Liene Molly density and primary stability in implant therapy

Authors’ affiliations: Key words: bone implant interface, bone regeneration, clinical assessment, diagnosis, L. Molly, Department of Periodontology, Catholic guided tissue regeneration, morphometric analysis, structural biology, tissue physiology University of Leuven, Leuven, Belgium L. Molly, Department of Periodontology, University of Maryland, Baltimore, MD, USA Abstract

Correspondence to: Introduction: To improve patient comfort, deviations from the very successful standard L. Molly protocol are being developed. To keep implant failure rates as low as University of Maryland possible, the most perfect treatment planning and a good patient selection are extremely 650 W Baltimore Street Baltimore MD 21201 important. Because bone density plays an important role in implant outcome, known USA relations of bone density could improve treatment planning. Tel.: þ 1 410 70671452 Fax: þ 1 410 7063028 Material and methods: A Pubmed search revealed 66 manuscripts investigating and discussing bone density of human jawbone whether or not related to implant stability or outcome. Forty-five of these will be discussed in this review. Results and discussion: Many pre-operative methods of jawbone density assessment are available. Most of those techniques correlate well with one another. Some are more elaborate to use in clinical practice. Primary stability measurements show significant correlations with different bone densities and also with implant outcome; however, not many studies investigate both at the same time. Conclusion: To investigate the outcome of adaptation methods of the surgical protocol with regard to the jawbone density, an objective pre-surgical determination of bone density is necessary.

It is necessary to indicate that this review yet been defined. Large epidemiological stu- paper investigates the assessment of bone dies will be necessary to investigate this. density rather than bone quality. Many Therefore, this review will only address one papers in the literature define bone quality factor of bone quality, namely bone density. as equivalent to bone density. This cannot Bone density seems to be of great im- be taken for granted because many more portance not only in primary implant sta- factors are important when investigating bility but also in the predictability of oral bone quality than bone density alone. Bone implant outcome. metabolism, cell turn over, mineralization, Following the standard osseointegration maturization, intercellular matrix, vascular- protocol, P-I Bra˚nemark put forward, very ity and others are very important in the high success rates can be obtained; up to To cite this article: Molly L. Bone density and primary stability in implant definition of bone quality and eventually 99% cumulative success rates are reported therapy. may very well influence implant outcome. in the interforaminal region of the lower Clin. Oral Imp. Res., 17 (Suppl. 2), 2006; 124–135 The extent to which every single factor of jaw (Lindquist et al. 1996). r 2006 The Authors bone quality, as stated above, influences the In this standard protocol, two-stage sur- Journal compilation r Blackwell Munksgaard 2006 outcome of the implant treatment, has not gery is a prerequisite, leaving the implant

124 Molly . Bone density and implant stability submerged for 3–6 months, depending on Verify whether there is any relation results, a table has been constructed to the region of interest where the implants indicated in the literature between pri- clarify the scientific relevance of each pa- are placed. This should allow primary os- mary stability and bone density. per included. seointegration. At the time point of unco- Investigate whether there is any rela- Group 3 contained all articles verifying a vering, the bone-to-implant contact (BIC) tionship indicated in the literature be- correlation between primary stability and ratio should be high enough to allow a load- tween bone density and treatment bone density. Eight articles were selected to bearing superstructure to be successfully outcome. be discussed in this group. In this case, placed and maintained. Many different screening of related articles did not reveal biological factors are contributing to the further manuscripts suitable for inclusion. failure of osseointegration of oral implants Material and methods In the results, a table has been constructed (Esposito et al. 1998). The authors con- to clarify the scientific relevance of each cluded that surgical trauma and anatomical Search strategy paper included. conditions are the most important factors A first Medline (Pubmed) search was per- Group 4 contained the articles discussing for primary implant losses; jawbone qual- formed to identify all articles investigating the adaptation of the surgical protocol re- ity, volume and overload are major deter- bone density. The search was restricted lated with bone density. In this group, 10 minants for late implant failures. The from 1988 till January 1, 2006. Because articles were selected. Research of the impact of these factors on implant failure in the literature bone density has always manuscripts related to the ones selected rate depends on the implant design and been referred to as bone quality, the follow- revealed selection of five more articles. surface characteristics and can be altered ing search parameters have been included Again, in the results, a table has been by modifying the surgical technique. Jaffin in the search: ‘assessment of bone quality constructed to clarify the scientific rele- & Berman (1991) and Herrmann et al. in human jaw bone’, ‘surgical protocol’ and vance of each paper included. (2005) stated that poor bone quantity and ‘jaw bone quality’. This search revealed especially poor bone quality are the main 66 results. For all of these manuscripts, risk factors for implant failure using abstracts were screened for inclusion to Results and discussion this standard protocol. One can figure answer one or more of the questions when deviations from this protocol take addressed in the aims. Forty-five of the Pre-operative methods of jawbone density assessment place; this risk factor becomes even more screened manuscripts were selected for important. further investigation. The manuscripts The golden standard for bone density measure- ments has been considered as the histological Primary osseointegration did not take that were not selected discussed the rela- and morphometrical measurement of the place yet when, e.g. early or immediate tion between bone density and extrac- jawbone loading is applied and in these instances tion difficulties during the third molar Small biopsies taken pre-operatively can be primary stability will be a major issue. extraction and between bone density and used for histomorphometric evaluation. Primary implant stability can be mea- the surgical treatment of cleft palate/ Trephine biopsies can be histologically pre- sured at implant placement using several alveolar ridge patients. The selected manu- pared, ground, sliced and stained to allow a biomechanical devices. scripts were divided into four different calculation of the percentage of bony tra- The relation between biomechanically groups according to the questions posed in beculae over the total biopsy area. This measured primary stability and pre-surgical the aims of the review. technique was compared with the subjec- measurements of bone density could help Group 1 contained all articles discussing tive perception of bone density by the in treatment planning. An adaptation of a method of bone density measurement surgeon during the preparation and place- the surgical technique, the loading protocol and/or assessing their validity. Eleven arti- ment of oral implants (Trisi & Rao 1999). or design and surface characteristics of the cles were selected. To extend this search, The surgeon was able to detect extremely implant could improve. related articles of the selected manuscripts dense bone and extremely soft bone but The aim of the present review is to: were also screened for inclusion. In this could not distinguish any other bone den- group, only two articles were included in sities. Comparison of 3D-obtained mor- present the different methods of bone the discussion of this topic based on the phometric data through micro-computed density measurements available for relevance in answering the posed question. tomography (mCT) with previously taken clinical use and to investigate whether In the results, a table has been constructed conventional CT images from human ca- their validity has been tested. to clarify the scientific relevance of each daver mandibles and maxillae revealed a Present the different methods of im- paper included. general agreement between both, stating plant stability assessment available Group 2 contained all articles discuss- higher bone density in the mandibles vs. for clinical use and to investigate ing methods of primary implant stability the maxillae and in the anterior areas vs. their validity in effectively testing measurements and their validity. Sixteen the posterior (Fanuscu & Chang 2004). implant stability as defined in this articles were selected. To extend the The mCT technique can give more speci- chapter. This will include assessment search, related articles of the selected fied information on trabecular thickness of the predictive value of insertion manuscripts were also screened for inclu- and trabecular separation but is more time torque measurements on implant out- sion. In this group, four articles were consuming and is not possible on in vivo comes. selected from this extended search. In the subjects.

