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ARTICLE IN PRESSG ModelANAT-50847; No. of Pages 7

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Contents lists available at ScienceDirect

Annals of Anatomy

j ourna l h omepage: www.elsev ier .de /aanat

fficacy of biologically guided implant site preparation to obtaindequate primary implant stability

duardo Anituaa,b,∗, Mohammad Hamdan Alkhraisatb, Laura Pinasb,c, Gorka Orivec

Private Practice in Oral Implantology, Vitoria, SpainEduardo Anitua Foundation, Vitoria, SpainPrivate Practice in Implant Prosthodontics, Madrid, Spain

r t i c l e i n f o

rticle history:eceived 12 November 2013eceived in revised form 25 January 2014ccepted 19 February 2014vailable online xxx

eywords:one drilling

nsertion torqueone typeone density

s u m m a r y

The primary stability of dental implants is essentially influenced by the quality and quantity of hostingbone. To study the effects of adaptation of the drilling protocol to the biological quality of bone estimatedby bone density and cortical/cancellous bone ratio, 8.5 mm-short implants were placed in different bonetypes by adapting the drilling protocol to result in a socket under-preparation by 0.2, 0.4, 0.7, 1 and 1.2 mmin bone types I, II, III, IV and V, respectively. The effect of the drilling protocol was studied on implantinsertion torque and osseointegration. Additionally, we analyzed the relationship of demographic dataand social habits to bone type and insertion torque. Then the correlation between insertion torque andbone quality was tested. One hundred ninety two patients (mean age: 62 ± 11 years) participated with295 implants. The most common bone type at implant site was type III (47.1%) followed by type II (28.1%).Data analysis indicated that gender, age, and social habits had neither correlation with bone type nor with

sseointegration insertion torque. The insertion torque was 59.29 ± 7.27 Ncm for bone type I, 56.51 ± 1.62 Ncm for bonetype II, 46.40 ± 1.60 Ncm for bone type III, 34.84 ± 2.38 Ncm for bone type IV and 5 Ncm for bone typeV. Statistically significant correlation was found between bone type and insertion torque. The followeddrilling protocol adapts socket under-preparation to the needs of establishing a sufficient primary stabilityfor implant osseointegration.

© 2014 Published by Elsevier GmbH.

. Introduction

The success and wide acceptance of implant dentistry as the firsthoice in replacement of missing teeth is based on the outcomef bone and implant interaction in a process known as osseointe-ration (Meyer et al., 2012). This dynamic process is significantlynfluenced by the quality of housing bone and the primary stabilityf the implant.

Bone quality is a collective term referring to the mechani-al properties, architecture, degree of mineralization, chemicalomposition and remodeling properties of bone (Shapurian et al.,006). Several classification systems have been formulated to helphe clinicians in describing the quality of bone using common

Please cite this article in press as: Anitua, E., et al., Efficacy of biologicimplant stability. Ann. Anatomy (2014), http://dx.doi.org/10.1016/j.aa

erms (Lekohlm and Zarb, 1985; Misch, 1990; Trisi and Rao, 1999),lthough the most accepted system in the field of oral implan-ology is that of Lekohlm and Zarb (1985) (Bergkvist et al., 2010;

∗ Corresponding author at: Eduardo Anitua Foundation, C/Jose Maria Cagigal 19,1007 Vitoria, Spain. Tel.: +34 945160653.

E-mail address: eduardoanitua@eduardoanitua.com (E. Anitua).

ttp://dx.doi.org/10.1016/j.aanat.2014.02.005940-9602/© 2014 Published by Elsevier GmbH.

Ribeiro-Rotta et al., 2012). Lekohlm and Zarb classified bone qual-ity into four categories (Types I–IV) according to bone composition(ratio between compact bone and spongy bone) and the subjectivebone resistance when drilling. The presence of compact bone andbone resistance decreases from bone type I to bone type IV. Sev-eral articles have corroborated the validity of Lekohlm and Zarbclassification by analyzing its correlation with the outcomes of his-tomorphometric analysis, measurements of bone mineral densityand variables of computed microtomography (CT) (Bergkvist et al.,2010; Pereira et al., 2013; Ribeiro-Rotta et al., 2011).

