Hyung-In Yoon1 Effect of a macroscopic groove on bone

In-Sung Yeo1
Jae-Ho Yang
response and implant stability

Authors’ Affiliations: Key words: bone-to-implant contact, macroscopic groove, rabbit tibia, removal torque,
Hyung-In Yoon, Jae-Ho Yang, Department of resonance frequency
Prosthodontics, School of Dentistry and Dental
Research Institute, Seoul National University,
Seoul, South Korea Abstract
In-Sung Yeo, Department of Prosthodontics, Section
of Dentistry, Seoul National University Bundang
Objectives: The aim of this study was to investigate the effect of a macroscopic groove on
Hospital, Gyeonggi-do, South Korea bone response and implant stability during the early stages of healing using a rabbit tibia
model.
Correspondening author:
Dr. Jae-Ho Yang Materials and methods: Anodized titanium implants with (n ¼ 24) and without (n ¼ 24)
Department of Prosthodontics macroscopic grooves were prepared. A total of 12 rabbits were used and each received four
School of Dentistry and Dental Research Institute
Seoul National University implants: six rabbits with implants with macroscopic grooves (test group) and six rabbits
62 Changgyeonggungno with implants without macroscopic groves (control group). Histomorphometry, resonance
Jongno-Gu
frequency, and removal torque value were evaluated 2 and 6 weeks post-implant-insertion.
Seoul 110-749, South Korea
Tel.: þ 82 2 2072 2661 Results: At 2 and 6 weeks, there was no significant difference between the two groups in
Fax: þ 82 2 2072 3860 the percentage of bone-to-implant contact (P40.05). At 6 weeks, the test group had
e-mail: jhoyang@snu.ac.kr
significantly higher implant stability quotient values than the control group (Po0.05). At 2
and 6 weeks, implants with grooves showed a significantly greater resistance to reverse
torque than control implants (Po0.05).
Conclusion: The groove on the oxidized titanium surface may increase both resistance to
shear load and adhesion at the bone–implant interface. A geometric feature such as a
macroscopic groove may facilitate osseointegration and increase implant stability in various
clinical conditions. Further studies are required to confirm whether the improvement in
implant stability will enhance treatment success in humans.

The design and surface characteristics of in a superior bone response to that achieved
dental titanium implants are crucial factors with a machined surface (Glauser et al.
for successful osseointegration (Albrekts- 2001, 2003; Ivanoff et al. 2003; Rocci
son et al. 1981; Albrektsson 1983; Al- et al. 2003; Zechner et al. 2003). Macro-
brektsson & Jacobsson 1987). Numerous irregularities such as grooves and pores of
studies have reported improved bone-to- various dimensions, which are parameters
implant contact (BIC) with the use of a of implant design, have been introduced to
1
modified surface compared with a turned implant threads in order to maximize the
Contributed equally to this work.
surface (Wennerberg et al. 1995, 1996, initial bone contact, enlarge the surface
Date:
Accepted 21 February 2010.
1998; Piattelli et al. 1998; Yeo et al. area, and dissipate interfacial stress (Carls-
2008). Many studies have also reported son et al. 1986; Brunski 1988; Ivanoff et al.
To cite this article:
Yoon H-I, Yeo I-S, Yang J-H. Effect of a macroscopic that modification of the implant surface 1997; Sykara et al. 2000).
groove on bone response and implant stability. by anodic oxidation, which is one of the One study of orthopedic implants de-
Clin. Oral Impl. Res. 21, 2010; 1379–1385.
doi: 10.1111/j.1600-0501.2010.01960.x several surface treatment methods, results monstrated that bone growth into macro-

