influence on early osseointegration of dental implants installed with two different drilling...

Influence on early osseointegration ofdental implants installed with twodifferent drilling protocols: ahistomorphometric study in rabbit

Juan BlancoElena AlvarezFernando MunozAntonio LinaresAntonio Cantalapiedra

Authors’ affiliations:Juan Blanco, Elena Alvarez, Antonio Linares,Department of Stomatology – Periodontology, School ofDentistry, University of Santiago de Compostela,Santiago de Compostela, SpainFernando Munoz, Antonio Cantalapiedra, School ofVeterinary of Lugo, University of Santiago deCompostela, Santiago de Compostela, Spain.

Corresponding author:Juan BlancoDepartment of Stomatology – PeriodontologySchool of DentistryUniversity of Santiago de Compostelac/Entrerrıos s/n 15702Santiago de CompostelaSpainTel.: þ 34 981 571 826Fax: þ 34 981 571 620e-mail: [email protected]

Key words: bone implant contact, early healing, primary stability, resonance frequency analysis

Abstract

Objective: To evaluate early osseointegration of dental implants installed with two different drilling

protocols.

Material and methods: Thirty-six cylindrical shape Mozo Grau implants, with a diameter of 3.75 and

11 mm long, were placed into the distal condyle (submerged) of each femur of 18 New Zealand

rabbits. In the control group, a 3.3 mm diameter drill was used as the last one prior implant installation

(standard protocol). In the test group, the same procedure was carried out but an additional 3.5 mm

drill was used as the final one (oversized protocol) Thus, we could obtain different primary stability at

day 0 between groups. Sacrifice of the animals was after 2, 4 and 8 weeks. Histomorphometric analysis

(bone-to-implant contact ratio [BIC%]) and implant stability quotient (ISQ) values (Ostells

) were

registered at each sacrifice time.

Results: The ISQ values were statistically significant different between groups at day 0 (control: 69.65;

test: 64.81); and after 2 weeks (control: 77.93; test: 74). However, after 4 and 8 weeks the results were

similar. BIC% showed a similar tendency, with 58.69% for the control group and 40.94% for the test group

after 2 weeks, this difference being statistically significant. At 4- and 8-week interval, BIC% was similar.

Conclusion: At 2-week interval (early healing), osseointegration had been influenced by different

primary stability at implant installation, being slower in the oversized protocol (lower primary stability),

which could be especially risky in challenging clinical situations, such as soft bone (class 3 and 4) and early/

immediate loading. However, from 4 week on, these differences disappeared. Nevertheless, we have to

consider that a direct transfer of the results of this animal study (time bone repair mechanisms) into clinic

has to be done with caution.

The term ‘‘osseointegration’’ refers to the process

whereby alloplastic materials (dental implants)

and bone are joined in a rigid, clinically asympto-

matic union that withstands functional loading

(Zarb & Albrektsson 1991). This is a definition

based on the mechanical stability of the implant.

In order to understand the healing process, it is

necessary to know the biological mechanisms

that play a role in the integration of the implant

with the surrounding bone.

Dental implant primary stability has been

demonstrated to be a key factor for implant

survival rates. Primary mechanical stability is

directly related to the quality and quantity of

bone at the recipient site, the type of implant

used and the surgical technique used to place the

implant (Meredith 1998). Biologically, this pri-

mary stability is obtained if the marginal and/or

apical areas of the implant site hold a large enough

quantity of compact bone and if the spongy bone

contains a sufficient number of trabeculae

(Albrektsson Berglundh & Lindhe 2003). Clini-

cally, at the time of implant placement, this kind

of primary stability is achieved by ‘‘tight fitting’’

between the implant surface and the avascular

cortical bone in the marginal area of the implant

bed. This intimate bone-to-implant contact (BIC)

is also the effect of the minute lateral displace-

ment exerted in the bone tissue during implant

adaptation, where the trabeculae of the marginal

portion shift towards the medullar space and the

sectioned blood vessels bleed. As a consequence,

a blood clot forms and is trapped between the

implant surface and the bone. This blood clot will

mature over the next few days and eventually be

replaced by granulation tissue (Albrektsson et al.

