- Email: [email protected]
Evaluation of the relationship between Periotest values, marginal bone loss, and stability of single dental implants: A 3-year prospective study
CLINICAL RESEARCH
Evaluation of the relationship between Periotest values, marginal bone loss, and stability of single dental implants: A 3-year prospective study Waseem Khalaila, DMD,a Minaem Nasser, DMD,b and Zeev Ormianer, DMDc
ABSTRACT Statement of problem. Although the Periotest has been shown to provide reliable information about initial implant stability, whether Periotest values (PTVs) can be correlated with the stability of implants in function for several years is unclear. Purpose. The purpose of this prospective clinical study was to investigate implant stability by using PTVs, as well as changes in stability and peri-implant marginal bone levels (as measured by radiographs) over a 3-year follow-up period. The exploratory hypothesis was that there is a significant correlation between PTVs and bone loss around the implant and that PTVs can provide predictive information about marginal bone-level changes and implant stability over time. Material and methods. The study population included patients who needed single-tooth replacement with restoration of cemented fixed partial dentures. Clinical data, PTVs, and periapical radiographs were collected at the time points of implant placement, 3 to 6 months after insertion, and 1 year, 2 years, and 3 years after the final definitive prosthetic restoration. Pearson correlation coefficient tests were performed to estimate the correlation between the PTVs received at the first follow-up time point and the subsequent PTVs received during the followup period (up to 3 years after the restoration). The Pearson test was applied, as well as the t test and repeated-measures ANOVA, to evaluate PTVs and bone loss changes over time. The Pearson test was also applied to estimate the correlation between the bone loss values measured at the first follow-up visit and the subsequent bone loss values at the annual follow-up time points (up to and including 3 years after the restoration). Results. A total of 43 implants were inserted in 34 patients (26 men and 8 women); the average patient age was 52.8 years. A significant reduction in implant stability was detected between implant insertion and the 3- to 6-month follow-up time point, which was then followed by a significant increase in stability at the 1-year follow-up time point and then stabilized during the 2- and 3-year follow-up time points (P<.014). Furthermore, a significant correlation was found between PTVs at the 1-year follow-up and the PTVs at all measured follow-up time points (P<.05). A positive correlation was obtained with high-strength correlation coefficient R (R>0.7) at all follow-up time points. Bone loss changes during the follow-up time points were significantly different and correlated with PTVs (P<.001). Conclusions. The Periotest is a reliable device for assessing implant stability and providing predictive information about marginal bone level changes around an implant. (J Prosthet Dent 2019;-:---)
Obtaining stability of a dental implant during insertion is considered a critical factor for implant success.1 When an implant is stable, new bone is expected to fill the bone-implant connection area, and therefore most of the implant surface will eventually be in direct contact with vital bone tissue.1 Measuring initial implant stability provides important prognostic information, which can
assist in establishing the treatment plan and loading protocol.2 Stability has been defined as “measuring the difficulty of removing an object from a balancing point.”3 Clinically, the initial stability of an implant is conventionally understood as immobilization of the implant immediately after insertion.3 Historically, different methods have
a
Graduate student, Department of Oral Rehabilitation, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel. Graduate student, Department of Oral Rehabilitation, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel. c Senior Lecturer, Department of Oral Rehabilitation, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel. b
THE JOURNAL OF PROSTHETIC DENTISTRY
1
2
Volume
Clinical Implications Although further confirmatory studies are needed, Periotest values (PTVs) may be useful as a predictive tool to assess long-term implant success, as well as potentially serving as a surrogate marker for bone loss.
been used to measure implant stability at the time of insertion, including subjective evaluation by the treating surgeon,4,5 percussion tests,5 invasive reverse-torque tests,6 resonance frequency analyzers (Osstell AB), and electronic devices developed for testing tooth mobility (Periotest; Salvin Dental Specialties, Inc). The unique characteristic of the last 2 methods is the ability to measure implant stability in a noninvasive manner which does not damage the bone-implant interface. A resonance frequency analysis (RFA) instrument such as Osstell provides a measurement representing implant stability which is determined by the rigidity of the bone-implant complex.7-9 One of the drawbacks of the initial stability measurement with RFA is the lack of agreement regarding the correlation between the implant stability quotient (ISQ) values and the short- and longterm implant outcomes, mostly with regard to implants with low primary stability.10 RPA can be measured during the implant restoration phase but not after the implant-supported restoration is delivered if the prosthesis cannot be detached. The Periotest device was originally intended to measure the characteristics of the periodontal ligament (PDL) and thus determine the degree of tooth mobility.11,12 Results are digitally displayed in Periotest units (Periotest values [PTVs]) on a scale ranging from 8 (low mobility) to 50 (high mobility). Regarding implant mobility, the scale values are narrower and range between -5 and +5.13 The Periotest device can measure values even when an abutment or crown is attached to the implant. This enables monitoring of the stability of the implant even after loading and over time. An essential contributing factor that affects long-term implant stability is bone loss around the implant. While the implant is in function, bone loss and absorption of crestal bone occur at a varying level, independent of implant type, time of loading, and occlusal forces.14,15 Past research has shown that, even in successful implants that have been in function for a decade or more, cumulative bone loss is a substantial factor in compromising long-term success.16 Bone loss has been reported to be a cumulative value at the end of a follow-up period.2,17,18 The challenge of reviewing these results is understanding initial bone loss rates versus later bone loss rates. The bone loss value at THE JOURNAL OF PROSTHETIC DENTISTRY