125 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135 Molly . Bone density and implant stability

Quantitative-computerized tomography (qCT) jawbone was investigated in 1999 (Denis- were placed according to the standard measurement of the jawbone sen et al. 1999). Small trephine biopsies of protocol. qCT is the most frequently used method to the human jawbone were prepared, 10 A significant relation was detected be- measure the density of the spine in the stored in alcohol and 10 histologically tween bone mineral density (single-energy diagnosis of in females. Ob- treated, and investigated on bone mineral CT) of the mandibular cortex and an ordi- jects with a known density are situated on density by DEXA. The coefficients of var- nal classification (1–3) of the morphology the same radiograph and allow a compar- iation are comparable with those of precise of the inferior cortex based on panoramic ison with the tissues to investigate. The qCT measurements. This DEXA method radiographs (Klemetti & Kolmakow 1997). ten 2-mm-thick vertical CT slices perpen- could thus replace pre-operative qCT mea- This finding may be interesting in implant dicular to the buccal and lingual plates of surement of bone density in case no CT is planning but a more specified classification 15 mandibles were investigated according necessary of the area of interest. No other is more elaborate when bone quality be- to this technique (Lindh et al. 1996). Ante- studies using DEXA as a bone density comes more important in the planning, e.g. rior sections showed higher values than analysis of human jawbone could be re- when immediate loading is applied. posterior sections, and a huge intra- and trieved from the Pubmed search. The paper Table 1 will clarify the impact of all studies intersubject variation was present. by Becker et al. (2000) suggests that DEXA discussed in this part of the discussion. Implementing an aluminum step-wedge measurements of the peripheral (ra- in the radiograph taken is based on the dius and ulna) do not gain any beneficial Pre-operative assessment of implant same principle. Some researchers have im- information on bone density at the site of stability plemented such a wedge in intra-oral radio- implant placement. In this study, the Stability is generally defined as ‘a measure graphs to measure bone density (Southard sample size was too small to identify a of the difficulty of displacing an object or et al. 2000; Nackaerts et al. 2006). They relation between peripheral osteoporosis system from equilibrium.’ In clinical were originally investigating the relation and implant loss. terms, however, ‘primary’ stability is not between jawbone density and general ske- clearly defined, but is commonly under- leton bone density measured through dual stood as a lack of implant movement im- energy X-ray absorptiometry (DEXA) (see Magnetic resonance imaging (MRI) of the jaw- mediately after placement. further) in the radius. bone The three most frequently used methods Nobel price winner Hounsfield (1980) Thin slice high-resolution MRI was used to gain an understanding of bone density described the quantitative calibration in for bone density and quantity assessment during implant placement are based on Hounsfield units, now frequently used in to allow proper implant planning in mand- biomechanical bone properties. The devices s all medical fields, in 1980. This X-ray ibles and maxillae (Gray et al. 1996). This used are Periotest (Medizintechnik, Gul- s attenuation unit is mostly used in com- technique can be used in patients where den, Bensheim, Germany), Osstell (Inte- puted tomographic scanning and charac- the use of ionizing radiation is contra gration Diagnostics, Gothenburg, Sweden) s terizes the relative density of a substance. indicated. So far, no publication could be and Osseocare (Nobel Biocare, Gothen- Each pixel is assigned a value between 1 found investigating the validity of deter- burg, Sweden). Another method could be and 1 k. The value of zero equals water, mining bone density through MRI. the subjective scoring of the surgeon using a andsofttissuesuchasmuscletissueequals pre-determined classification as mentioned þ 40, air ( 1000) and bone ( þ 50 to earlier (Trisi & Rao 1999). þ 2500). Quantitative cone beam-compu- Ordinal bone density classification of the jaw- bone based on panoramic and cephalometric s terized tomography (qCBCT) was com- radiographs Periotest measurements s pared with qCT (Aranyarachkul et al. In 1985, Lekholm & Zarb described a The Periotest device is a tapping device 2005). Both techniques used Hounsfield classification method to pre-operatively that measures the braking point when tap- units to score bone density. The correlation score bone density based on panoramic ping the implant surface (Aparicio et al. between both techniques was very signifi- radiographs. This classification was used 2006). Aparicio (1997) reported on 1182 cant; the ratings of the qCBCT were, how- worldwide because it is easy to use and Bra˚nemark implants inserted consecutively ever, higher than for the qCT method, does not involve a huge investment. Bass in 315 patients and followed for 8 years, which means an overestimation of bone & Triplett (1991) showed in their results on measuring PTVs at several time intervals. density when using the cone beam method. 1097 investigated Bra˚nemark implants in The two most important findings were the This should of course be taken into con- 303 jaws which bone density graded as four correlation of PTV post-operatively and sideration when performing implant plan- exhibited the greatest failure rate. Herr- secondary failure and the possibility of ning using the qCBCT radiographic mann et al. (2005) came to the same early detection (before fabrication of the visualization. finding. They investigated 487 sites, of superstructure) of a failing implant. which only 3% showed bone density, While the single PTV measurement has DEXA scan measurements of the jawbone four combined with an unfavorable anat- been shown to correlate (only descriptive The DEXA technique to measure bone omy. Jaffin & Berman (1991) also found a statistics) with the ordinal bone density density is frequently used to characterize high failure rate (35%) in type 4 bone. All classification, there is as yet no evidence fracture risk in large epidemiological stu- studies investigate bone density relation that it provides valid means to define dies. The precision of DEXA in human with implant outcome when implants primary stability (Lekholm & Zarb 1985;