Periera et al. have found a correlation between the Lekohlm andZarb classification and the histomorphometric parameters of bonevolume, density, bone surface, thickness of the bone trabeculae,and inter-trabecular space (Pereira et al., 2013). Bergkvist et al.calculated the bone mineral density (BMD) using the Hounsfieldunits obtained from a CT scan and found a significant correlationbetween the BMD and Lekohlm and Zarb classification (Bergkvist

ally guided implant site preparation to obtain adequate primarynat.2014.02.005

et al., 2010). Ribeiro-Rotta et al. have also found a significantcorrelation with values of microtomography in relation to bonearchitecture, density and volume (Ribeiro-Rotta et al., 2012).Accordingly, these results support the clinical use of the Lekohlm

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nd Zarb classification for the assessment of bone quality and thestablishment of a specific treatment plan based on this property.he other parameter crucial to implant osseointegration is therimary stability of the implant (Lopes and König Júnior, 2002).his biometric parameter is the result of mechanical anchoragedirect contact) of the implant to the hosting bone (Sennerbynd Meredith, 1998) and is quantitatively measured immediatelyfter implant insertion. The main function of primary stabilitys to prevent excessive implant micro-movements in order tossure healthy bone remodeling around the implant and, thus, itssseointegration (Szmukler-Moncler et al., 1998). Several studiesave indicated that the tolerated threshold of micro-movements

s between 50 and 150 �m (Akagawa et al., 1986; Galindo-Morenot al., 2012; Pilliar, 1991). Brunski et al. reported that there is aritical limit below 100 �m that is considered a functional stimulusenerating no negative effect on bone regeneration around themplant (Brunski, 1999). Davies suggests that excessive implant

icro-motion may interfere with the formation of the fibrin clotn the implant surface during early wound healing (Davies, 1998).herefore, the primary stability allows bone formation around themplant increasing the bone to implant contact to provide the sec-ndary stability of the implant. This secondary stability depends onhe factors previously mentioned in addition to host factors (bloodupply to the wound) and surface characteristics of the implantDavies, 2003; Nevins et al., 2012; König Júnior et al., 1998).

Implant primary stability is the net outcome of quantity anduality of hosting bone, the design of the implant, and the sur-ical procedure (drilling technique) (Rabel et al., 2007). Implantacro-design is a parameter significantly influencing implant pri-ary stability. Self-tapping implants incorporate a cutting edge in

he apical part of the implant to avoid the need of using tappingrocedures during socket preparation. The purpose of this design

s to enhance the primary stability of the dental implant, particu-arly in low density bone (Markovic et al., 2013; Olsson et al., 1995).linically, it can be measured by several methods like the insertionorque peak and the resonance frequency analysis (RFA). However,n the scientific literature, there is a discrepancy between studiesn the correlation of the insertion torque and the implant stabil-ty quotient (ISQ) (Barewal et al., 2012; Friberg et al., 1999). Thisiscrepancy is due to differences in the working principles of bothechniques: the insertion torque measures the rotational stiffnessf the implant-bone interface while the resonance frequency anal-sis evaluates the axial stiffness of this interface (Barewal et al.,012).

After determination of the importance of implant primary sta-ility, clinical research has been conducted to evaluate the optimalalue of the insertion torque to ensure implant osseointegration.ngelke et al. have concluded that an insertion torque greater than0 Ncm is advisable to obtain adequate primary stability and aorque value ≤11 Ncm is considered a risk factor increasing theikelihood of implant failure (Engelke et al., 2013).