1983), woven bone and lamellar bone, producing

secondary stability. Therefore, secondary stability

is the consequence of the formation of new bone

and the remodelling process in both the area of

most direct contact (the bone–implant interface

itself) and a more distant area (Meredith 1998).

Date:Accepted 12 June 2010

To cite this article:Blanco J, Alvarez E, Munoz F, Linares A, Cantalapiedra A.Influence on early osseointegration of dental implantsinstalled with two different drilling protocols: ahistomorphometric study in rabbitClin. Oral Impl. Res. 22, 2011; 92–99.doi: 10.1111/j.1600-0501.2010.02009.x

92 c� 2010 John Wiley & Sons A/S

mailto:[email protected]

A non-invasive intraoral method for evaluating

implant stability has been developed in recent

years. Meredith et al. (1994) described a new

clinical non-invasive approach that consisted in

evaluating bone anchorage around an implant by

measuring the resonance frequency of a transdu-

cer coupled to the implant (Meredith et al. 1994;

Meredith et al. 1996; Meredith et al. 1997a,

1997b). This new technique was named resonance

frequency analysis (RFA). Numerous in vitro and

in vivo studies have corroborated RFA as a tech-

nique designed to reflect the bone/implant inter-

face and hence may be useful in documenting

clinical implant stability (Meredith et al. 1996;

Meredith 1998; Zix et al. 2008). However, no

correlations between histological parameters of

osseointegration and implant stability quotient

(ISQ values) could be identified by other authors

(Huwiler et al. 2007; Abrahamsson et al. 2009).

When trying to achieve primary stability in soft

bone (class 3 and 4), clinicians have attempted to

improve the stability by using osteotome for

condensation or undersized drills before implant

installation (Bahat 1992, 1993; Summers 1994,

1995; Blanco et al. 2008). However, sometimes it

is not possible to achieve ideal primary stability,

due to a bad control of the drilling and/or wrong

drilling sequence during surgery, resulting in an

oversized bone preparation.

The objective of this study was to evaluate the

early osseointegration of dental implants in-

stalled with two different drilling protocols (stan-

dard and oversized) in a soft bone animal model.

Materials and methods

Once approval from the Ethics Committee of the

University of Santiago de Compostela had been

granted, this research was carried out using 18

New Zealand white rabbits weighing an average

of 5.5 kg. All animals were installed in the

animal experimentation service facility at the

Veterinary Hospital Rof Codina of Lugo (Spain).

All experiments were performed according to the

Spanish Government Guide and the European

Guide for Animal Care. The experimentation site

was located on both distal condyles of the femurs.

The implants used in this study were MG

Osseous implants (Mozo Graus

, Valladolid,

Spain) made of commercially pure grade-IV tita-

nium, featuring 2.5 mm of machined surface

(1 mm in the platform and 1.5 mm of threads in

the endo-osseous portion), followed by 8.5 mm of

surface treated with resorbable blast media (RBM

blasted with calcium phosphate ceramics) all the

way to the apical portion of the implant. The

implants selected were 3.75 mm (core: 3.3 mm)

in diameter/11 mm long, and cylindrical down to

the seventh thread, after which it adopts a conical

component, with a self-tapping feature closer to

the apex.

Surgical procedure

In accordance with the described standards for

surgery on experimental animals, the surgery was

performed in the surgical area of the Rof Codina

Veterinary Clinical Hospital, at the University of

Santiago de Compostela, School of Veterinary

Medicine at Lugo. All surgeries were performed

by the same operator (J. B.). The surgical ap-

proach occurred under general anaesthesia and

was under the supervision of the veterinary sur-

geon at all times.