126 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135 Table 1. Pre-operative methods of jawbone density assessment Authors Publication Type of the study Number of Question addressed Result date subjects Trisi & Rao 1999 Prospective 56 Correlation of ordinal classification of bone Interclass correlation analysis of variance investigated the difference quality with histomorphometric bone of one class with the overall score of data sets, it showed that classes density D1 (P ¼ 0.01) and D4 (P ¼ 0.0006) were significantly different from the total population, the clinical classes D2 (P ¼ 0.6) and D3 (P ¼ 0.4) were not significantly different Fanuscu & Chang 2004 In vitro cadaver humans Correlate micro CT with conventional CT General agreement between mCT and qCT was not noted Lindh et al. 1996 15 Correlation of qCT with bone mineral density Anterior mandible revealed higher values than posterior ones (BMD) (Po ¼ 0.05) and the variations between the mandibles was statistically significant (P ¼ 0.0001). This was investigated for qCT measurements and compared with the BMD histological, both showed the same results Nackaerts et al. 2006 In vitro cadaver humans 47 Correlation between DEXA bone The correlation coefficient between the aluminum equivalent values measurements and aluminum equivalent of and the areal BMD results of the DXA scan was 0.81 (Po0.001) intra-oral X-rays measuring the BMD of the same bone sample Southard et al. 2000 Prospective CT 41 Relation between bone density in the The density of the maxillary alveolar arch was most strongly related alveolar arches and other bone areas, to the density of the mandibular alveolar process (P ¼ 0.0006) but e.g. there was no relation found with other areas through DEXA measurements Hounsfield 1980 In vitro Descriptive method of measuring bone Descriptive method density through gray values on CT images Aranyarachkul et al. 2005 In vitro cadaver humans 9 Correlation between qCT and qCBCT A very high correlation between qCT and qCBCT (r ¼ 0.92–0.98) was discovered Denissen et al. 1999 In vitro cadaver humans 20 Correlation between mineral density and A very high correlation between DEXA density measurements and DEXA density measurements of trephine histomorphometric measurements could be detected (r ¼ 0.9995) biopsies Becker et al. 2000 Cohort study 98 The relation between osteoporosis and No substantial associations between pDEXA bone density scores and implant failure implant failures were observed (r ¼ 0.71–1.23, Po0.5) Gray et al. 1996 Descriptive study 12 Description of the MRI technique to visualize Descriptive method

2 | 127 bone anatomy and density Bass & Triplett 1991 Retrospective CT 274 The correlation between implant outcome There was no significant difference found in implant outcome and jaw bone anatomy, implant location and between the different scorings for jaw bone anatomy according to ln rlIp.Res. Impl. Oral Clin. age at implant placement the Lekholm & Zarb classification, there was a significant statistically better outcome for implants placed in the anterior lower jaw compared with the posterior lower jaw restored with fixed ol oedniyadipatstability implant and density Bone . Molly restorations (X2 ¼ 0.0001) and no difference could be found in implant outcome between the different ages at implant placement Herrmann et al. 2005 Retrospective CT 487 implants Identification of prognostic implant failures Bone quality 4 according to the Lekholm & Zarb classification was the jawbone quality with the highest failure rate (P ¼ 0.00013) Jaffin & Berman 1991 Retrospective CT 1054 implants Relation between bone quality according to Only descriptive statistics are available because of the low failure rate 17 the Lekholm & Zarb classification and Spl ) 06/124–135 / 2006 2), (Suppl. implant outcome Klemetti & 1997 In vitro cadaver humans The correlation between the BMD of the The changes in the mandibular cortex were significantly related to Kolmakow mandibular cortex and the ordinal the BMD of the buccal cortex (P ¼ 0.002) classification of the morphology of the inferior cortex on panoramic radiographs

CT, computed tomography; mCT, micro-computed tomography; qCT, quantitative-computerized tomography; DEXA, dual energy X-ray absorptiometry; qCBCT, quantitative cone beam-computerized tomography; MRI, magnetic resonance imaging. Molly . Bone density and implant stability