The objective of this study has been to evaluate the efficiency ofdaptation of the drilling protocol to the quality of bone in achievingdequate primary stability and minimizing the risk of implant fail-re at the early stage of osseointegration. This biologically drivenrilling protocol will help to systematize the under-preparationf implant socket in a reproducible manner. Under-preparation ofmplant sockets would have the advantages of local optimizationf bone density, increase in the insertion torque and primary sta-ilization of the implant, and increase the bone-to-implant contactFriberg et al., 1999; Tabassum et al., 2011). For this purpose, thealues of bone density obtained from cone-beam CT scan and bone

Please cite this article in press as: Anitua, E., et al., Efficacy of biologicimplant stability. Ann. Anatomy (2014), http://dx.doi.org/10.1016/j.aa

omposition (cortical and trabecular bone) have been used to assesshe bone quality and determine the diameter of the last drill usedefore the insertion of the dental implant. The goal is to insert the

mplant at an insertion torque of 30 Ncm.

PRESSomy xxx (2014) xxx–xxx

2. Materials and methods

In this retrospective study, patient records were reviewed toidentify patients who had received dental implant therapy. Theinclusion criteria were patients aged over 18 years, the insertionof 8.5 mm-long implants, implants insertion in pristine bone, thepresence of information on bone type, insertion torque, and implantfailure and/or prosthetic rehabilitation. Patients/implants that didnot meet these criteria were excluded from the study.

Prior to surgery and in order to make a proper treatment plan, allpatients had undergone a standard diagnostic protocol consistingof review of the medical and dental history, diagnostic casts, andradiographic evaluation (panoramic radiographs, when available,and cone-beam CT scan). The cone-beam CT scans were analyzedwith diagnostic software (BTI Scan II, Biotechnology Institute, Vito-ria, Spain) to measure both the residual bone height and the bonedensity at future implant sites. Bone density and the thickness ofthe cortical bone were the two parameters used to propose a bonetype classification that would help in determining the diameter ofthe final drill used before implant insertion:

- Bone Type I: Bone density greater than 1000 HU and composedmostly of cortical bone. It corresponds to Lekohlm & Zarb type Ibone.

- Bone Type II: Bone density of 850–1000 HU, composed of3–4 mm-thick cortical bone surrounding a dense cancellous bone.It corresponds to Lekohlm & Zarb type II bone.

- Bone Type III: Bone density of 550 to <850 HU, composed of2 mm-thick cortical bone surrounding a dense cancellous bone. Itcorresponds to Lekohlm & Zarb type III bone.

- Bone Type IV: Bone density of 400 to <500 HU, composed of0.5–1 mm thick cortical bone surrounding cancellous bone. It cor-responds to Lekohlm & Zarb type IV bone.

- Bone type V: Bone density of 100 to <400 HU, composed mostly ofcancellous bone. It corresponds to Lekohlm & Zarb type IV bone.

2.1. Preparation of autologous platelet concentrate

Plasma rich in growth factor was prepared using PRGF-EndoretKit (BTI, Vitoria, Spain). Briefly, citrated venous blood was cen-trifuged at 480 g for 8 min to separate blood components. Then,the plasma column was fractionated into fraction 2 (F2) defined asthe 2 ml of plasma above the buffy coat and fraction 1 (F1) definedas the plasma column above the F2. Activated fraction 1 (F1) wasemployed to prepare a fibrin membrane that covered the surgicalarea before flap closure and activated fraction 2 (F2) was injectedinto the implant bed and at the incision boarders. This fraction wasalso used to moisten the dental implants before insertion.

2.2. Flap elevation and bone drilling

Patients received 1 g of amoxicillin 1 h before surgery and 1 gof acetaminophen 30 min before surgery, respectively. Under localanesthesia, a full-thickness flap was reflected to expose the alveolarcrest for implant site preparation.

Bone drilling was performed at low velocity (150 rpm) withoutirrigation and the drilling sequence followed for the insertion ofthe 8.5 mm-long implants was adapted to the bone type as to theselection of the diameter of the last bone drill used before implantplacement. The diameter of the last drill was 0.2, 0.4, 0.7, 1 and1.2 mm smaller than the diameter of the implant in bone types I,

ally guided implant site preparation to obtain adequate primarynat.2014.02.005

II, III, IV and V, respectively. This permitted the under-preparationof the implant socket by 3.6%, 7.3%, 12.7%, 18.2%, and 21.8% for animplant with a diameter of 5.5 mm inserted in bone types I, II, III,IV and V, respectively.