An incision was made at the distal femoral

condyle with a scalpel fitted with a number 15

blade, following a continuous line. Subsequently,

the skin, the subcutaneous tissue and the muscle

were drawn back to gain access to the bone.

Implant bed preparations were carried out accord-

ing to the recommendations of the manufacturer

(Mozo Graus

). Study groups were formed in

relation to the last drill used before implant

installation. In one condyle (control group), the

last drill was 3.3 mm in diameter (standard pro-

tocol) and in the other condyle (test group) the

last drill was 3.5 mm in diameter (oversized

protocol). Lastly, the countersink drill was used,

aiming to avoid the potential effect on primary

stability of the cortical bone plate. Once the

implant bed was prepared, the implants were

inserted and the resonance frequency was imme-

diately measured in both groups. Thus, using a

split design, in one condyle, one implant was

placed in the control group, and in the other

condyle, one implant was placed in the test

group. Finally, the incision was closed in layers

with reabsorbable suture (Vicryls

, Ethicon, Som-

erville, NJ, USA), leaving the implants sub-

merged. A total of 36 implants were placed,

two per rabbit (Fig. 1a–e).

After surgery, the rabbits were moved to the

laboratory animal house of the University of

Santiago de Compostela’s Lugo Campus and

put into individual hutches, with the following

conditions: temperature of 22 � 21C and a rela-

tive humidity of 50–70%.

Histological analysis and resonancefrequency evaluation

The animals in the study were sacrificed at 2, 4

and 8 weeks after implant installation, so that

samples could be obtained and prepared for his-

tological analysis. After being euthanized, flaps

were raised to obtain access to the submerged

implants in order to measure the ISQ values. The

implants were separated from each femur using a

diamond saw (Exact 300CLs Apparatebeau, Nor-

destedt, Hamburg, Germany). The biopsies were

processed for ground sectioning in conformity

with the Donath method (Donath 1995). The

samples were dehydrated and infiltrated with

resin (Technovit 7200s, VLC-Heraus Kulzer

GmbH, Werheim, Germany). Finally, the sam-

ples were sectioned using a grinding technique

(Exact 400CSs Apparatebeau, Hamburg, Ger-

many) up to approximately 20mm using the

Levai Laczko staining method.

Histometric evaluation

For the histometric analysis, the samples were

processed with an Olympuss

DP12 image digi-

talization unit that was coupled to an Olympuss

CH30 microscope and an Olympuss

SZX9 stereo

microscope (Olympuss

DF PLAPO 1 � �2 lens,

Tokyo, Japan). Using Olympus MicroImage soft-

ware, version 4.0 for Windows, the points of

interest on the digitalized images of the histologi-

cal samples were identified.

One examiner, who was blinded to treatment

allocation of the specimens, identified the follow-

ing linear measurements in each section with a

magnification of � 40 of the original one.

BIC

It is defined as the length of the bone surface in

direct contact with the implant starting from the

shoulder of the implant.

Implant perimeter (IP)

This starts from the implant shoulder to the last

visible thread, disregarding the unthreaded apical

portion (Nkenke et al. 2003) (Fig. 2).

BIC ratio (BIC%)

Defined as BIC/IP (� 100 [%]).

The primary variables were BIC% and ISQ

values at different time intervals.

Statistical analysis

Descriptive statistics were produced for each one

of the variable and groups (mean values, standard

deviation, median and scatter plots). Confidence

intervals for the differences of the means with a

confidence level of 95% were presented. The

Wilcoxon test for non-parametric paired data

was applied to both the clinical results (ISQ values

obtained from the measurements made with the

Osstell Mentors

, Integration diagnostic, Goteborg,

Sweden) and the histological results (BIC%). The

probability level of Po0.05 was considered as the

level of statistical significance.

All statistical analysis was performed with

SPSS 15.0 for Windows (SPSS Inc., Chicago, IL,

USA).

