The purpose of this study was to evaluate the effect of defect type and depth as well as measurement direction on implant stability in an ex vivo peri-implant bovine rib bone model. Six kinds of defects (3-wall 2.5 mm, 3-wall 5 mm, 1-wall 2.5 mm, 1-wall 5 mm, circumferential 2.5 mm, circumferential 5 mm), and control (no defect) were prepared in 14 bovine rib bones. A total of 84 defects and 14 controls were created. The same type and size of implants (4 × 10 mm) were placed in each group. The thickness of cortical bone and the insertion torque were measured for each defect, and the implant stability quotient (ISQ) value was measured 3 times from 4 different directions. The thickness of cortical bone ranged from 2.71–3.18 mm. Insertion torque decreased as the defect size increased. As the defect size for the same defect depth increased, the ISQ value decreased (P < .001). There were significant differences between the ISQ values obtained with different measurement directions only between the control and 3-wall 5 mm defect (P < .0001). The ISQ value opposite to the defect direction was higher than that in the defect direction in all 3 directions of the 3-wall and 1-wall 5 mm defects. ISQ values were influenced by defect type and depth. Loss of cortical bone reduced the stability of implants and reduced the ISQ value. Measurement direction also influenced ISQ values.

Introduction

Implant stability can be defined as the absence of clinical mobility1  and can be evaluated by percussion tests, insertion torque, mobility, resonance frequency analysis (RFA) values, radiographic interpretation, and sensations of the operator.15  Although operator sense is a very good tool for evaluating implant stability, it is not an objective method and requires extensive experience.

Resonance frequency analysis (RFA), first described by Meredith et al,6  is now widely used to evaluate implant stability because it is an objective method and does not damage the implant.2  RFA results are expressed as implant stability quotients (ISQs), ranging in value from 1 to 100.2  Resonance frequency is determined by the stiffness of the bone-implant complex; this was demonstrated by Meredith et al, who performed repeated RFA measurements of implants placed in a self-curing resin.6  Various factors influence RFA, such as defect depth, implant stiffness, exposed fixture height, healing time, surface texture, implant shape, implant length, bone quality, and marginal bone loss.3,716 

The increase in the number of patients treated using dental implants seems to lead to a concomitant increase in the number of patients who suffer from peri-implant disease. Peri-implantitis includes alveolar bone loss around the implant. Bone defects around the implant can manifest in various forms and affect the stability of the implant.13,17  Bone defects in peri-implantitis lesions can be classified according to the criteria presented by Goldman and Cohen.18  One-wall intrabony defects are defects limited by 1 osseous wall and the implant surface. Three-wall intrabony defects are limited by 3 osseous walls and the implant surface. In peri-implantitis, circumferential defects are also common.19  The type of intrabony defect around the implant could affect the stability of implant to different extents. Although the effect of vertical bone loss on the stability of implants has been studied, the relationship between peri-implant bone defect type and the stability of implants has not yet been studied. Therefore, the purpose of this study was to evaluate the effect of defect type and depth as well as transducer direction on implant stability in an ex vivo peri-implant model, namely, bovine rib bone.

Materials and Methods

Drilling procedure and defect preparation

Fourteen frozen bovine rib bones were used in this study. Before the experiment, the frozen bovine rib bones were left for 3 hours at room temperature. The flat and wide side of the bovine rib bones—large enough to allow placement of 4-mm diameter implants—was used in this experiment. Seven implant beds were prepared in each rib bone, with the centers of the implant beds 15 mm apart from each other. The drilling sequence recommended by the manufacturer (Sola, Shinhung Co, Ltd, Seoul, Korea) was modified because of the thick cortical bone of the bovine rib as follows: 2.0 mm, 2.4/2.8 mm, and 3.2/3.6 mm using a 4.0 tap drill.

Six kinds of defects (3-wall 2.5 mm, 3-wall 5 mm, 1-wall 2.5 mm, 1-wall 5 mm, circumferential 2.5 mm, and circumferential 5 mm) and controls (no defect) were prepared. Three types of defect configurations were prepared (Figure 1). A 3-wall defect was prepared by removing the distal side of the prepared implant placement hole using a 4-mm trephine bur (Figure 1a). One-wall defects were prepared by removing bone 4 mm distal of the prepared implant hole using a #770 bur (Figure 1b). Circumferential defects were made using a trephine bur with an external diameter of 8 mm around the prepared hole. After drilling with the trephine bur, all remaining bone inside the trephine bur was removed using a #770 bur (Figure 1c). Each defect model was prepared at 2 different depths (2.5 mm and 5 mm). In the control, 1 drilling hole was left without creating a defect. The thickness of the cortical bone was measured using a UNC-15 probe. Outside the rib arch was considered the buccal side, and inside the rib arch was considered the lingual side. One-wall and 3-wall defects were made on the same side (distal side) in each bovine rib bone. The side opposite the defect was considered to be the mesial side (Figure 1d).