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ig. 1. Bone drilling sequence employed to prepare the implant bed for an implant

Fig. 1 showed the full drilling sequence for the preparationf the implant bed for the placement of an implant of 5.5 mm.one drilling was started with initial drills at 850–1000 rpm with

rrigation. Bone drilling was then continued at 150 rpm withoutrrigation. The final drill was inserted to the full length of themplant socket prepared in bone types III, IV, and V while it wasnserted to 35% and 75% of the implant length for bone types I andI.

.3. Implant placement

BTI 8.5 mm-long implants (BTI, Vitoria, Spain) were wetted withctivated fraction 2 of the PRGF-Endoret. These cylindrical implantsad an acid etched surface and a self-tapping apex of 1.5 mm in

ength. The implants were inserted with a surgical motor at annsertion torque of 25 Ncm and then continued manually to finishhe implant placement. When high value of the insertion torqueas needed to completely insert the dental implant, the implantas removed, the final drill or the drill of the next diameter was

e-inserted into the socket, and the implant was then placed intohe socket. The final insertion torque was registered in the patient’secord. After the surgical site was covered with a fibrin membrane,he flap was repositioned and closed with 5/0 monofilament suture.ctivated fraction 2 of the PRGF-Endoret was injected at the inci-ion borders.

.4. Follow-up

Visits were scheduled according to the needs for prostheticehabilitation and the visit after 10 days was for suture removal.

.5. Statistical analysis

The patient was the statistical unit for the description of demo-raphic data, social habits, bruxism, medical history and historyf periodontal disease. Mean and standard deviations were calcu-ated for the age variable while relative frequency was calculatedor the rest of patient-related variables. The implant was the sta-

Please cite this article in press as: Anitua, E., et al., Efficacy of biologicimplant stability. Ann. Anatomy (2014), http://dx.doi.org/10.1016/j.aa

istical unit for the statistical description of implant location, boneype and insertion torque. Mean and standard deviation were calcu-ated for insertion torque values. Relative frequency was calculatedor implant location and bone type.

diameter of 5.5 mm. The diameter of the final drill is determined by the bone type.

Shapiro–Wilk test was performed to evaluate whether the dataof insertion torque and bone type followed a normal distribution.Table 1 summarized the type of test applied to analyze the rela-tionship between gender, age, smoking and bone type and therelationship between gender, age, smoking, implant diameter andbone type on insertion torque. The statistical significance was set atp < 0.05. All the statistical analyses were performed using the SPSSv15.0 for Windows statistical software package (SPSS Inc., Chicago,IL, USA).

3. Results

3.1. Demographic outcome

One hundred ninety two patients met the inclusion criteria hav-ing a total of 295 implants with a length of 8.5 mm. The mean ageof the participants was 62 ± 11 years (range 36–92 years) and 75%of patients were females. A summary of the most relevant data ispresented in Table 2.

3.2. Bone quality

Bone type III was the most common type of bone and presentin 47.1% of the implantation sites. Bone type II was the hostingbone for 28.1% of the implants and bone type IV was presentaround 21.7% of implants. Bone type I and bone type V was foundaround 2.4% and 0.7% of the implants. The drilling protocol allowedthe insertion of the dental implants at an insertion torque of46.76 ± 19.66 Ncm whereas almost 80% of the implants had aninsertion torque ≥25 Ncm and 73.6% ≥30 Ncm. Only 8.8% of theimplants were inserted at a torque value ≥70 Ncm and 9.5% of theimplants had an initial torque ≤15 Ncm. In all, 49.5% of the implantswere placed in one surgical stage and 50.5% in two surgical stages.The implants were inserted in the molar (74.9%), premolar (18%)and anterior (7.1%) areas. About 55.6% of the implants were placedin the maxilla and 44.4% in the mandible.