Truhlar et al. 1994). Furthermore, there is Other workers have measured insertion tions on Frialit-2 implants, showed a at present no evidence that the single report torque in N cm during placement of statistically significant increase in implant s of a measurement using the Periotest implants in pre-tapped sites (Ueda et al. success for the immediate-loaded implants device provides any predictive value of 1991) or when placing self-tapping im- if the insertion torque was higher than implant outcome. plants (Friberg et al. 1999a, 1999b, 2003; 20 N cm (Ottoni et al. 2005). The relative Johansson et al. 2004). Insertion torque in risk for implant failure was associated s Osstell measurements pre-tapped sites differs from thread-cutting with insertion torque for the test group Meredith et al. (1996) first published on forces measured with a screw tap or a self- where implants were loaded immediately their new resonance frequency device de- tapping implant. The major variable influ- (r ¼ 0.79, P0.007). veloped to investigate the height of the encing insertion torque when a threaded Clinical studies on immediate implant implant not surrounded by bone and the implant is inserted into a pre-tapped hole in loading have been using a predetermined stability of the implant/tissue interface bone is the relative tolerance of the thread level of insertion torque as an inclusion (Aparicio et al. 2006). profile of the tap and the implant fixture. If criterion (Hui et al. 2001; Calandriello A high correlation (r ¼ 0.84, P0.05) thread-cutting forces are excluded, then et al. 2003; Malo et al. 2003; Vanden was found when comparing the mean tor- insertion torque is a function of the com- Bogaerde et al. 2003; O¨ stman et al. 2005). que values of the upper/crestal portion with pressive stresses applied locally to the sur- These authors also used a modified surgical the resonance frequency values at implant rounding bone and friction at the implant– technique to improve initial stability by a placement (Friberg et al. 1999a, 1999b). bone interface. Moreover, many authors combination of thinner drill diameters, MkIV Bra˚nemark implants, however, in- have used the peak insertion torque value osteotomes, wide-platform implants and serted in low-quality bone show a lower as an indication of primary implant stabi- tapered implants. Although survival rates insertion torque and higher resonance fre- lity. For a parallel-walled Bra˚nemark type were high, the importance of high insertion quency than standard Bra˚nemark implants. of implant, the peak value is generated torque for the outcome is not known. This translates into better primary stability when the implant head is seated in the Concerns have been forwarded that a high with a reduction of the energy imparted marginal bone. For tapered implant de- insertion torque may lead to overcompres- into the bone at the implant site (O’Sulli- signs, a continuous increase of insertion sion and negative tissue effects. However, van et al. 2004a, 2004b). Many authors torque can be seen as a result of lateral Calandriello et al. (2003) could not see any correlated these resonance frequency mea- compression during insertion (O’Sullivan influence of torque (15–52 N cm) on mar- surements to deviations from the standard et al. 2000). The relationship between true ginal bone levels after 1 year in function. protocol. If these resonance frequency mea- cutting resistances insertion torque and Table 2 will clarify the impact of all studies surements can be related with pre-treat- peak insertion torque is presently not clear. discussed in this part of the discussion. ment determined bone quality, these High correlations between PTVs and in- correlations become very interesting for sertion torque force (R value 0.74579) Relation of primary stability with bone pre-treatment outcome prediction and for 75 implants installed in 12 fresh bovine density eventual altering of the protocol. However, ribs were also described (Tricio et al. 1995). The study of Truhlar et al. (1994) com- at present, no evidence that the single There is as yet, however, no evidence that pared PTVs in the different categories of the s report of a measurement using the Osstell insertion torque measurment provides a ordinal classification of Lekholm & Zarb device during implant placement provides valid means to define primary stability. (1985). The investigators found mean any predictive value of implant outcome. Three studies that evaluated the prog- PTVs at second-stage surgery of 3.82 nostic value of insertion torque measure- 3.04 for type 1, 3.7 3.06 for type 2, s Insertion torque measurements (Osseocare ) ments to predict future implant failure 3.3 3.2 for type 3 and 1.29 3.57 The use of cutting resistance measure- were found. Friberg et al. (1999a, 1999b) for type 4 quality bone. Another group ments to assess bone density during im- followed 523 Bra˚nemark implants for 3 correlated the same techniques and their plant surgery was first described by years, of which 412 were subjected to results show a different change of PTVs Johansson & Strid (1994). The technique cutting torque measurements. Comparison over time in densities 1 and 2 compared involved the measurement of torque cre- of the insertion torque values for 14 failed, with 3 and 4, which could indicate a better ated when cutting a thread in a hole in bone and 398 successful implants did not reveal bone-to-implant contact over time in better as determined by the current drawn by an any statistically significant differences. Si- bone densities (Morris et al. 2003). A electric motor. A decomposition procedure milar results were obtained by Johansson et similar finding was published in Truhlar was applied to eliminate torque compo- al. (2004), who used the same technique to et al. (2000); these authors added that nents resulting from frictional forces and evaluate 222 Bra˚nemark implants placed in hydroxyapathite-coated implants became shiver packing during the tapping course, grafted and non-grafted maxillae and fol- less stable over time in contrast with non- which, according to the authors, resulted in lowed for 1 year. There was no difference coated implants, which showed an im- a true profile of cutting resistance. Bone between 28 failed and 194 successful im- provement in stability over time. However, quality was expressed as the energy re- plants with regard to initial cutting torque PTV values at implant placement and quired to remove a unit volume of bone, value. A recent study, however, comparing thereafter should be better correlated with and for cortical bovine bone an in vitro the survival of immediately (test) or de- an objective bone density classification to measurement of 0.3 J/mm3 was quoted. layed (control) loaded single-tooth restora- obtain more specified information.

