, Daprile G, Piattelli A, Iezzi G. Development of a new implant primary stability parameter: insertion torque revisited. Clin Implant Dent Relat Res 2013; 15:637–644. 32. Hsu JT, Huang HL, Chang CH, Tsai MT, Hung WC, Fuh LJ. Relationship of three-dimensional bone-to-implant contact
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ABSTRACT Background: Quantitative intraoperative evaluation of bone quality at implant placement site and postinsertion implant primary stability assessment are two key parameters to perform implant-supported rehabilitation properly. A novel micromotor has been recently introduced allowing to measure bone density at implant placement site and to record implant insertion-related parameters, such as the instantaneous, average and peak insertion torque values, and the insertion torque/depth integral. Purpose: The aim of this study was to investigate in vivo if any correlation existed between initial bone-to-implant contact (BIC) and bone density and integral values recorded with the instrument. Materials and Methods: Twenty-five patients seeking for implant-supported rehabilitation of edentulous areas were consecutively treated. Before implant placement, bone density at the insertion site was measured. For each patient, an undersized 3.3 × 8-mm implant was placed, recording the insertion torque/depth integral values. After 15 minutes, the undersized implant was retrieved with a 0.5 mm-thick layer of bone surrounding it. Standard implants were consequently placed. Retrieved implants were analyzed for initial BIC quantification after fixation, dehydration, acrylic resin embedment, sections cutting and grinding, and toluidine-blue and acid fuchsine staining. Correlation between initial BIC values, bone density at the insertion site, and the torque/depth integral values was investigated by linear regression analysis. Results: A significant linear correlation was found to exist between initial BIC and (a) bone density at the insertion site (R = 0.96, explained variance R2 = 0.92) and (b) torque/depth integral at placement (R = 0.81, explained variance R2 = 0.66). Conclusions: The system provided quantitative, reliable data correlating significantly with immediate postinsertion initial BIC, and could therefore represent a valuable tool both for clinical research and for the oral implantologist in his/her daily clinical practice. KEY WORDS: bone density, bone to implant contact, dental implant, histomorphometry, implant stability, insertion torque, primary stability
*Researcher, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; †adjunct professor, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; ‡consultant, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; § associate professor, Faculty of Psychology, Vita-Salute San Raffaele University, Milan, Italy; ¶full professor and chairman, Dental School, Vita-Salute University and IRCCS San Raffaele, Milan, Italy; **associate professor, Dental School, University of Brescia, Brescia, Italy Corresponding Author: Dr Paolo Capparé, Department of Dentistry, IRCCS San Raffale, Via Olgettina 48, Milan 20132, Italy; e-mail: [email protected]
Conflict of interest: We certify that we have no affiliation with or financial involvement in any organization or entity with direct financial interest in the subject matter or materials discussed in the manuscript and that the material is original and has not been published elsewhere. © 2015 Wiley Periodicals, Inc. DOI 10.1111/cid.12294
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INTRODUCTION Success of dental implants relies on successful osseointegration1 that, in turn, correlates with primary stability at implant placement.2 Mechanical stabilization of implant at insertion ensures the fixture remains strictly in place while a stable bond creates between bone and implant surface. Lack of sufficient primary stability at insertion allows implant micromotion in a range that favors fibrous integration instead of osseointegration3–5 and is linked to early implant failure.6 Primary stability depends on several factors.7 Implant design (implant and threads shape) and surface topography are the most important implant-related factors.8 Bone density and the topographical relationship between cortical and cancellous bone at insertion site are regarded as the most important site-related factors.9–13 Measuring bone density and assessing cortical–cancellous bone distribution at the placement site before implant insertion are therefore of paramount importance. At present, bone density measurement at implant sites relies either on presurgical radiographic evaluation or intraoperatory empirical assessments. Radiographic evaluation through CT or CTCB scans has been shown to provide substantial data about the topographical relation of cortical and cancellous bone at the placement site.14–18 CT may provide reliable information about bone density at the insertion site but only as an averaged value,16 and still, concerns remain about the radiation exposure risk.18 CBCT exposes the patients to a smaller radiation dose, but information it provides on bone density is far from being reproducible19,20 