Figure 1.

Schematic drawings of defect types (occlusal view) and photo of bovine rib bone after installation of seven implants. (a) 3-wall defects. (b) 1-wall defects. (c) Circumferential defects. (d) Control and 6 kinds of defects in bovine rib bone. From left side (mesial side, opposite side of the defect) no defect, 1-wall 5-mm defect, 1-wall 2.5-mm defect, circumferential 5-mm defect, circumferential 2.5-mm defect, 3-wall 5-mm defect, and 3-wall 2.5-mm defect. The defect side was considered the distal side.

Figure 1.

Schematic drawings of defect types (occlusal view) and photo of bovine rib bone after installation of seven implants. (a) 3-wall defects. (b) 1-wall defects. (c) Circumferential defects. (d) Control and 6 kinds of defects in bovine rib bone. From left side (mesial side, opposite side of the defect) no defect, 1-wall 5-mm defect, 1-wall 2.5-mm defect, circumferential 5-mm defect, circumferential 2.5-mm defect, 3-wall 5-mm defect, and 3-wall 2.5-mm defect. The defect side was considered the distal side.

Implant placement and ISQ measurement

A total of 14 bovine rib bones were used for this study. Seven external connection type implants were placed in each rib bone. Implants with a 4-mm diameter and 10-mm length (Sola, Shinhung Co, Ltd, Seoul, Korea) were placed in each prepared hole. Insertion torque was measured during placement. After implant placement, the primary stability of the implant was measured. The ISQ value was measured from 4 directions: mesial, distal, buccal, and lingual. Measurements were repeated 3 times in each direction to improve precision and assess reproducibility. The mean of the 3 measurements in each direction was regarded as the ISQ value representative of that direction. The mean of 12 measurements in 4 directions was considered representative of the ISQ value of that implant.

Statistical analyses

Statistical analyses were performed with the help of an affiliated biostatistician in the biostatistics unit of Samsung Biomedical Research Institute. The results were analysed using statistical analyses software (SAS, SAS Institute Inc, Cary, NC). Cortical bone thickness, insertion torque, and ISQ values were analysed with a mixed model considering random effects between subjects using Tukey's method. P-values were corrected using Bonferroni's method to prevent inflated type I error. The significance level of these tests (P) was .05.

Results

Cortical bone thickness, insertion torque, and ISQ values are shown in Table 1. The original thickness of cortical bone ranged from 2.71–3.18 mm. All cortical bone was removed when creating 5-mm deep defects. However, thin cortical bone remained in the 2.5-mm deep defects. Insertion torque differed according to defect type and depth. Insertion torque in the control (17.93 ± 11.64) was significantly higher than that in any of the defects (P < .05). Insertion torque in the 2.5-mm deep defects was higher than that in the 5-mm deep inserts.

Table 1

Cortical bone thickness (mm), insertion torque (Ncm), and implant stability quotient (ISQ) value of the 6 defect types and control.

Cortical bone thickness (mm), insertion torque (Ncm), and implant stability quotient (ISQ) value of the 6 defect types and control.
Cortical bone thickness (mm), insertion torque (Ncm), and implant stability quotient (ISQ) value of the 6 defect types and control.

ISQ values varied widely according to defect type and depth. The ISQ value of circumferential 5-mm defects was the lowest (56.07 ± 8.51), while that of the control was the highest (84.70 ± 5.52). As the defect size increased for the same defect depth, the ISQ value decreased (P < .001). For 1-wall and circumferential defects, the ISQ values of the 2.5-mm defects were greater than those of the 5-mm defects (P < .0001). In 3-wall defects, the mean ISQ value of the 5-mm defects (81.74 ± 3.32) was higher than that of the 2.5-mm defects (80.93 ±4.88).

We measured ISQ values from 4 directions to evaluate the effect of the measurement direction on ISQ values (Table 2). Measurements were repeated 3 times in each direction. There were significant differences between the ISQ values obtained in different measurement directions only between the control and 3-wall 5-mm defect (P < .0001). In the control group, the ISQ values at the mesial and distal sides were higher than those at the buccal and lingual sides. However, the ISQ values at the buccal and lingual sides were higher than those at the mesial and distal sides in the 3-wall 5-mm defect. In addition, the ISQ value at the distal side (defect side) was lower than that at the mesial side (the opposite side of the defect) (P < .001). In 1-wall and circumferential defects, there was no significant differences among the 4 directions.