3.3. Statistical analysis

ally guided implant site preparation to obtain adequate primarynat.2014.02.005

3.3.1. Gender and ageThe frequency analysis of bone type in female patients demon-

strated the following order, in descending manner: bone type III,

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Table 1Summary of the statistical analysis of factors that may influence bone type and insertion torque.

Dependent variables Factor Normality Test P-value

Bone type Gender No �2 0.259Age No Kruskal–Wallis 0.433Smoking No �2 0.657

Insertion torque Gender No Mann–Whitney 0.619Age Yes Pearson correlation test 0.152Smoking No Kruskal–Wallis 0.147Diameter No Spearman’s correlation test 0.829Bone type No Kruskal–Wallis 0.00

Table 2Summary of demographic data of 192 patients who met the inclusion criteria.

Patients data (number of patients) Patients data (number of patients)

Gender Females (144); males (48) Relevant medicalhistory

Radiotherapy (1)Chemotherapy (2)Diabetes mellitus (4)Hypertension (13)Cardiovascular disease (7)Psychological disorders (4)

Age (years) 62 ± 11 Neurological disease (4)Social habits Smoking (31); daily alcohol

consumption (4)Hyperthyroidism (5)

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Periodontal disease (Armitage, 1999) Present (77)

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one type II, bone type IV and bone type I (Fig. 2). This frequencyrder was also maintained in males with the only difference beinghat, in two female patients, the bone density was below 400 HUndicating the presence of bone type V. The statistical analysis ofhe influence of patient gender on the bone quality indicated thebsence of a significant association between the two variables.

The results of the statistical analysis between age and bone typendicated that age was not a parameter significantly influencingone type. The frequency of the different bone types according toge was the same as that encountered for the gender variable.

Furthermore, we studied the relationship between gen-er, age, and the insertion torque. The insertion torque was

Please cite this article in press as: Anitua, E., et al., Efficacy of biologicimplant stability. Ann. Anatomy (2014), http://dx.doi.org/10.1016/j.aa

8.04 ± 2.06 Ncm for men and 46.23 ± 1.36 for women. Patientsged up to 65 years had an insertion torque of 47.78 ± 1.48 Ncm,hile patients aged over 65 years had a value of 44.96 ± 1.81. The

ig. 2. The bone type present at the implant sites according to patient gender.

Rheumatoid arthritis (2)Anemia (1)Asthma (1)

statistical analysis indicated no significant effect of gender and ageon the insertion torque values.

3.3.2. SmokingIn all, 39 implants were inserted in patients who smoked up to

10 cigarettes/day and 31 implants in patients who smoked morethan 10 cigarettes/day. The hosting bone was type II in 25.6%, typeIII in 46.8% and type IV in 28.2% of the implants inserted in lightsmokers. These numbers were 32.3%, 48.4% and 19.4%, respectively,for heavy smokers. The statistical analysis indicated the absenceof a significant correlation between smoking and bone type. Theinsertion torque had a mean value of 46.87 ± 1.32, 42.31 ± 3.08 and51.61 ± 3.22 Ncm for non-smokers, light smokers and heavy smok-ers. The statistical analysis revealed no significant effect of smokingon the implant insertion torque.

ally guided implant site preparation to obtain adequate primarynat.2014.02.005

3.3.3. Implant diameter and insertion torqueFig. 3 showed the distribution of the 8.5 mm-implants accord-

ing to their diameter. The implant diameter had a mean value

Fig. 3. Distribution of the 8.5 mm-long implants according to their diameter.

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ig. 4. The effect of bone quality on the value of insertion torque of 8.5 mm-longmplants.

f 4.5 ± 0.5 mm and almost 85% of the implants had a diameter4.0 mm. The statistical analysis indicated the absence of correla-

ion (p = 0.386) between the insertion torque and implant diameter.

.3.4. Bone type and insertion torqueFig. 4 showed the variation in the insertion torque between

ifferent types of alveolar bone. The insertion torque was9.29 ± 7.27 Ncm for bone type I, 56.51 ± 1.62 Ncm for bone type II,6.40 ± 1.60 Ncm for bone type III, 34.84 ± 2.38 Ncm for bone type

V. For bone type V, the insertion torque had a value of 5 Ncm. Sta-istical analysis revealed a significant association between the typef bone and the insertion torque.