Blanco et al �Healing of implants installed with two drilling protocols

c� 2010 John Wiley & Sons A/S 93 | Clin. Oral Impl. Res. 22, 2011 / 92–99

Results

Two of the animals were sacrificed prematurely

due to femoral fracture induced by an infectious

process. Therefore, the final sample was com-

prised of 16 rabbits and 32 implants. Five rabbits

were sacrificed after 2 weeks, five after 4 weeks

and six after 8 weeks.

ISQ values (Osstell Mentors

)

The ISQ values of the resonance frequency regis-

tered with the Osstell Mentors

are shown in

Table 1 and Fig. 3. At implant installation, the

ISQ for the control group was 69.65 � 6.17, and

64.81 � 6.39 for the test group. The difference in

ISQ values was statistically significant. This

shows that the control implants had a higher

primary stability than the test ones.

After 2 weeks, there was a significant differ-

ence between test and control for the ISQ values.

The control showed an ISQ value of 77.93 �3.74 and the test 74 � 3.94.

However, after 4 and 8 weeks of healing, the

difference ceased to be significant. Nevertheless,

the ISQ values increased over time in both groups

(Fig. 3).

Histomorphometric results (BIC%)

The results of the percentage of BIC at each time

interval are displayed in Table 2 and Fig. 4. The

percentage of BIC registered for the rabbits sacri-

ficed after 2 weeks (Figs 5 and 6) displayed

statistically significant differences between the

test group (3.5 mm) and the control group

(3.3 mm). The values found were 40.94 � 7.77

and 58.69 � 10.67, respectively. However, no

significant differences were found in the other

two sacrifice groups, after 4 (Figs 7 and 8) and 8

weeks (Figs 9 and 10).

Discussion

The main determinants of implant stability are

the mechanical properties of the bone tissue at

the implant site and the degree of implant en-

gagement with that bone tissue. The mechanical

properties of bone are determined by the compo-

sition of the bone at the implant site and may

increase during healing because soft trabecular

bone tends to undergo a transformation into

dense cortical bone at the vicinity of the implant

surface. The strength of the implant–bone inter-

face is also influenced by surgical technique and

implant design and surface. For instance, the use

of a narrower final drill or a wider or tapered

implant will force more of the implant threads

into contact with the surrounding bone (Sen-

nerby & Meredith 2008).

The objective of this experimental study was to

evaluate whether the primary stability achieved

at the time of implant placement with two

different drilling protocols, influences the speed

of implant osseointegration. The results we

found show a tendency towards increased BIC

over time in both groups. Primary stability was

observed to have a significant positive influence

on the early osseointegration process (2 weeks);

Fig. 1. (a) View of the surgical area at the distal condyle of the femur of the rabbit. (b) The implant installed with the transporter. (c) The implant without the transporter. (d) Implant stability

quotient value registered with the Ostell Mentors

system. (e) Radiographic view of the implant after installation.

Fig. 2. The contained zone represents the measured area of

bone implant contact, from the implant shoulder to the last

visible thread in the histological section. Levai Laczko

staining method. Original magnification � 12.5.

Table 1. Implant stability quotient (ISQ) values

ISQ values Control (3.3) Test (3.5) 95% CI Wilcoxon test

Mean (SD) Median Mean (SD) Median

Day 0 69.65 (6.17) 72 64.81 (6.39) 64 1.05 to 8.63 P¼ 0.018n

Week 2 77.93 (3.74) 77 74 (3.94) 73 1.08 to 6.91 P¼ 0.042n

Week 4 81.65 (3.15) 81 78.78 (4.83) 77 � 2.71 to 8.31 P¼ 0.225Week 8 82.79 (5.07) 83.25 82.33 (5.7) 85.75 � 3.99 to 4.82 P¼ 1

nP-valueo0.05: statistical significance.

CI, confidence interval for the differences of the means; SD, standard deviation.


94 | Clin. Oral Impl. Res. 22, 2011 / 92–99 c� 2010 John Wiley & Sons A/S

osseointegration was faster in the control group

(greater primary stability) than in the test group.