128 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135 Table 2. Per-operative assessment of primary stability Authors Publication Type of the Number of Question addressed Result date study subjects Trisi & Rao 1999 Prospective 56 Correlation of ordinal classification of Interclass correlation analysis of variance investigated the difference of one bone quality with histomorphometric class with the over all score of data sets, it showed that classes D1 (P ¼ 0.01) and bone density D4 (P ¼ 0.0006) were significantly different from the total population, the clinical classes D2 (P ¼ 0.6) and D3 (P ¼ 0.4) were not significantly different Aparicio 1997 Retrospective CT 315 The relation of the PTV at implant The percentage of secondary failures (implant outcome) was related to the insertion with different implant initial PTV corresponding to a borderline implant (only descriptive statistics) characteristics, e.g. implant outcome Meredith 1996 In vitro Verify if resonance frequency analysis can Resonance frequency analysis is reproducible (better than 1%) and there is a et al. give an idea of the bone tissue interface strong correlation (Po0.01) between the exposed height of an implant above and the bone level surrounding the mimicking bone and resonance frequency in vitro implant O’Sullivan 2004a, 2004b Prospective CT 13 The correlation of bone quality and The mean insertion torque for type IV bone according to the Lekholm & Zarb et al. implant stability classification was significantly different statistically from other types of bone for (P ¼ 0.05). No difference correlated with the type of bone could be found for the different implant types in this study Johansson 1994 In vitro cadaver 42 Correlation between cutting resistance of A linear correlation could be found represented in a graph & Strid animals the bone and the aluminum-referred density form X-ray assessment Ueda et al. 1991 In vitro cadaver 2 Relationship between insertion torque Removal torque was lower than insertion torque but no statistical analysis was humans and removal torque available Friberg et al. 1999a, 1999b Prospective CT 105 The correlation between cutting torque A high correlation was found between the insertion torque encountered at values and radiographically and clinically implant placement and the bone quality assessments (descriptive statistics) assessed bone quality scores Friberg et al. 1999a, 1999b Prospective CT 9 Implant stability comparisons at implant The insertion torque encountered during the first part of implant insertion was insertion using resonance frequency and highly correlated with the resonance frequency measurement at implant insertion torque placement (r ¼ 0.84, Po0.05) Friberg et al. 2003 RCT 44 The relation between primary and Resonance frequency at implant insertion was significantly higher (P ¼ 0.004) in secondary implant stability and the 1 year the test than in the control group. As for implant outcome there was no outcome of the implants with two difference between test and control (P ¼ 0.48) different surfaces 2 | 129 O’Sullivan 2000 In vitro cadaver 9 Correlation of primary stability of five The peak insertion torque encountered during insertion of MkIV is significantly et al human different implant types higher (Po0.05) compared to the insertion torque encountered during insertion of standard Bra˚ nemark implants, MkII and oxidized titanium implants. ln rlIp.Res. Impl. Oral Clin. The resonance frequency measured after insertion of MkIV implants was statistically significant better (Po0.05) compared with standard Bra˚ nemark implants ol oedniyadipatstability implant and density Bone . Molly Tricio et al. 1995 In vitro cadaver 12 The correlation between PTV There was a statistically significant correlation between the insertion torque animals measurements and insertion torque force and PTVs (R ¼0.75) and between the mean gray values of the selected during implant insertion and gray value area around the implants and PTVs (R ¼0.83) around the implant

17 Johansson 2004 RCT 40 The correlation between cutting Significantly higher torque values were required for placing implants in

Spl ) 06/124–135 / 2006 2), (Suppl. et al. resistance and particulate grafts (one stage) used in inlay grafts than for block grafts (two stage) used in only grafts (Po0.001). A strong correlation between insertion torque measurements and the estimates of bone quality according to the Lekholm & Zarb classification was found (Po0.001) Ottoni et al. 2005 RCT 23 The relation between failure rate and The relative risk for implant failure was associated with insertion torque for insertion torque in immediate and implants in the group of immediate loading (r ¼ 0.79, P 0.007) delayed loaded implants Calandriello 2003 Prospective CT 26 The relation between primary stability or Statistical analysis could not reveal relation between bone quality, bone et al. bone quality and quantity and marginal quantity or insertion torque and marginal bone loss or implant outcome bone loss or implant outcome Molly . Bone density and implant stability

Single resonance frequency analysis P0.001). A manuscript defining a strong measurements were evaluated at different correlation between computerized tomo- time points after implant placement with graphy values (Hounsfield values) and the ordinal Lekholm & Zarb classification the cutting torque values encountered of bone density measured on panoramic during implant placement (correlation radiographs (Zix et al. 2005). This study coefficient ¼ 0.77, P ¼ 0.01) was published did not find any significant relation and in 2005 (Ikumi & Tsutsumi 2005). When suggested that a follow-up over time of the implant torque values were compared with RFA values could elucidate better relations. the subjective scorings based on radio- Huang et al. (2002) tried to correlate RFA graphs according to the ordinal classifica- with different bone densities using finite tion of Lekholm & Zarb (Johansson et al. element analyses to mimic different bone 2004), only classes 2, 3 and 4 were de- qualities. RFA was computed with differ- tected. Lower torque forces were encoun- ent bone types and bone densities. Their tered when inserting the implant into type results show a linear decrease in RFA 4 bone, not only for the first part of implant values with a decrease in bone density. insertion but also for the middle and last These results must be interpreted with part. As for analysis of early implant out- caution concerning the non-isotrophic come, the insertion torque forces for suc- character of bone in vivo.Therelation cessfully osseointegrated implants were between resonance frequency measure- higher than for the failures. Whenever in- ments over time and bone density mea- sertion torque shows correlation with pri- sured according to the ordinal Lekholm & mary oral implant stability or with Zarb classificiation based on radiographs prediction of implant outcome, a sugges-