and may depend on the particular device used.21,22 Surgeons therefore still rely on the empirical bone density classification proposed by Misch,23 later modified by Trisi and Rao.24 In the Misch assessment system, bone density is classified through the subjective operator’s perception while drilling the implant tunnel (being D1 density attributed as the surgeon perceives “harder” bone down to D4, corresponding to the softest), while Trisi and Rao define three classes only. Both classifications suffer from being nonquantitative and subjective, and not reproducible. At present, an easy-to-use and reliable system to preoperatively quantify the bone quality unfortunately does not exist. As the assessment of bone density at placement site is crucial to plan and perform implant placement properly, conditioning choices concerning implant design
and surgical technique for implant placement, evaluating implant primary stability at insertion, provide additional valuable information to decide the loading strategy, allowing the surgeon to decide whether to follow an immediate loading protocol or preferring an early or delayed one.25,26 Primary stability may be measured, in a clinical setting, by recording values at insertion as the peak insertion torque (IT) or – for research purposes only – the removal torque. Instrumental assessment may exploit either the resonance frequence analysis27,28 or the Periotest29,30 methods, both evaluating implant stability by analyzing and interpreting the response a transducer or the implant itself respectively provides when stimulated by ultrasounds or mechanically. It has also been shown, both on animal bone sections and on synthetic bone models, that implant primary stability, assessed with one or more of the methods mentioned above, significantly correlates with immediate postplacement bone-to-implant contact (BIC).31–33 Concerning a possible reliable and objective measurement of bone density at placement site, it has been shown that cutting resistance at threading is a good estimator of bone quality at the placement site by in vitro studies on pig ribs34 and jaw autopsy specimens.35 Recently, a surgical micromotor has been introduced featuring an instantaneous torque measurement system. This feature is exploited to measure bone density at an intermediate step of implant tunnel preparation by means of a proper probe, according to the same principle already highlighted in the previously mentioned studies,34,35 that is, that resistance at cutting (or, as in the case of the device under examination, at probing) correlates significantly with bone density. The device, moreover, allows to record the instantaneous IT and other correlated values at implant placement. It has already been shown, in a study on bovine ribs,36 that the device provides reliable bone density values, significantly correlating with actual histomorphometric bone density. When used in vivo on human subjects, the device allowed distinguishing zones of the jaws presenting different bone densities37 and provided bone density measurements independently on the operator performing them. It has also been shown that the torque/depth function integral the device provides at implant placement correlates with immediate BIC at insertion, suggesting the device allows site-specific intraoperative BIC measuring and provides reliable
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information about the primary stability of the implant placed.36 Correlation between bone density and insertion measurements the device provides with immediate BIC has so far not been investigated in a human study, and such is the aim of the present paper. MATERIALS AND METHODS Twenty-five patients (16 women and nine men, mean age 56.3 years, range 35–71) were enrolled between December 2012 and January 2014. Inclusion criteria were good general health; no chronic systemic diseases; the presence, either in the upper or in the lower jaw, of an edentulous area requiring the placement of at least one dental implant; sufficient bone volume to place a 5.0 × 12.0-mm (diameter × length) fixture; adequate oral hygiene (mean modified Plaque Index score of 1 or lower and mean modified Sulcus Bleeding Index score of 1 or lower38). Exclusion criteria were the presence of any chronic systemic disease, smoking (>10 cigarettes/day), alcohol or drug abuse, and previous or ongoing bisphosphonate therapy. The study was performed at the Department of Dentistry, San Raffaele Hospital, Milan, Italy. All patients signed an informed consent form for the participation in the study. Surgical Protocol One hour prior to surgery, patients received 1 g of amoxicillin (Zimox, Pfizer Italia, Latina, Italy), and they continued to receive 1 g twice a day for a week after the surgical procedure. Surgery was performed under local anesthesia (mepivacaine 20 mg/ml with adrenaline 1:80.000; Optocain, Molteni Dental, Scandicci, Italy). Incisions were made on the top of the alveolar crest, with releasing incisions if needed. A full-thickness flap was elevated, and bone crest was accurately exposed through vestibular and lingual or palatal subperiosteal dissection.