c 2010 John Wiley & Sons A/S

 1379
Yoon et al  Effect of a macroscopic groove on bone

scopic pores is dependent upon the dimen- den) were used in control animals. Twenty- with a thickness of approximately 50 mm
s
sion of the pore being larger than a thresh- four anodized implants with a 110 mm- were prepared using the Exakt system
old value of approximately 100 mm (Pilliar wide and 70 mm-deep groove on the center (Exakt Apparatebau, Norderstedt, Ger-
et al. 1998). Growth of the bone matrix of the inferior thread flank (Brånemark many) according to the method described
s
into such porous structures enables im- system Mk III Groovy, Nobel Biocare by Donath and Breuner (1982). The repre-
plants to interlock mechanically with the AB) were used in test animals. sentative section of each implant was
surrounding bone (Bobyn et al. 1980). ground along its long axis and stained
Micromachined grooves influence the cha- Animals and surgical procedure with hematoxylin and eosin. A light mi-
racteristics of bone deposition around im- The study was approved by the Animal croscope (Olympus BX microscope, Olym-
plants (Chehroudi et al. 1997). Grooved Research Committee of Seoul National pus, Tokyo, Japan) and image analysis
topography is thought to stimulate cell University (approval number: SNU- software (Kappa PS30C Imagebase, Kappa
migration and induce guided contact osteo- 081004-4) and all experiments were per- Opto-electrics GmbH, Gleichen, Ger-
genesis, the extent of which is dependent formed in accordance with the guidelines of many) were used to calculate the degree
upon the dimensions of the groove (Brun- the Institute of Laboratory Animal Re- of BIC. All microscopic measurements
ette & Chehroudi 1999; Davies 2003). It sources of Seoul National University. were made using a  10 objective and
has been reported that geometric grooves, Twelve adult New Zealand White male  10 eyepiece. The percentage of BIC was
which are clearly larger than osteoblasts, rabbits, weighing 2.5–3.0 kg, were used. calculated in four consecutive threads from
stimulate directed bone growth and deposi- Before surgery, the shaved skin over the the bone cortex (Fig. 1a). The BIC ratios in
tion within the grooves, consequently op- area of the proximal tibia was cleansed the groove-only of the experimental im-
timizing implant stability (Hall et al. with betadine. Incisions were made plant and the corresponding section of the
2005). through the fascia and periosteum in order control implant were also measured (Fig.
Hall et al. (2005) have pointed out that to expose the tibia metaphysis. The im- 1b and c).
variations in thread geometries within the plant sites were prepared with 2.0 and
range of 50–200 mm have been overlooked 3.0 mm twist drills (without screw tapping)
Resonance frequency analysis and mea-
in previous studies. Few studies have in- placed approximately 8 mm apart in the surement of removal torque value
vestigated the influence of geometrical fea- proximal section of each tibia. The im- The remaining six rabbits (three sacrificed
tures such as macroscopic grooves on plants were then inserted. The implants at 2 weeks and three sacrificed at 6 weeks
osseointegration. Implants with a macro- penetrated one cortical bone layer and three post-implant-insertion) were used for reso-
scopic groove on the inferior flank of an threads were visible above the cortex. Each nance frequency analysis (RFA) and mea-
anodized titanium surface have become rabbit received four implants, with two surement of removal torque value (RTV).
commercially available recently. There is implants being inserted into each tibia. Bone resonance frequencies were measured
insufficient evidence, however, concerning Cover screws were connected to the top using a measuring device (Osstellt Men-
the effects of such a design on bone re- of the fixtures and the surgical sites were tort, Integration Diagnostic AB, Göteborg,
sponse and implant success. closed in separate layers using resorbable Sweden) immediately following implant
The aim of the present study was to sutures for submerged healing. All animals insertion in all six animals, and then at
investigate the effect of the groove topogra- were administered 6.5 mg/kg gentamycin either 2 or 6 weeks in order to assess
phy of dental implants on the bone–im- daily for 3 days post-operatively. Six days implant stability. All measurements were
plant interface and implant stability in a post-operatively, one animal was sacrificed expressed as an implant stability quotient
rabbit tibia model using histomorphome- and excluded from the study due to inflam- (ISQ), ranging from 1 (the lowest stability)
try, resonance frequency analysis, and mation of the soft tissue. The other 11 to 100 (the highest stability). After expos-
measurement of removal torque value. animals recovered without complications. ing the implants, the cover screws and the
At either 2 or 6 weeks post-implant-inser- tissue above the fixtures were removed. A
tion, the animals were anesthetized and magnetic probe (SmartPegt, Integration
Materials and methods sacrificed by an intravenous administration Diagnostic AB) was connected to the im-
of potassium chloride. plant and used to detect vibration as a
Implant preparation measure of its frequency response. The
A total of 48 threaded, commercially avail- Histomorphometric analysis mean of three measurements was recorded
able titanium implants were used in the Five rabbits (two at 2 weeks and three at 6 as the representative ISQ value of each
present study. The implants were 8.5 mm weeks) were used for the histomorpho- implant.
in length and 3.75 mm in diameter. All of metric analysis. En bloc resection includ- The RTVs of each implant used for non-
the implants had an anodic oxidized tita- ing adjacent bone collar was performed for destructive RFA were also measured at 2
nium surface of highly crystalline titanium each set of implants and the samples were and 6 weeks. The magnetic probe was
oxide and microporous structures that ran- immediately fixed in 4% neutral formalde- removed and a manual connector (Star-
ged in size from a submicrometer level to hyde. The specimens were dehydrated and gript, Nobel Biocare AB) was engaged
s
10 mm (Hall & Lausmaa 2000). Twenty- embedded in light-curing resin (Technovit securely to the implant. The connector
four of these anodized implants (TiUnitet 7200 VLC, Heraus Kultzer, Wehrheim, was grabbed firmly by the jaws of the
Mk III, Nobel Biocare AB, Göteborg, Swe- Germany). Undecalcified ground sections removal torque (RT) tester (Model