Table 2

Comparison of implant stability quotient (ISQ) values according to the measurement direction.

Comparison of implant stability quotient (ISQ) values according to the measurement direction.
Comparison of implant stability quotient (ISQ) values according to the measurement direction.

In 3-wall and 1-wall defects, ISQ values were divided into 3 directions: defect direction (distal side), opposite to the defect direction (mesial side), and perpendicular to the defect direction (buccal and lingual side). ISQ values were analysed according to these 3 directions (Table 3). The ISQ value opposite to the defect direction was higher than that in the defect direction. Only 2 5-mm defect depth groups showed statistically significant differences. In the circumferential defect and control groups, measurement direction orientation could be divided into 2 directions: parallel to the rib bone direction (mesial and distal direction) and perpendicular to the rib bone direction (buccal and lingual direction). ISQ values were evaluated in these 2 directions (Table 4). Although the ISQ values in the parallel direction were higher than those in the perpendicular direction, this difference was not significant (P > .05).

Table 3

Paired comparison of implant stability quotient (ISQ) values according to the measurement direction in 3- and 1-wall defects

Paired comparison of implant stability quotient (ISQ) values according to the measurement direction in 3- and 1-wall defects
Paired comparison of implant stability quotient (ISQ) values according to the measurement direction in 3- and 1-wall defects
Table 4

Paired comparison of implant stability quotient (ISQ) values according to the measurement direction in control and circumferential defects.

Paired comparison of implant stability quotient (ISQ) values according to the measurement direction in control and circumferential defects.
Paired comparison of implant stability quotient (ISQ) values according to the measurement direction in control and circumferential defects.

The reproducibility of all ISQ values measured 3 times was evaluated using a mixed effect model considering random effects to obtain the intraclass correlation coefficient (ICC). ICC was 0.993 (95% CI for ICC [0.991–0.995]).

Discussion

Implant stability is an important factor in evaluating implant success.20  The ISQ value is widely used to monitor implant stability objectively. ISQ values are affected by many factors.3,715  When ISQ measurements are performed after implant installation, the effect of marginal bone loss after implant placement can be masked by the ongoing healing process in a clinical setting. In our previous study, we recorded bone levels and ISQ values during the early healing phase following implant placement;21  measurements were performed every week for 12 weeks. Mean marginal bone loss over 12 weeks was 1.28 ± 0.51 mm on the mesial side and 1.32 ± 0.57 mm on the distal side of the implants. ISQ values were not significantly correlated with bone loss. Although this result could be due to bone loss lower than the threshold at which ISQ can discriminate,22  corticalisation of the surrounding bone during the healing process likely compensated for the loss of implant stability.

After initial marginal bone loss following implant placement, peri-implant defects can alter the ISQ value. We designed this study to evaluate the effect of defect type and depth on implant stability. The amount of cortical bone surrounding the implant fixture changes according to defect type and depth, and influences the stiffness of the implant-bone interface. Winter et al14  showed that implant stability increased as the thickness of cortical bone increased using finite element analysis. Tozum et al17  showed that an increase in peri-implant circular bone loss might decrease ISQ values using acrylic models. Hong et al3  also studied the influence of cortical bone on primary stability using 2 different types of polyurethane bone models. Cortical bone 1.5-mm thick increased the ISQ value significantly. In our study, defect type and depth affected the amount of cortical bone remaining, as well as the ISQ values. As defect size increased and loss of cortical bone increased, ISQ values decreased. Although bovine rib bone is thicker than human alveolar bone, all cortical bone was removed when creating 5-mm defects. However, a thin cortical bone layer remained in the 2.5-mm defect groups. This difference was responsible for the significant ISQ value difference between 2.5-mm defect and 5-mm defect group in the 1-wall and circumferential defects. This difference was also found in all 4 measurement directions. However, there was no significant difference in the ISQ values in the 3-wall defects. Loss of cortical bone in the 3-wall defects might not have been sufficient to influence the stability of the implant.

Rodrigo et al23  reported that no Straumann implant with ISQ ≥60 failed, while 19% of implants with ISQ ≤60 failed before the placement of the prosthetic restoration. The ISQ values of all groups (except the circumferential 5-mm group) was over 60 in this study. Because of thick cortical bone, the ISQ values was over 80 in the control and 3-wall defect type. However, the ISQ value in circumferential 5-mm defect type was less than 60. In a clinical situation, additional treatment to improve primary stability should be considered to reduce the possibility of implant failure.