When considering the jaw quadrants, the insertion torque ofhe 8.5 mm-long implants varied considerably (Fig. 5). Implantsere inserted at a torque of 36.73 ± 2.15 Ncm and 39.64 ± 2.03 Ncm

n quadrants 1 and 2 of the maxilla. The insertion torque inhe anterior maxilla was 41.84 ± 4.56 Ncm, in the upper premolarrea it was 36.50 ± 2.37 Ncm and in the upper molar area it was8.19 ± 1.97 Ncm.

Please cite this article in press as: Anitua, E., et al., Efficacy of biologicimplant stability. Ann. Anatomy (2014), http://dx.doi.org/10.1016/j.aa

This torque value was higher in the mandible reaching a valuef 53.83 ± 2.18 and 61.44 ± 1.21 Ncm in quadrants 3 and 4, respec-ively. The insertion torque was 56.92 ± 4.65 and 57.59 ± 1.33 Ncmn the lower premolar and molar area, respectively.

ig. 5. The values of insertion torque of 8.5-mm-long implants according to jawuadrant.

PRESSomy xxx (2014) xxx–xxx 5

3.3.5. Loading protocolThe results of the present study indicate that the described pro-

tocol has been effective in permitting the osseointegration of allimplants. The immediate loading protocol was established for 16implants inserted into bone type II and bone type III. The insertiontorque of these implants ranges from 40 to 65 Ncm with a meanvale of 55 ± 3.48 Ncm. One-stage surgery was performed in 69% and53% of the implants placed in bone type II and III, respectively. Two-stage surgery was performed for 78% of the implants placed in bonetype IV. The surgery was also done in two stages for the implantsplaced in bone type V but the time span between the two surgerieswas increased and prosthetic rehabilitation was done following theprogressive loading protocol.

4. Discussion

The relationship between bone quality and insertion torque onone hand and the RFA on the other hand has been investigatedin several studies. Ribeiro-Rotta et al. have found a significantcorrelation between the insertion torque peak and computedmicrotomography parameters of bone architecture and density(Ribeiro-Rotta et al., 2012). However, this correlation was weak orabsent for RFA (Akca et al., 2006; Ribeiro-Rotta et al., 2012; Rozeet al., 2009). Barewal et al. have reported significant differences inthe insertion torque of implants placed in different types of bonequality (Barewal et al., 2012). Moreover, Barewal et al. have shownthe success of dental implants placed in bone of different types,when the protocol of implant loading was selected on the basisof the insertion torque (Barewal et al., 2012). Given the above, itappears that the insertion torque peak is a better predictor of themechanical stability at the bone–implant interface (Barewal et al.,2012; Norton, 2011; Ribeiro-Rotta et al., 2012). It is also notewor-thy that a significant correlation has been described between bonedensity and insertion torque peak and between bone density andthe bone type as classified by Lekohlm and Zarb (Norton, 2011;Ribeiro-Rotta et al., 2012).

The bone type classification is proposed in order to adapt thedrilling protocol to the needs of achieving adequate primary stabil-ity. The bone types I, II and III coincide with the Lekohlm and Zarbclassification. The difference is in that Lekohlm and Zarb bone typeIV is subdivided into two categories: bone type IV and bone type Vdepending on the presence or absence of thin cortical layer and thebone density measured on CBCT. The presence of low density bonepresents a challenge to achieving the success of dental implantsand requires a specific treatment plan and surgical protocol to min-imize the risk of implant failure (Bahat, 2000; Friberg et al., 1999).Jaffin et al. have reported the failure of 35% of the implants placedin bone type IV (Jaffin and Berman, 1991). It is important to men-tion that the implants placed in the study of Jaffin et al. were ofsmooth surface which would increase the likelihood of implant fail-ure (Jaffin and Berman, 1991). Khang et al. and Tabassum et al. haveobserved high implant failure rates for maxillary bone with lowdensity (Khang et al., 2001; Tabassum et al., 2011). Similarly, it hasbeen observed that implant failure was more common in low den-sity bone (Pagliani et al., 2013; Sennerby and Roos, 1998). One of thestrategies to minimize the risk of implant failure in soft bone is theimprovement in the implant primary stability. In that sense, sev-eral methods have been developed to increase the insertion torqueand thus the primary stability. Under-preparation of the implantsocket, changes in the design of the endosseous fixture and the useof osteotomes instead of drills to compact/condense the housingbone are among the clinical maneuvers to favor implant osseointe-