1380 | Clin. Oral Impl. Res. 21, 2010 / 1379–1385 c 2010 John Wiley & Sons A/S

 Yoon et al  Effect of a macroscopic groove on bone

MGT50, Mark-10 Corp., Hicksville, NY, The percentage difference in RTVs between Statistics
USA). Slowly increasing reverse torque was each pair of implants from each rabbit, The non-parametric Wilcoxon’ signed rank
applied, and the peak torque value required defined as (RTVtest  RTVcontrol)  100/ test was used to calculate possible statisti-
to initiate reverse rotation was measured. RTVcontrol was also calculated. cal differences between the two groups.
A P-value of o0.05 was considered statis-
tically significant.

Results
Histomorphometric analysis
Light microscopy demonstrated that the
cortical bone formed after 2 weeks of heal-
ing was insufficient to fill the thread sur-
faces. Newly formed bone of low maturity
and density was observed to be adherent to
the implant surfaces near the cortical layer
(Fig. 2). Osteoid and the surrounding osteo-
blasts were found frequently within the
groove structure, in contact with the super-
ficial oxide area at the bone marrow space.
At 2 weeks, the mean and standard devia-
tion (SD) of the BIC percentage was
47.5  11.0% for the test group (Mk III
Groovy) and 38.0  18.9% for the control
group (TiUnitet Mk III) (Table 1). At 6
weeks, all implants were well integrated
and had established an intimate contact
Fig. 1. Schematic illustrations of implants for the evaluation of bone-to-implant contact (BIC). (a) The BIC was
with mature cortical bone (Fig. 3). The
measured from the first integrated thread to that directly above the cutting chamber area. The BIC ratio in the
groove only of the experimental implant (b) and the corresponding section of the control implant (c) were also BIC ratio for the test group was
measured. 56.0  8.4%, and that for the control

Fig. 2. Histological images at four different magnifications ( 10,  40,  100, and  200) at 2 weeks, from top to bottom; left column ([a]–[d]): control group
s
(TiUnitet Mk III), right column ([e]–[h]): test group (Brånemark system Mk III Groovy). Newly formed bone of low maturity is adherent to the implant surface. Osteoid
and active osteoblasts are found within the grooves on the thread flanks. Note that the shape of the cutting chamber differs according to the direction of the section.

c 2010 John Wiley & Sons A/S

 1381 | Clin. Oral Impl. Res. 21, 2010 / 1379–1385
Yoon et al  Effect of a macroscopic groove on bone