There was no statistical difference found at any time was investigated (Barewal et al. 2003). tion for adaptation of the surgical technique The resonance frequency measurements can be possible. were performed at surgery and every week Table 3 will clarify the impact of all studies thereafter up to 6 weeks after surgery. The discussed in this part of the discussion. lowest resonance frequency measurement was found at 3 weeks for all groups of bone Possible adaptation methods of the density. The decrease in resonance fre- surgical protocol with regard to jawbone quency was the largest in the group with density bone density graded as 4 (8.6%); in the Before starting this discussion, one must be same group, the increase between weeks aware that in the literature, many studies 3 and 6 in resonance frequency was the were conducted to compare two techniques largest of all groups (26.9%). These differ- but only a few proved that the difference ences between groups were, however, only between both techniques is really due to the low or high bone densities present. measurements at implant insertionovertime and in immediately loaded implants and implants loaded accordingstandard to protocol the Question addressed Result statistically significant for groups 1 and 4 bone density at the 3-week follow-up. This is probably again due to the subjective Adaptation of the surgical technique origin of the classification method used. Several papers suggest the use of osteo-

Number of subjects Insertion torque measurements retrieved tomes in the placement of oral implants from 31 implants placed in 10 human in the posterior maxilla or maxillary tuber- cadaver jawbones were compared with mi- osity (Komarnyckyj & London 1998; No- croradiographical bone density analysis and cini et al. 2000; Toffler 2001). Most papers morphometric analysis (Friberg et al. only suggest the low bone density in the 1995). A statistically significant relation region of interest but do not test the bone

Type of the study was found between the peaks of bone density. Toffler (2001), when investigating density retrieved from the microradio- the use of osteotomes with internal sinus graphs and the peaks of insertion torque elevation, even concludes that histological retrieved from implant placement for each and clinical comparisons for the traditional implant site (r ¼ 0.90, P0.001). Another lateral sinus elevation were lacking. Roc- 2003 Prospective CT 36 Follow-up over time Only descriptive statistics available date statistically significant relation was found cuzzo & Wilson (2002) published a manu- for the correlation between total bone area script on the use of acid-etched implant surrounding the inserted implant measured placement in combination with the use of

. Continued morphometrically on microradiographs and osteotomes in preparation of the implant stman et al. 2005 Prospective CT 20 Comparison in resonance frequency

¨ the mean cutting resistance values occur- site. They also suggested that the bone in O Hui et al.Malo et al.Vanden Bogaerde 2001 2003et al. Prospective CT Prospective CT 24 76CT, computed tomography; RCT, randomized-controlled trial. Follow-up over Follow-up time over time Descriptive article Only of descriptive the statistics technique available of immediate provisional restoration Authors Publication

Table 2 ring during implant insertion (r ¼ 0.74, the posterior maxilla has a poor quality. In

130 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135 Molly . Bone density and implant stability

conclusion, a 6-week healing period allows successful primary osseointegration before loading based on clinical and radiographic measurements post-operatively and 1-year 0.001)

o follow-up. They conclude that long-term P follow-up is necessary to observe mainte- nance of osseointegration over time. An investigation the role of human re- 0.004), after 5 weeks no

¼ combinant tissue factor, platelet-rich P

0.038, Hotelling’s Trace) plasma and tetracycline in the improve- o 0.001) P ment of bone density of a human calvaria o

P bone graft was performed (Philippart et al. 2003). Six months after the sinus floor augmentation procedure, bone cores were extracted for microscopic analysis and im- 0.001). A strong correlation between insertion

o plants were placed. Histology revealed vas- P

0.001, Hotelling’s Trace). Non-coated implants show cularized connective tissue rich in lamellar o P 0.001) and the correlation between total bone area and bone specula; however, no histomorpho- o 0.0001) P during implant planning, a significant linear relationship was metry was performed. Thus, no correlation o P ( of bone density with a standard bone sam- 0.01) with correlation coefficient of 0.77

in vitro ple can be performed. A control group to ¼ P

in vitro compare implant outcome was not present. There is no evidence that the discussed The only difference inbetween resonance implants frequency inserted measurements in was types observed 1 and 4 bone ( No statistically significant correlationfrequency could at be implant found placement between and the the resonance type of bone present more differences could be observed mean cutting resistance values also showed a positive relation ( Description of a finitefrequency element analysis model infound the detection of resonance The correlation between thehighly bone correlated density ( and cutting resistance peaks was A significant correlation betweenfound cutting ( resistance and CT values could be better PTV values than HA-coated implants ( Descriptive statistics The differences in thestatistically changes different in ( the PTVs for each bone quality were torque measurements and theLekholm estimates & of Zarb bone classification quality was according found to ( the Significantly higher torque valuesparticulate were grafts required (one for stage) placingstage) used implants used in in in inlay only grafts grafts than ( for block grafts (two manuscripts have proven the influence of bone density on implant outcome for the largest part because the bone density as- sessment mostly performed has not been validated.

Adaptation of the implant design In 2000, the initial stability of five different implant designs was compared in fresh hu- man cadavers (O’Sullivan et al. 2000). The standard Bra˚nemark implant was compared with the MkII self-tapping Bra˚nemark im- plant, the MkIV-tapered self-tapping Bra˚ne- s mark implant, the Astra Tioblast (Astra frequency measurements and thebone kind available of based on theclassification Lekholm for & bone Zarb quality values and the type of bone present Is it possible to develop aresonance technique to frequency define of animplant implant placement before and bone quality basedmicroradiography on and morphometric analysis bone and cutting resistanceplacement at implant Verification if different PTV in differentdensities bone occurs measurements defined by theZarb Lekholm classification & and bone grafting Question addressed Result Tech AB, Molndahl, Sweden) implant and s the 3i Osseotite (3i[Implant Innovations Incorporated], Palm Beach, Florida, USA) implant. Peak insertion torque, resonance frequency measurements and removal tor- 35 Correlation between resonance frequency 10 The correlation between cutting resistance Number of subjects 1838 implants Correlate PTV with bone density Descriptive statistics que measurements gave an impression of the primary stability of the implants and these measurements were compared with the previously determined bone quality CT In vitro In vitro cadaver human In vitro Type of the study CT assessed with the ordinal Lekholm & Zarb classification on the basis of oral radiographs. The MkIV Bra˚nemark implant showed statistically significant higher peak

date insertion torque values than the standard Bra˚nemark implant, the MkII Bra˚nemark s implant and the 3i Osseotite implant, and also showed statistically significant higher