ally guided implant site preparation to obtain adequate primarynat.2014.02.005

gration (Friberg et al., 1999; Galindo-Moreno et al., 2012). Cavallaroet al. and Engelke et al. concluded that changes in the drillingprotocol are necessary to improve primary implant stability fordifferent bone densities (Cavallaro et al., 2009; Engelke et al., 2013).

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Implant socket preparation has been performed following lowpeed drilling as it has been shown not to cause overheating ofone and thus permitting the drilling without irrigation (Anituat al., 2007). This drilling and the use of bone drills (designed torap bone particles) facilitate the collection of autologous bonearticles (Anitua et al., 2007). The good quality of bone particlesesulted from drilling at low speed has been shown in a recenttudies (Anitua et al., 2007; Park et al., 2012).

The drilling protocol described in this study was adapted tohe bone type/density to control and standardize the under-reparation of the implant site to achieve optimal values of

nsertion torque and to avoid excessive compression of the host-ng bone. This will allow for bone remodeling around the implanto increase the BIC and results in the secondary stability of themplant. The remodeling process involves two synchronized pro-esses: bone resorption and bone formation. Pereira et al. havetudied markers of bone formation and resorption based on thelassification of Lekohlm and Zarb and found no significant associa-ion between the bone type and bone formation/resorption (Pereirat al., 2013). Trisi et al. have placed dental implants at low and highorque in the mandible of sheep and reported that the componentf bone resorption was greater for high torque implants with thereation of bone micro-fractures (Trisi et al., 2011). Tabassum et al.ave studied the effect of compressing (under-preparation of theocket) the cancellous bone on the BIC of the implants insertedn the iliac crest of goats (Tabassum et al., 2011). The resorptionomponent of bone remodeling was higher around the implantsnserted at greater compression and the authors concluded that theiological limit of compression is below 25% (Tabassum et al., 2011).n another study Nevins et al. have concluded that an intermedi-te level of bone compression is optimal for the osseointegrationf dental implants (Nevins et al., 2012).

It has been reported that insertion of the implant at high torqueesulted in ischemic necrosis of the bone and thus in the failuref the implant (Bashutski et al., 2009). However, as other studiesave found no differences in the success of implants inserted at highnd low torque, we may conclude that the bone type and implantesign can influence the bone response to compression producedy the implant. Conical implants, by their morphology, generateifferent degrees of compression, the maximum of which is at theider implant area. A cylindrical implant compresses bone in the

ame way throughout its length.However, it seems that the optimal insertion torque depends

n the bone type, implant design and diametrical ratio betweenhe hosting socket and the implant (Nevins et al., 2012). Severallinical and experimental studies have reported successful osseoin-egration of implants placed at high torque (≥70 Ncm) while otherseported negative effects. Khayat et al. have found no differences inmplant failure or in the peri-implant bone loss between implantsnserted at low torque (≤50 Ncm) and implants inserted at highorque (≥70 Ncm) (Khayat et al., 2013). However, this bone lossas measured at two points during the first year and that the

mount of bone loss has been doubled at the later time point formplants inserted at high torque, which makes it necessary to eval-ate the peri-implant bone loss at longer times. In fact, the highompression of the peri-implant bone increased the marginal boneoss by 22–50% (Rodoni et al., 2005). It has been reported thatigh compression of the bone, achieved by use of osteotomes or

mplant insertion at high torque (alveolus diameter smaller thanhe diameter of the implant), significantly reduced the percentagef bone-to-implant contact (BIC) at the earliest stages of osseointe-ration (Buchter et al., 2005; Norton, 2011). These negative effects

Please cite this article in press as: Anitua, E., et al., Efficacy of biologicimplant stability. Ann. Anatomy (2014), http://dx.doi.org/10.1016/j.aa

ay increase the risk of failure for implants inserted at high torqueDonati et al., 2008).