group was 51.9  6.0%. No significant tissue (Figs 2g and h and 3g and h). At 2 difference between the groups (P ¼ 0.028)
difference was found between the groups weeks, the percentage of BIC was (Table 1).
at either 2 or 6 weeks post-implant-inser- 51.2  5.8% for the groove of the test
tion (P ¼ 0.715, 0.345) (Table 1). group and 29.0  17.9% for the corre-
New bone formation and remodeling sponding flank surface of the control Resonance frequency analysis and mea-
surement of removal torque value
were observed predominantly within the group (Table 1). No significant difference
The results of RFA at the 2 and 6 week
grooves, and mineralized matrices were was found (P ¼ 0.068), but there was a
time-points are shown in Table 1. Imme-
observed to be in close contact with the tendency for homogenously high BIC in
diately after implantation, the mean ISQ
oxidized surface area. Almost all of the the macroscopic groove structure. At 6
values of the two implant groups were
grooves were filled with mineralized tissue weeks, the BIC ratio was 62.4  5.3%
similar. After 2 weeks, significant differ-
or unconnected islands of bone matrix, for the test group and 49.4  4.2% for
ences were observed in the ISQ values
including the thread surfaces in the marrow the control group. There was a significant
of the grooved implants compared with
those at the time of implant insertion
Table 1. Measured values of histomorphometric analysis and biomechanical tests (P ¼ 0.027), whereas the values of the con-
Sample Test group Control group P value
trol group did not differ significantly from
size (Means and SDs) (Means and SDs)
those at the time of implant insertion
BIC (%)
(P ¼ 0.168) (Fig. 4a). There were no signif-
2 weeks 4 47.5  11.0 38.0  18.9 0.715
6 weeks 6 56.0  8.4 51.9  6.0 0.345 icant differences in RFA between the two
BICn (%) groups (P40.05). The ISQ values of both
2 weeks 4 51.2  5.8 29.0  17.9 0.068 groups increased significantly between im-
6 weeks 6 62.4  5.3 49.4  4.2 0.028
plant insertion and 6 weeks (P ¼ 0.027 for
ISQ
2 weeks 6 68  1 65  2 0.058 the test group and P ¼ 0.028 for the control
6 weeks 6 73  2 70  3 0.043 group) (Fig. 4b). The grooved implants had
RTV (Ncm) significantly higher ISQ values than the
2 weeks 6 35.1  9.7 26.3  8.9 0.028
control implants (Po0.05).
6 weeks 6 75.6  10.5 58.9  14.7 0.027
The means and SDs of RTVs for the test
n
BIC, bone contact within grooves and on the corresponding flank surface. group at 2 and 6 weeks were 35.1  9.7
s
Control group, TiUnitet Mk III, Test group, Brånemark system Mk III Groovy.
and 75.6  10.5 N cm, respectively. The

Fig. 3. Histological images at four different magnifications ( 10,  40,  100, and  200) at 6 weeks, from top to bottom; left column ([a]–[d]): control group
s
(TiUnitet Mk III), right column ([e]–[h]): test group (Brånemark system Mk III Groovy). Note that all implants are integrated and that all grooves are filled with
mineralized bone. All specimens show an intimate contact with mature cortical bone. The differing shape of the cutting chamber in the lower part of implant can also
be observed.

1382 | Clin. Oral Impl. Res. 21, 2010 / 1379–1385 c 2010 John Wiley & Sons A/S

 Yoon et al  Effect of a macroscopic groove on bone

Fig. 4. Results of resonance frequency analysis (given as ISQ values) following 2 weeks (a) and 6 weeks (b) of healing. The ISQ values of the two groups increased
significantly between implant insertion and 6 weeks of healing (Po0.05).