. Relation between primary stability and bone density resonance frequency values than the stan- dard Bra˚nemark implant. In type 4 bones, Barewal et al. 2003 Prospective CT 20 The correlation between resonance Zix et al. 2005 Retrospective Huang et al. 2002 Friberg et al. 1995 Ikumi & Tsutsumi 2005 Prospective CT 13 The correlation between CT values of the Lekholm & ZarbMorris et al. 1985 2003 Descriptive Set-up of a classification Description of a classification Authors Publication CT, computed tomography; RCT, randomized-controlled trial. Truhlar et al. 2000 Prospective CT 2900 implants Correlation of PTV with bone quality Johnasson et al. 2004 RCT 40 The correlation between cutting resistance Truhlar et al. 1994 Retrospective

Table 3 the MkIV Bra˚nemark implant maintained a

131 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135 3 | 132 Table 4. Possible adaptation methods of the surgical protocol in regard to jawbone density stability implant and density Bone . Molly Authors Publication Type of Number of Question addressed Result date the study subjects ln rlIp.Res. Impl. Oral Clin. Toffler 2001 Descriptive Description of the technique: apical alveolar Description of the technique displacement with osteotomes Nocini et al. 2000 Case report Description of osseous distraction through Description of the technique the use of osteotomes Komarnyckyj & 1998 Prospective CT 16 Detecting if the use of osteotomes in sinus A statistically significant difference between the initial situation and the London elevation procedure is effective situation after bone augmentation by means of osteotomes could be

17 detected (Po0.01)

Spl ) 06/124–135 / 2006 2), (Suppl. Philippart et al. 2003 Prospective CT 18 The use of implants in sinus augmentation Descriptive statistics procedures O’Sullivan et al. 2000 In vitro cadaver 9 Correlation of primary stability of five The peak insertion torque encountered during insertion of MkIV is human different implant types significantly higher (Po0.05) compared with the insertion torque encountered during insertion of standard Bra˚ nemark implants, MkII and oxidized titanium implants. The resonance frequency measured after insertion of MkIV implants was significantly better statistically (Po0.05) compared with standard Bra˚ nemark Implants Astrand et al. 2003 Cohort study 40 Evaluating the difference between the MkVI Descriptive statistics implants and the standard Bra˚ nemark implants Mordenfeld et al. 2004 Retrospective CT 52 Follow-up over time Descriptive statistics O’Sullivan et al. 2004a, 2004b Animal study 6 Differences in primary and secondary Only higher resonance frequency measurements could be detected while stability between tapered and straight using short (6 mm) implants in the tibea when comparing those results at implants implant insertion for the tapered implants compared with the straight ones (P ¼ 0.0275). For 10 mm implants no significant statistical difference could be detected. The implants placed in the femur show a higher insertion torque for the test implant compared with the control implant (P ¼ 0.0005) Glauser et al. 2003 Prospective CT 38 Presenting short-term success rate of surface- Descriptive statistics modified immediate occlusally loaded implants Khang et al. 2001 RCT 97 The comparison between two similar Dual acid etched implants were significantly more successful than machined implants with different surface surfaced implants (Po0.01). No significant statistical relation with bone characteristics quality according to the Lekholm & Zarb classification could be detected Iezzi et al. 2005 CT 8 Histological and histomorphometrical Descriptive statistics analysis of the bone response to submerged implant inserted in human jaw bone after certain healing periods Quirynen et al. 2005 Retrospective CT 539 Find predisposing conditions for peri-apical The incidence of retrograde peri-implantitis was significantly higher lesions and to evaluate treatment strategies (Po0.0001) for Ti-Unite implants when compared with the machined implants Salonen et al. 1997 Retrospective CT 74 Detecting differences between ITI implants No real correlation between ITI and TPS was established; only descriptive TPS implants statistics were made to verify that Bass & Triplett 1991 Retrospective CT 274 The correlation between implant outcome There was no significant difference found in implant outcome between the and jaw bone anatomy, implant location and different scorings for jaw bone anatomy according to the Lekholm & Zarb age at implant placement classification, there was a significantly better outcome statistically for implants placed in the anterior lower jaw compared with the posterior lower jaw restored with fixed restorations (X2 ¼ 0.0001) and no difference could be found in implant outcome between the different ages at implant placement