Biomechanical studies have shown that the majority of stressransmitted to the peri-implant bone is concentrated in the crestal

PRESSomy xxx (2014) xxx–xxx

bone (the first 2–3 mm of implant length) regardless of the implantdesign (Anitua et al., 2010; Nissan et al., 2011a,b; Pierrisnard et al.,2003), making this area essential in achieving primary implant sta-bility. This has motivated us to adapt the drilling according to thebone composition (cortical/cancellous) and bone density to max-imize the efficiency of the first 4–5 threads of the implants inproviding stability to the implant.

The results of the present study indicate that the describedprotocol has been effective in permitting the insertion of dentalimplants at a torque ≥30 Ncm and resulted in the osseointegrationof all implants. The insertion torque was dependent on the availablebone type and higher values were obtained for denser bone tissue.It is noteworthy that the drilling protocol followed in this study waseffective in obtaining an insertion torque ≥30 Ncm in low-densitybone (bone type IV). However, the insertion of implants in bonetissue where the density was less than 400 Ncm was completelydifferent from bone type IV of higher density. In fact, bone resis-tance during drilling was significantly reduced and radiographicanalysis showed the absence of cortical bone. This motivated usto add another bone category, known as bone type V. Bone type Vwas encountered in the posterior maxilla and the implant insertiontorque had a value of 5 Ncm.

However, a specific bone category has been suggested to beclassified as bone type V. This type of bone lacked cortical boneand the cancellous bone component was of low density, compli-cating the achievement of insertion torque higher than 5 Ncm. Insuch bone, implant surgery should be done in two stages, with anincrease in the osseointegration period, and followed by a progres-sive loading protocol. It is noteworthy that none of the 295 implantsfailed although the insertion torque value was 5 Ncm in 2.5% of theimplants. This could be related to fact that the loading protocolwas delayed for most implants and immediate loading protocolwas followed when torque values were between 40 and 65 Ncm.

In this study, implant diameter did not significantly correlateto the insertion torque. This could be related to the standardiza-tion of the implant socket under-preparation in relation to implantdiameter. Trisi et al. have found no significant correlation betweenimplant diameter and insertion torque peak in high and mediumfresh bovine bone (Trisi and Berardini, 2012).

It is worthwhile mentioning that one of the limitations of thisstudy is the measurement of bone density in HU on cone-beamCT scan. In contrast to CT, the gray density values of the CBCT arenot absolute, but could be predictive for the subjective bone qualityclassification and primary implant stability (Arisan et al., 2013). Theefficacy of the drilling protocol adopted in this study was measuredby the value of the insertion torque and the use of PRGF-Endoretwould not affect the value of the insertion torque. Moreover, PRGF-Endoret was used for all the implants analyzed in this study andthis biological preparation is proposed as adjuvant to promote theosseointegration of the dental implants in which primary stabilityis a key parameter.

5. Conclusions

The surgical protocol followed in this study adapts the implantsocket preparation to the needs of establishing a sufficient primarystability to permit the osseointegration of the dental implant. Theunder-preparation of the socket is increasing by the decrease in thequality of the hosting bone reaching a maximum value of 1.2 mm.An adequate insertion torque (≥30 Ncm) was not obtainable in abone with a density below 400 HU and could indicate the need forconsideration of other measures to favor the osseointegration of

ally guided implant site preparation to obtain adequate primarynat.2014.02.005

the implant, such as, increasing the time span for implant uncover-ing and following a progressive loading protocol. More studies areneeded to report on the implant osseointegration in low qualitybone and measures to take to minimize the risk of implant failure.

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