Valderrama et al24  suggested that the specific orientation of measurement could affect the resonance frequency analysis reading, based on their observations that ISQ values were significantly different whether the transducer was parallel or perpendicular to the alveolar crest. Veltri et al25  and Fischer et al26  showed that buccal-palatal measurements were lower than mesial-distal measurements in totally edentulous maxilla. When they measured the ISQ value perpendicular to the bony crest, they found that the ISQ values were 8 to 10 units lower than those measured in the parallel orientation. In the current study, we found that in addition to the ISQ measurement direction, the defect type and direction of the defect also influenced ISQ values. ISQ values in the perpendicular orientation were 4 units lower than those in the parallel orientation in the control, and this difference was significant (P < .0001). The orientation of the transducer also influenced the ISQ values in the 3-wall 5-mm defects. The ISQ values of the distal side of 3-wall 5-mm defects were 1–4 units lower than those of the other sides (P < .0001).

In this study, defect depths of 2.5 mm and 5 mm resulted in significant difference in ISQ values for all defect types except 3-wall 5-mm defects. Lachmann et al,22  using an ISQ measuring device, reported a threshold of 2 mm (range: 1–3 mm) for RFA discrimination of bone loss. They recommended that because many factors—such as implant length and implant diameter—can influence the threshold, the threshold should be applied to follow-up on the same implant. Turkyilmaz et al13  demonstrated a negative correlation between peri-implant vertical bone defects and ISQ values in a cadaver model. The average ISQ values were calculated for 4 bone defect sites, and it was found that ISQ values decreased at a rate of 2.7 ISQ/mm.

Conclusion

RFA is a nondestructive method used extensively in clinical research to monitor implant stability due to its high reproducibility.2  Repeated measurement of ISQ values during this study confirmed the high reproducibility of ISQ values.

The limitations of this study include the small number of samples and variation among rib bone samples. Despite these limitations, however, we demonstrated that ISQ values of 1-wall and circumferential defects were influenced by defect type and depth. Loss of cortical bone reduced implant stability and ISQ values. Measurement direction also influenced ISQ values.