CT, computed tomography; RCT, randomized-controlled trial. Molly . Bone density and implant stability high primary stability in contrast with all group was included in this study. PTV based on the ordinal scoring on radiographs other types tested. The relation between values of ITI (Straumann, Basel, Switzer- according to the Lekholm & Zarb classifi- outcome of tapered MkIV Bra˚nemark im- land) implants show higher values than cation showed no statistical difference in plants and soft bone quality was questioned those of titanium plasma-sprayed implants, the implant outcome for the different ordi- (Astrand et al. 2003). In a test group, which means a better stability for the rough nal categories (Bass & Triplett 1991). The patients were treated with the tapered surface implants (Salonen et al. 1997). same held true for the implant outcome of MkIV Bra˚nemark implants and in a control Two different surface types were placed implants supported with a removable group the standard MkII Bra˚nemark im- in various bone qualities (Khang et al. superstructure. This group, however, did plants. Investigators suggested a lower 2001). The surgeon assessed bone quality find a significant difference of implant out- bone quality in the upper jaw. However, during implant placement using a subjec- come related to the positioning of the im- no correlation between bone quality mea- tive classification (dense, normal and soft). plant in the jaw. These two findings surements and implant outcome was de- The analysis of implant performance re- contradict one another and therefore we scribed. The results for both implant lated to bone quality revealed statistically could question the validity of the Lekholm systems do not show any statistical differ- significant results. Cumulative success & Zarb classification in its additional ben- ence but in the conclusions they do state rates (CSR) at the 4-year follow-up were efit to investigate bone quality effect on that the MkIV implant demonstrates an 93.8% and 87.8% for acid-etched and ma- different deviations from the standard improved survival rate compared with ear- chined surface, respectively, in dense bone protocol. lier results of other Bra˚nemark implants quality; as for the soft bone quality, the There is no evidence that the discussed placed in soft-quality bone. CSRs were 96.8% and 84.8%, respec- manuscripts have proven the influence of The survival rate of wide-platform MkII tively, which is even far more significant. bone density on implant outcome for the Bra˚nemark implants in the posterior mand- Eight implants were retrieved from a hu- largest part because the bone density as- ible and maxilla was questioned while sup- man jawbone with a trephine burr (Iezzi sessment mostly performed has not been posing that the bone quality in these areas et al. 2005). All implants were submerged validated. was lower than in other regions (Morden- and unloaded at the time of retrieval; the Table 4 will clarify the impact of feld et al. 2004). The authors suggested that reason for retrieval was different in most all studies discussed in this part of the wide-platform implants present an accepta- cases but was not disintegration. The bone- discussion. ble treatment alternative; they, however, to-implant contact varied considerably (30– did not set up a true correlation with bone 90%) but rough surface implants showed a quality and did not include a control group. faster osseointegration on the histological Conclusion Another study of the group of O’Sullivan evaluation. It was extrapolated that rough tested the differences in primary stability surface implants can be loaded successfully Many different bone density assessments for different tapering of implants in rabbit after 2 months even when inserted in soft are available at the moment. Most of these tibea and femur (O’Sullivan et al. 2004a, bone. The term soft bone was, however, show good correlation with one another. In 2004b). The insertion torque and resonance not defined, and neither was bone quality clinical studies investigating implant stabi- frequency analysis revealed a higher inser- assessed before implant placement. The lity or treatment outcome of different pro- tion torque for both grades of tapering relation between surface topography and tocols, however, mostly the subjective compared with the standard Bra˚nemark origin of failure was illustrated (Quirynen ordinal scoring by means of radiographs is implants; the resonance frequency analysis et al. 2005). Ti-Unite Bra˚nemark implants being used. This scoring showed that it is revealed that it depended on the kind of showed higher retrograde peri-implantitis only possible to detect extremely soft bone, bone the implant was inserted in and prob- than machined surface implants. The over- which occurs only in 3% of the patients. ably related to the bone quality, but unfor- all failure rate, however, was considerably This means that less than 1% of the fail- tunately this was not tested. higher for machined surface implants than ures can be detected with this technique. It for the Ti-Unite implants. The faster pri- was, however, possible to detect that im- Adaptation of the implant surface mary osseointegration process achieved plant stability in soft bone quality shows Glauser et al. (2003) investigated whether with these modified surface implants thus the lowest resonance frequency measure- the changed surface characteristics and the allows a lower implant failure rate and a ments after 3 weeks and that these mea- tapered design of the MkVI Ti-Unite possibility for early detection of retrograde surements show extremely increased Bra˚nemark (Nobel Biocare, Gothenburg, peri-implantitis at frequent patient follow- values, especially in the soft bone after 6 Sweden) implants could have a beneficial up visits. This early detection of retrograde weeks. To determine specifically, how- effect on immediate loading. Implants were peri-implantitis should be performed ever, at what stage implants can be suc- mainly inserted in soft bone (76%) (Glau- through bone quality comparisons over cessfully loaded, more elaborate bone ser et al. 2003). The bone quality was time postsurgery. density detection should be performed. measured by the ordinal Lekholm & Zarb Histomorphometric techniques show very classification based on radiographs. The Adaptation of the loading protocol good results of correlations between area of outcome of 97.1% after 1 year is high Data looking at implant outcome of im- bone present in the vicinity of the implant when compared with other imme- plants supported with a fixed superstruc- and primary implant stability measure- diate loading studies; however, no control ture and the correlation with bone quality ments, and bone-to-implant ratio and

133 | Clin. Oral Impl. Res. 17 (Suppl. 2), 2006 / 124–135 Molly . Bone density and implant stability primary stability. This technique, how- could adapt treatment planning to obtain a bone densities, many studies suggest but ever, implies another surgical intervention better outcome. only a few prove a different outcome be- and an extra cost and is thus difficult to Periotest and insertion torque values and cause mostly no elaborate bone density implement clinically. It could, however, resonance frequency analysis could give measurements were performed pre-opera- give additional information if correlated important information on implant stability tively. with another technique clinically used in and implant outcome, primary failure or bone density measurement. An integration secondary. The correlations of these mea- of the newly developed finite element ana- surements with pre-evaluated bone quality lysis model (Olsen et al. 2005) in pre- are important for future treatment plan- Acknowledgement: I would like to operative computer planning systems ning. Especially for resonance frequency acknowledge working group 3 and all could help, together with a standardized measurements, the follow-up over time is its attendees: Neukam, F. W., Flemming, qCT (e.g., based on Hounsfield units) clas- extremely important to make correlations T. F., Bain, C., Chiapasco, M., Esposito, sification, to better understand the relation with implant outcome. M., Gottfredsen, K., Jung, R., Lekovic, of bone density and primary or secondary As for the impact of the surgical techni- V., Mombelli, A. & Schou, S., for their implant failure. Based on these results, one que on implant outcome in different support and cooperation.

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