Early clinical work indicated a relationship

between bone density and primary implant sta-

bility. Friberg et al. (1999) correlated cutting

resistance (i.e. bone density) with primary stabi-

lity for maxillary implants. Follow-up measure-

ments performed at the time of abutment

connection (6–8 months later) and after 1 year

in function indicated that all implants, irrespec-

tive of initial stability, tended to reach a similar

level of stability. These facts are in accordance

with what we have observed in our study from 4

weeks on, where the implants in both groups

attained the same stability levels.

Andersson et al. (2008) examined 102 Neoss

implants and found an inverse relationship be-

tween cutting torque (bone density) and changes

in implant stability during a study period of 12

months . They also identified a correlation be-

tween bone hardness, measured according to

Lekholm & Zarb (1985), and primary stability.

Implants in soft bone with low primary stability

showed a marked increase in stability compared

with implants in dense bone. We found this

tendency in our study in both groups (soft bone

model), which is similar to the results of a study

in rabbits finding that resonance frequency in-

creases with time as a function of an increased

stiffness resulting from new bone formation and

remodelling (Meredith et al. 1997b).

Some studies have failed to show a correlation

between the degree of BIC and RFA measure-

ments (Meredith et al. 1997b; Akca et al. 2006;

Ito et al. 2007). This may have to do with the

Fig. 3. Implant stability quotient values scatter plot for control (3.3) and test (3.5) treatment.

Table 2. Bone-to-implant (BIC) contact percentage

BIC% Control (3.3) Test (3.5) 95% CI Wilcoxon test

Mean (SD) Median Mean (SD) Median

Week 2 (N¼ 5) 58.69 (10.67) 56.34 40.94 (7.77) 40.91 6.89 to 28.58 P¼0.043n

Week 4 (N¼ 5) 49.97 (10.16) 46.87 55.43 (6.18) 56.3 � 22.92 to 12.01 P¼0.686Week 8 (N¼ 6) 60.74 (10.03) 58.48 57.32 (7.8) 50.76 � 13 to 19.84 P¼0.753

nP-valueo0.05: statistical significant.

SD, standard deviation; CI, confidence interval for the differences of the means.

Fig. 4. Bone implant contact percentage scatter plot for control (3.3) and test (3.5) treatment.

Fig. 5. (a, b) Control group. These images represent the

2-week interval. Levai Laczko staining method. Original

magnification � 12.5, and the close up images � 40.



nature of the test, because the degree of bone

contact does not necessarily reflect the stiffness

of the surrounding bone. In modern implant

dentistry using moderately rough implants, the

surface is often covered by a thin layer of bone,

which is probably not important for the biome-

chanical support of implants. The study con-

ducted by Abrahamsson et al. (2009) to

evaluate the relationship between BIC and ISQ

values during a 12-week healing period in the

animal model did not find any correlation be-

tween the two parameters, either; the results

were in line with those found by Huwiler et al.

(2007), Schliephake et al. (2006) and Ito et al.

(2008). However, we did find a positive

correlation between the increase in ISQ values

and BIC.

We found significant differences in BIC be-

tween the two groups after 2 weeks; these differ-

ences may be of major importance in terms of

loading time. Thus, when there is suitable pri-

mary stability (ISQ values), loading could be

carried out early and even immediately. Ostman

et al. (2005, 2008) reported low failure rates when

using an implant stability quotient of 60 as an

inclusion criterion for immediate loaded implants

in totally edentulous maxillae and in posterior

mandibles. Sennerby & Meredith (1998) found

the RFA technique to be helpful in deciding when

to replace an immediately loaded temporary

prosthesis with a permanent prosthesis after im-

plant placement.