Abbreviations

     
  • ISQ

    implant stability quotient

  •  
  • RFA

    resonance frequency analysis

References

References
1
Sennerby
L
,
Meredith
N.
Implant stability measurements using resonance frequency analysis: biological and biomechanical aspects and clinical implications
.
Periodontol 2000
.
2008
;
47
:
51
66
.
2
Aparicio
C
,
Lang
NP
,
Rangert
B.
Validity and clinical significance of biomechanical testing of implant/bone interface
.
Clin Oral Implants Res
.
2006
;
17
(
suppl 2
):
2
7
.
3
Hong
J
,
Lim
YJ
,
Park
SO.
Quantitative biomechanical analysis of the influence of the cortical bone and implant length on primary stability
.
Clin Oral Implants Res
.
2012
;
23
:
1193
1197
.
4
Merheb
J
,
Coucke
W
,
Jacobs
R
,
Naert
I
,
Quirynen
M.
Influence of bony defects on implant stability
.
Clin Oral Implants Res
.
2010
;
21
:
919
923
.
5
Olive
J
,
Aparicio
C.
Periotest method as a measure of osseointegrated oral implant stability
.
Int J Oral Maxillofac Implants
. Winter
1990
;
5
:
390
400
.
6
Meredith
N
,
Alleyne
D
,
Cawley
P.
Quantitative determination of the stability of the implant-tissue interface using resonance frequency analysis
.
Clin Oral Implants Res
.
1996
;
7
:
261
267
.
7
Al-Nawas
B
,
Groetz
KA
,
Goetz
H
,
Duschner
H
,
Wagner
W.
Comparative histomorphometry and resonance frequency analysis of implants with moderately rough surfaces in a loaded animal model
.
Clin Oral Implants Res
.
2008
;
19
:
1
8
.
8
Huang
HM
,
Chiu
CL
,
Yeh
CY
,
Lin
CT
,
Lin
LH
,
Lee
SY.
Early detection of implant healing process using resonance frequency analysis
.
Clin Oral Implants Res
.
2003
;
14
:
437
443
.
9
Karl
M
,
Graef
F
,
Heckmann
S
,
Krafft
T.
Parameters of resonance frequency measurement values: a retrospective study of 385 ITI dental implants
.
Clin Oral Implants Res
.
2008
;
19
:
214
218
.
10
Meredith
N
,
Shagaldi
F
,
Alleyne
D
,
Sennerby
L
,
Cawley
P.
The application of resonance frequency measurements to study the stability of titanium implants during healing in the rabbit tibia
.
Clin Oral Implants Res
.
1997
;
8
:
234
243
.
11
Moon
SH
,
Um
HS
,
Lee
JK
,
Chang
BS
,
Lee
MK.
The effect of implant shape and bone preparation on primary stability
.
J Periodontal Implant Sci
.
2010
;
40
:
239
243
.
12
Sennerby
L
,
Persson
LG
,
Berglundh
T
,
Wennerberg
A
,
Lindhe
J.
Implant stability during initiation and resolution of experimental periimplantitis: an experimental study in the dog
.
Clin Implant Dent Relat Res
.
2005
;
7
:
136
140
.
13
Turkyilmaz
I
,
Sennerby
L
,
Yilmaz
B
,
Bilecenoglu
B
,
Ozbek
EN.
Influence of defect depth on resonance frequency analysis and insertion torque values for implants placed in fresh extraction sockets: a human cadaver study
.
Clin Implant Dent Relat Res
.
2009
;
11
:
52
58
.
14
Winter
W
,
Mohrle
S
,
Holst
S
,
Karl
M.
Parameters of implant stability measurements based on resonance frequency and damping capacity: a comparative finite element analysis
.
Int J Oral Maxillofac Implants
.
2010
;
25
:
532
539
.
15
Yoon
HC
,
Choi
JY
,
Jung
UW
,
et al
.
Effects of different depths of gap on healing of surgically created coronal defects around implants in dogs: a pilot study
.
J Periodontol
.
2008
;
79
:
355
361
.
16
Bayarchimeg
D
,
Namgoong
H
,
Kim
BK
,
et al
.
Evaluation of the correlation between insertion torque and primary stability of dental implants using a block bone test
.
J Periodontal Implant Sci
.
2013
;
43
:
30
36
.
17
Tozum
TF
,
Turkyilmaz
I
,
McGlumphy
EA.
Relationship between dental implant stability determined by resonance frequency analysis measurements and peri-implant vertical defects: an in vitro study
.
J Oral Rehabil
.
2008
;
35
:
739
744
.
18
Goldman
HM
,
Cohen
DW.
The intrabony pocket: classification and treatment
.
J Periodontol
.
1958
;
29
:
272
291
.
19
Schwarz
F
,
Herten
M
,
Sager
M
,
Bieling
K
,
Sculean
A
,
Becker
J.
Comparison of naturally occurring and ligature-induced peri-implantitis bone defects in humans and dogs
.
Clin Oral Implants Res
.
2007
;
18
:
161
170
.
20
Albrektsson
T
,
Zarb
GA.
Current interpretations of the osseointegrated response: clinical significance
.
Int J Prosthodont
.
1993
;
6
:
95
105
.
21
Yang
SM
,
Shin
SY
,
Kye
SB.
Relationship between implant stability measured by resonance frequency analysis (RFA) and bone loss during early healing period
.
Oral Surg Oral Med Oral Pathol Oral Radiol Endod
.
2008
;
105
:
e12
e19
.
22
Lachmann
S
,
Laval
JY
,
Jager
B
,
et al
.
Resonance frequency analysis and damping capacity assessment. Part 2: peri-implant bone loss follow-up. An in vitro study with the Periotest and Osstell instruments
.
Clin Oral Implants Res
.
2006
;
17
:
80
84
.
23
Rodrigo
D
,
Aracil
L
,
Martin
C
,
Sanz
M.
Diagnosis of implant stability and its impact on implant survival: a prospective case series study
.
Clin Oral Implants Res
.
2010
;
21
:
255
261
.
24
Valderrama
P
,
Oates
TW
,
Jones
AA
,
Simpson
J
,
Schoolfield
JD
,
Cochran
DL.
Evaluation of two different resonance frequency devices to detect implant stability: a clinical trial
.
J Periodontol
.
2007
;
78
:
262
272
.
25
Veltri
M
,
Balleri
P
,
Ferrari
M.
Influence of transducer orientation on Osstell stability measurements of osseointegrated implants
.
Clin Implant Dent Relat Res
.
2007
;
9
:
60
64
.
26
Fischer
K
,
Stenberg
T
,
Hedin
M
,
Sennerby
L.
Five-year results from a randomized, controlled trial on early and delayed loading of implants supporting full-arch prosthesis in the edentulous maxilla
.
Clin Oral Implants Res
.
2008
;
19
:
433
441
.