corresponding values for the control group The histomorphometric results of this titative evaluation of the bone–implant
were 26.3  8.9 and 58.9  14.7 N cm, study are in accordance with those of interface (Aparicio et al. 2006).
respectively. Significant differences in Hall et al. (2005), who reported that The RTV results of the present study are
RTVs were found between grooved im- 78.7  15.8% of grooves and 46.2  in accordance with those of the rabbit tibia
plants and the control implants at 2 and 27% of corresponding flank surfaces were study of Hall et al. (2005), which showed
6 weeks post-implant-insertion (P ¼ 0.028, in contact with bone. There were numer- that grooved implants had approximately
¼ 0.027) (Table 1). The mean percentage ical differences between the present study 30% greater RTVs than implants without a
differences in the RTVs were 36.4  and that of Halland colleagues, possibly groove at 6 weeks post-implant-insertion.
27.5% at 2 weeks and 33.2  24.9% at 6 because of differences in the number of The present study demonstrated that the
weeks. Grooved implants showed a greater integrated threads, the amount of sur- mean RTV at 6 weeks was almost twice as
resistance to reverse torque than the control rounding bone, and the position of the high as that found by Hall and colleagues,
implants (Table 1). groove on the thread flank, which was on who reported 37.3  10.2 N cm for im-
the inferior surface in the present study and plants with a 110 mm-wide groove on the
on the superior surface in the study by Hall superior flank. Differences in the ratio of
Discussion and colleagues. Despite these differences, cortical vs. cancellous bone and the posi-
stimulated migration of the bone-forming tion of the groove may have influenced the
The present study has demonstrated the cells and subsequent bone tissue formation interfacial shear strength. If the geometric
effect of the groove topography of dental were evident within the groove structures characteristics of the implant provide a
implants on the bone–implant interface in both studies. mechanical anchorage within the bone,
and implant stability. A macroscopic The ISQ values of both the grooved and deformation of cortical bone during im-
groove may improve early bone response non-grooved implants increased signifi- plant removal is probably more difficult
and implant stability. Our results indicate cantly with the duration of healing, which than the deformation of cancellous bone,
that the groove shows an affinity for bone reflects changes and remodeling at the and is restricted by the protruding parts of
formation. There was no statistically sig- bone–implant interface during the process the thread at the interface (Sennerby et al.
nificant difference in BIC between the two of osseointegration (Abrahamsson et al. 1992). Further studies are required to eval-
groups, but this is explained by the fact that 2004). In studies of loaded anodic oxidized uate the effect of a positional change of the
both the experimental and control implants titanium implants in dogs, the average ISQ groove on the transmission of shear force.
had the same anodized surface. Our histo- values following 3 months of healing were We did not include pairwise comparisons
morphometric analysis demonstrated that found to be over 65 (Al-Nawas et al. 2006, between the two groups in identical anato-
bone grew intimately into the dental im- 2008). These findings are comparable with mical locations of the tibiae (using each
plant grooves. The results of the biomecha- those of the present study, as a bone re- implant as a measurement-unit) because
nical tests (RFA and RTV) showed that the modeling period of 12 weeks in dogs is these results were similar to those men-
groove structure had a positive influence equivalent to around 6 weeks in rabbits tioned above. Furthermore, the sample size
on implant stability. From the RTV per- (Roberts et al. 1984). A higher ISQ value in was too small to allow reliable statistical
centage differences calculated in the pre- RFA is considered to be an indication of a analysis of such pairwise comparisons. De-
sent study, we infer that the macroscopic more stable implant, and is attributable to spite the fact that bone quality differs in
groove increased implant stability by at bone growth into the groove structure. different areas of the rabbit tibia, previous
least 30%. However, the RFA cannot provide a quan- studies have neglected to consider whether

c 2010 John Wiley & Sons A/S

 1383 | Clin. Oral Impl. Res. 21, 2010 / 1379–1385
Yoon et al  Effect of a macroscopic groove on bone

the implant was inserted proximally or best consecutive threads’’, and ‘‘contact at during the early period of healing. A geo-
distally into the tibial metaphysis (Sen- whole implant thread surface’’ (Al-Nawas metric feature as a macroscopic groove may
nerby et al. 1992; Hall et al. 2005). et al. 2008). Selection of thread space may facilitate more rapid osseointegration and
It has been reported that a 6-week heal- not represent the actual BIC, but measure- improve implant stability in various clin-
ing period in the unloaded state in rabbits is ment of BIC at the whole implant thread ical conditions. Further studies are required
sufficient to allow woven bone to be re- surface may also be problematic because to confirm whether the improvement in
placed by mature, lamellar bone, which the shape of the cutting chamber, which is implant stability observed in this animal
can then adhere directly to the implant at the lower part of the dental implant, study will enhance treatment success in
surface and provide sufficient strength for differs according to the direction of the humans.
load bearing (Roberts et al. 1984). A section (Figs 2a, e and 3a, e). In the present
2-week healing period in rabbits is known study, we evaluated the BIC from the first
Acknowledgements: This study was
to be equivalent to one and a half months integrated thread to that directly above the
supported by a grant from the Seoul
in humans, indicating that rabbits heal cutting chamber area, which is considered
National University Dental Hospital
approximately three times more rapidly to be the most appropriate measurement.
Research Fund (contract grant number:
than humans (Roberts et al. 1984). We A limitation of the present study was its
04-2008-0024). The authors are grateful
used a rabbit tibia model and 2- and small sample size, particularly in the his-
to Dr. Jin-Sun Hong, Ji-Eun Moon, and
6-week observation time-points because tomorphometric analysis. Studies of larger
In-Phill Park of the Department of
these allow an adequate assessment of early samples are required, although the poten-
Prosthodontics, Seoul National
bone response and implant stability within tial for large sample sizes in animal studies
University Dental Hospital, for their
a relatively short period of time. The ana- is limited.
invaluable assistance with the animal
lysis of BIC is based on various methods of In conclusion, a macroscopic groove may
surgery.
calculation such as ‘‘contact at the three increase bone growth and implant stability

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