Figure 1 The bone density measurement probe.
whole depth of the cortical bone layer and subsequently used a 2.3-mm bur to drill a first narrow tunnel to 8-mm depth (the desired implant placement depth for the experimental implant). Before enlarging the tunnel to its final width, a bone reamer was used to drill a 3-mm deep, 3-mm wide circular access hole in order to eliminate the first, overdense, cortical bone ridge layer and allow proper bone density measurement. After mounting the probe on the handpiece, and switching it in its measurement mode, the first probe thread was inserted in the access hole. The surgeon proceeded to switch on rotation and let the probe screw itself into the previously prepared tunnel without exerting any additional pressure (Figure 2). The upside-down cone shape of the threads allowed the device to measure the friction encountered by the first thread only. When the device was in its measurement mode, the probe rotated at a given speed (30 rpm) and could reach 35 N × cm maximum torque. While the probe deepened into the tunnel, a digital software performed a high-frequency sample measurement of the instantaneous torque
Bone Density Measurement The center was provided with a TMM2 surgical micromotor (IDI Evolution, Concorezzo, Italy). When a bone density measurement was performed, a measuring probe was mounted on the handpiece (Figure 1). The probe was a 2-mm wide cylinder featuring equally spaced threads, whose width was 3 mm and shape was a 1-degree reverse cone (patented). At tunnel preparation, the surgeons first created a 2.2-mm round hole for the
Figure 2 Bone density measurement. The probe screws into the 2.3-mm wide tunnel. The tunnel will be subsequently enlarged for implant placement according to results of bone density measurement.
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Figure 3 The torque/depth curve displayed by the micromotor during bone density measurement and at implant insertion. The curve is generated by plotting the instantaneous torque measurements as the measuring probe or the implant deepen into the tunnel. The device calculates the average of all recorded torque values, records the peak value, and calculates the area bound by the curve (integral), showing the corresponding parameters on the bottom of the screen (X axis is 0–12 mm in both cases). Cm, average torque; Cp, peak torque; I, integral; P, maximum depth in 0.1 mm.
needed to keep speed constant. The device recorded also the depth the probe had reached, given the fact probe threads were evenly spaced, and their pitch was known. The device, calibrated with high-precision dynamometers, automatically performed a self-calibration routine at each switching on. The device displayed a torque/ depth graph as an output showing how the instantaneous torque had varied according to the probe depth, together with torque peak and average, and the value of the torque/depth curve integral (Figure 3). Istantaneous torque may be regarded as a point-to-point estimator of bone density along the tunnel, the rationale being that the denser the bone is, the greater the friction on the probe thread, and the greater the torque needed to keep rotation speed constant will be. This rationale relies on previous studies on cutting resistance at threading34,35 and on the observation, in a study on bovine ribs,36 that the device torque measurements at probing significantly correlated with actual histomorphometric bone density. Average torque at probing, therefore, may be regarded as an estimate of average bone density along the whole tunnel. After recording these data, surgeons proceeded to insert an undersized 3.3 × 8-mm (diameter × length) experimental implant (IDI Evolution). Again, the device allowed recording the average and peak torque, the torque/depth curve, and its integral at insertion. The latter provides the area bound by the torque/depth curve and represents the cumulative contribution of the whole implant surface to the instantaneous torque measurement (Figure 3). Data collection was supervised by a single operator trained in the detection method and was recorded in the device solid-state memory to be downloaded later to a personal computer for statistical analysis. The inserted implant was left in place for 15 minutes in order to allow the surrounding bone tissue to adapt
through its elastic response. Afterwards, the surgeon retrieved a core containing the implant, surrounded by a 0.5-mm thick adhering bone layer, with a trephine (Figure 4). A 5.0 × 12-mm (diameter × length) implant (IDI Evolution) was then inserted in the core collection site after preparing it according to the manufacturer implant placement protocols. Specimen Processing Retrieved specimens were fixed in 10% pH 7.0-buffered formalin for 10 days and then transferred to 70% ethanol solution. Dehydration followed in ascending concentration of ethanol up to 100%. Specimens were then infiltrated and embedded in a hydrophilic acrylic resin (LR White, London Resin Company, Berkshire, England). Nondecalcified, 50-μm thick longitudinal sections were prepared by using a cutting and grinding TT system (TMA2, Grottammare, Italy) and slide mounted separately. Sections were double stained with toluidine blue and acid fuchsine. BIC Measurement through Transmitted Light Microscopy Data Recording and Analysis Data for BIC measurement were recorded with a transmitted bright-field light microscope (Axiolab, Zeiss,
Figure 4 The undersized implant is collected after 15 minutes, with a 0.5-mm thick layer bone surrounding it.