The introduction of new implant surfaces may

let us reduce treatment time protocols, because it

may be able to diminish the time required for

Fig. 6. (a, b) Test group. These images represent the 2-week

interval. Levai Laczko staining method. Original magnifica-

tion � 12.5, and the close up images � 40.Fig. 7. (a, b) Control group. These images represent the

4-week interval. Levai Laczko staining method. Original




tion � 12.5, and the close up images � 40.



osseointegration. The evidence from histomor-

phometric data and clinical studies suggests that

rough implant surfaces exert a clinically signifi-

cant influence on osseointegration. Berglundh

et al. (2003) have carried out a histological study

investigating the sequential healing events asso-

ciated with the placement of SLA (sand blasted,

large grit, acid etched) surface titanium implants.

This study confirms previous reports (Cochran

et al. 1998; Schenk & Buser 1998) that initial

bone formation around rough titanium implants

occurs not only to the exposed bone wall of the

surgically created implant bed but also along the

osteoconductive implant surface. Furthermore, it

was demonstrated that there was a higher level of

organization in the wound and higher BIC during

the early healing (from 2 h) associated with the

SLA surface compared with the machined sur-

faces (Abrahamsson et al. 2004). In addition, a

modification of the SLA implant surface has been

introduced (SLActive). This new surface allows

for immediate cell reaction right after implant

placement and accelerates bone remodelling dur-

ing the osseointegration process. Pre-clinical re-

sults have shown that SLActive provides 60%

more bone integration after 2 weeks compared

with the SLA surface (Buser et al. 2004). Results

from a human clinical study measuring implant

stability with the Osstell device demonstrated a

statistically significant improvement in stability

with SLActive implants over those with SLA

during the critical early treatment period between

weeks 2 and 4 (Oates et al. 2007). It has been

recently shown that implants with a SLActive

surface would promote complete bone regeneration

of acute dehiscence defects in dogs within a period

of 12 weeks (Schwarz et al. 2007). Surface treat-

ments with a calcium phosphate coating promote

early bone healing as well as subsequent bone

apposition, generating rapid biological fixation

of the implant to the bone (Le Guehennec et al.

2007; Meirelles et al. 2008). The implant analysed

in this paper presents a surface blasted with cal-

cium phosphate ceramics. Such a surface may

influence the speedy early healing obtained in

this study.

How well an implant is fixated to the sur-

rounding bone tissue is dependent on different

implant and host-related factors. Six factors,

listed by Albrektsson et al. (1981) have gained a

general acceptance as being especially important:

biocompatibility, design, surface quality, status

of host tissue, surgical technique and loading

conditions. Therefore, the development of new

implant designs (tapered), surfaces and clinical

techniques has enabled a marked reduction of the

initial healing period, even to the point of an

immediate/early loading of implants that show

high primary stability (Attard & Zarb 2005;

Ostman 2008). However, in a recently published

randomized-controlled clinical trial, no differ-

ences between standard cylindrical and tapered

implants were noted in terms of primary stabi-

lity, yielding clinically equivalent short-term

outcomes (Lang et al. 2007). Thus, the success

of immediate/early loading implant techniques is

dependent on the ability of the clinician to

achieve and to determine, the degree of primary

implant stability and changes in stability along

with new bone formation and remodelling. In

addition, the results of our study reflect the

importance of careful management of the surgical

technique in terms of both the selection of the

drilling protocol and/or gentle drilling.

Conclusion

The most important finding of our study is that,

with the tapered implant design utilized here, the

speed of osseointegration after 2-week interval

(early healing) has been significantly influenced

by primary stability achieved at implant installa-

tion time, being slower in the oversized protocol

(lower primary stability), which could be espe-

cially risky in challenging clinical situations,

such as soft bone (class 3 and 4) and early/

immediate loading. However, from 4 weeks on,

these differences disappeared. Nevertheless, we

have to consider that a direct transfer of the

Fig. 9. (a, b) Control group. These images represent the 8-

week interval. Levai Laczko staining method. Original




tion � 12.5, and the close up images � 40.



results of this animal study (time bone repair

mechanisms) into clinic is not recommended.

Acknowledgements: This

investigation was supported by the Mozo Grau

Company. The authors declare that they have

no conflict of interest.

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