Implant Motor and BIC
Oberchen, Germany, or BX 41, Olympus Co, Tokyo, Japan) equipped with a high-resolution digital camera (FinePix S2 Pro, Fuji Photo Film Co. Ltd., Minato-Ku, Japan). Image recording and analysis were performed with a dedicated software (Image-Pro Plus 6.0, Media Cybernetics Inc., Bethesda, MD, USA). BIC for each section was calculated as the ratio between the length of the implant section in contact with bone and the perimeter of the implant body, at a ×25 magnification. At each measurement, the software was calibrated using the diameter or length of the implant as a reference. Measurements were performed by a single researcher. Intraexaminer variability was controlled by carrying out two measurements; if the difference between the two values was greater than 5%, the measuring was repeated. Statistical Analysis In order to investigate the correlation between initial BIC and average torque at probing, measuring bone density at placement site, a linear regression analysis was performed. Again, a linear regression analysis was performed to investigate the correlation between initial BIC and values of the torque/depth integral at insertion. In both cases, the Pearson R coefficient was calculated, and results were regarded as significant when p < .05. All results are provided as mean 1 standard deviation. All statistical analyses were performed by means of a dedicated software program (SPSS 11.5.0, SPSS, Chicago, IL, USA). RESULTS All patients healed uneventfully. Average torque at probing and integral values of the torque/depth curve at insertion recorded at each placement site are shown in Table 1. Table 1 shows also initial BIC values measured for each implants. Average torque at probing was 8.68 1 7.14 N × cm, a value that may be regarded as an estimate of average bone density, considering all placement sites. Average torque at insertion was 10.68 1 7.47 N × cm. Average integral at insertion was 7.0 1 4.5 N × cm2. This value may be regarded as an estimate of the average cumulative contribution of all implants to the instantaneous torque measurements for each of them. Average BIC at insertion was 41.1 1 21.3%. Linear regression graphs are shown in Figure 4. A significant linear correlation was found between immediate BIC at insertion and bone density at the placement site (R = 0.96, explained variance R2 = 0.92; Figure 5),
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TABLE 1 Data Collected for Each Patient Patient #
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
Cm (N × cm)
I (N × cm2)
BIC (%)
1 2 5 15 3 14 3 19 20 29 1 1 9 9 3 11 14 11 9 7 12 11 4 4 0
1.8 2.1 4.0 10.8 3.3 9.9 2.1 15.0 7.8 12.3 0.9 1.2 9.3 10.1 3.4 10.8 12.5 13.4 3.1 8.8 11.2 10.8 4.3 5.4 0.7
21 19 39 68 19 66 19 68 83 83 12 17 41 45 21 50 51 50 43 39 50 51 33 28 11
BIC = bone-to-implant contact; Cm = average torque; I = torque/depth curve integral.
and between immediate BIC at insertion and integral of the torque/depth curve at placement (R = 0.81, explained variance R2 = 0.66, Figure 5). All linear correlations were significant (p < .05). In both cases, residual analysis was coherent with the hypothesis of the linear model being consistent. DISCUSSION The final aim of any prosthetic rehabilitation plan in implantology is to provide an effective, long-lasting recovery of the edentulous patient’s masticatory function and aesthetics. Success of implant-supported prostheses begins with proper diagnosis. Among the many patient-related factors affecting the success of the rehabilitation plan, bone quality at implant placement site is of paramount importance. The oral surgeon, in fact, will take crucial decisions about the type of implant(s) to be placed, the surgical technique to adopt, and – partially –
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Figure 5 Correlation between BIC at insertion and average torque at bone density measurement and integral of the torque/depth curve at insertion. Left: BIC values (Y axis) versus the corresponding average torque at probing (Cm, X axis), for each implant, correlating BIC at insertion with the corresponding placement site bone density estimate (R = 0.96). Right: BIC values (Y axis) versus the corresponding torque/depth integral value (I, X axis), correlating BIC at insertion with the cumulative contribution each implant whole surface provided to the instantaneous torque measurement for that implant (R = 0.81).
about the following loading strategy (delayed, early, or immediate) to follow, on the basis of data about bone density and the spatial relationship between cortical and cancellous bone at implant placement site. While bone quantity may be assessed preoperatively with precision through CT or CBCT radiographs, tomographic tests do not allow for a quantitative, site-specific reproducible assessment of bone density, and still, concerns remain about the radiation risk their application exposes patients to. So, evaluation of bone density still relies on subjective, empirical methods. Such methods, beyond suffering from being not reproducible, do not allow for intraoperatory refinement of the surgical technique as they provide information at a too late stage of the implant placement procedure. The surgeon, therefore, bases his/her intraoperative choices on nonquantitative, subjective evaluations. A more accurate evaluation of bone quality would allow, instead, for the development of specific, quantitativebased, rationales for implant placement. The device used in the present study was shown, in a study on bovine ribs, to provide average torque values at probing that significantly correlated with histologic bone density data.36 Such result is in strict accordance with previous in vitro studies on pig ribs34 and autopsy jaw specimens35 where it had been shown that cutting resistance measurements at threading correlated significantly with bone density values collected through microradiographs of the threading sites. The device was also shown to distinguish predefined zones with different bone densities in a study involving 1,254 bone density measurements in 464 patients.37 Bone density estimates the
device provides are operator independent.36 In the present study, a statistically significant correlation (R = 0.96) was found between initial BIC after insertion and average torque values measured with the specific probe at the placement site before insertion, showing that bone density at the site of insertion correlates significantly with the initial BIC (as shown also by bench experiments33). In other words, the present study shows that the device allows the surgeon to quantitatively assess a parameter (average torque at probing) correlated with bone density,36 which in turn correlates to a postinsertion parameter as initial BIC is. The surgeon can, therefore, modulate its intraoperative behavior according to the initial instrument readings. The device, moreover, provided a site-specific graphical representation of the point-to-point instantaneous density and IT variation along the tunnel length (Figure 3). This may be regarded very helpful for the clinician because it showed up the areas of greater or lesser resistance along the surgical site by their degree of corticalization (crestal, intermediate, and apical). This could be of further help in the preparation of the implant site defining if any undersizing of the implant tunnel and/or bone compaction is necessary, assisting in the choice of the most appropriate implant system for the anatomy of the implant site (macro and micromorphology of the implant surface) of a one-stage or twostage protocol, with or without the use of taps and cortical drills. CONCLUSIONS Results of present study show, moreover, a significant (R = 0.81) correlation exists also between the IT/depth
Implant Motor and BIC
integral and the initial BIC rate at insertion. It is known that initial BIC at insertion is correlated with primary stability31–33,39 and that topographical features of the implant and surgical implant placement technique may modulate such correlation.8,40–42 Assessment of the initial BIC after implant insertion may provide valuable – and, above all, quantitative – information about the interaction between the implant just inserted with the surrounding bone. These information may be regarded both as an intraoperatory assessment of the consistency of choices done (implant shape, site preparation, etc.) and as a postoperatory primary stability assessment, useful to plan the loading strategy properly. Availability of such quantitative information, moreover, may allow to define rationales to plan and perform any loading strategy through targeted clinical studies. Studies on immediate loading, where primary stability is known to play a fundamental role in the success of rehabilitation43 and especially on immediate loading on single implants could, in particular, benefit of such possibility. In the present protocol, intraoperative site-specific measurements of bone density recorded with the system under testing at placement site and the integral of the torque/depth curve correlated significantly with initial BIC. Within the limitations of this study, the system under testing could provide quantitative, reproducible, and reliable data about bone density at the site of insertion and about immediate postinsertion BIC, and could represent a valuable tool both for the oral implantologist in his/her daily clinical practice and for the clinical researcher in planning and performing clinical research protocols in implant surgery. REFERENCES 1. Brånemark PI. Osseointegration and its experimental background. J Prosthet Dent 1983; 50:399–410. 2. Davies JE. Mechanisms of endosseous integration. Int J Prosthodont 1998; 11:391–401. 3. Brunski JB. Biomechanical factors affecting the bone-dental implant interface. Clin Mater 1992; 10:153–201. 4. Brunski JB. Avoid pitfalls of overloading and micromotion of intraosseous implants. Dent Implantol Update 1993; 4:77–81. 5. Szmukler-Moncler S, Salama H, Reingewirtz Y, Dubruille JH. Timing of loading and effect of micromotion on bone-dental implant interface: review of experimental literature. J Biomed Mater Res 1998; 43:192–203. Summer.
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