-
Issue
-
the 1-year follow-up time point has been reported to represent initial bone loss that originates from a combination of mechanical and biological factors.19 Initial bone loss after 1 year of loading has been measured in several studies and reported to range from 0.4 to 0.83 mm of loss. Because of the importance of ascertaining implant stability at this 1-year postloading mark, it is important to develop and evaluate clinical methods to achieve an accurate implant prognosis.20-23 Although research has reported that PTV measurements made immediately after implant insertion could be correlated with later implant failure,24 whether PTVs can be correlated with bone-level changes, specifically marginal bone loss, has not been well established. The Periotest has been shown to provide reliable information about initial implant stability. Whether PTVs can be correlated with the stability of implants in function for several years is even less well established. The purpose of this prospective study was to investigate implant stability by using PTVs, as well as changes in stability and peri-implant marginal bone levels over a 3-year follow-up period. The research hypothesis was that a significant correlation would be found between PTVs and bone loss around the implant and that PTVs can provide predictive information about marginal bonelevel changes and implant stability over time. MATERIAL AND METHODS This study was approved by an ethics committee on January 3, 2014. The study population included patients who needed single-tooth replacement with restoration of an abutment-supported, cement-retained implant crown. Implants were to be inserted in healed bone without the use of bone grafts or in an edentulous area at least 3 months after extraction. All patients had to have American Society of Anesthesiologists (ASA) physical status classification of either 1 or 2. The study patients were enrolled from the predoctoral clinic at the School of Dental Medicine in Tel-Aviv University. Clinical data, PTVs, and periapical radiographs were collected at the following time points: baseline value (initial implant placement, immediately after insertion); first follow-up (at implant exposure, 3 to 6 months after insertion); second follow-up (1 year after definitive restoration); third follow-up (2 years after definitive restoration); and fourth follow-up (3 years after definitive restoration). Information was also collected regarding age, sex, and health status. Implant stability measurements were recorded by using the Periotest device as follows: a transfer coping was attached to the implant, and the head of the patient was stabilized so that the implants were perpendicular to the floor; the Periotest was held parallel to the floor for a more reliable result. The test point was 2 mm coronal to Khalaila et al
-
2019
3
Figure 1. A, Periotest device. B, Implant Periotest value measurement. Patient sitting in upright position and device located on coronal aspect of implant transfer coping.
Table 1. Implant characteristics
Jaw Maxilla
the implant-transfer connection point (Fig. 1). When a restoration was attached, it was placed 2-mm coronal to the implant-crown connection point. Each measurement was performed 3 times, and the average value was recorded for each implant. To assess marginal bone loss, radiographs were made by using a film holder (XCP Biteblock; Dentsply Sirona); the images were then scanned and saved in a personal computer. The peri-implant marginal bone level was measured at the time of implant insertion (baseline) and at the follow-up time pointsd3 to 6 months, 1 year, 2 years, and 3 years after implant restoration and loading. The ImageJ program (NIH Image; National Institutes of Health) was used to measure the images. Crestal bone changes were registered as modifications in the distance from the implant shoulder to the bone level on the mesial and distal sides (Fig. 2). To correct dimensional distortion, the apparent dimension of each implant was measured by using the program and then compared with Khalaila et al
Position
Mandible
Anterior
Posterior
10
11.5
13
16
3.75
4.2
5
30
6
37
12
7
21
3
19
16
8
13
Figure 2. Bone loss measurement. Blue line indicates implant length from coronal part to apex. Yellow line displays bone loss.
Implant Diameter (mm)
Implant Length (mm)
the real implant length. In addition, for each implant, mesial-distal bone level measurements were made and averaged. Statistical analyses were performed by using a statistical software program (IBM SPSS Statistics, v25; IBM Corp) (a=.05). The Pearson correlation coefficient tests were performed to estimate the correlation between the PTVs received at the first follow-up time point and the subsequent PTVs during the follow-up period (up to 3 years after restoration). The Pearson test was applied, as well as the t test and repeated-measures ANOVA, to evaluate PTVs and bone loss changes over time. The Pearson test was also applied to estimate the correlation between the bone loss values measured at the first follow-up time point and the subsequent bone loss values at the annual follow-up time points (up to and including 3 years after restoration). RESULTS A total of 43 implants were inserted in 34 patients (26 men and 8 women). In 9 patients, 2 implants were inserted in areas that met the inclusion criteria. The average patient age was 52.8 years. The average diameter of the inserted implants was 4.15 mm (range: 3.75 to 5.0 mm), and the average length was 12.12 mm (range: 10 to 16 mm). Among the 43 implants, 13 (30%) were placed in the maxilla, and 30 (70%) were placed in the mandible (Table 1). Implant stability (measured by PTVs) ranged from −7.25 to 20 with a mean value of −0.165 at implant
THE JOURNAL OF PROSTHETIC DENTISTRY
4
Volume
-
Issue
-
Table 2. Pearson correlations between Periotest values Follow-up PTV (3 to 6 mo After Insertion)
1 y After Restoration PTV
2 y After Restoration PTV
3 y After Restoration PTV
Pearson correlation
.699**
.573**
-.095
-.090
P (2-tailed)
<.001
<.001
.717
.781
40
33
33
33
.573**
d
PTV Placement
N 1-y Pearson correlation
.584*
.593*
.001
.014
.042
33
17
12
Pearson correlation
.409
d
.984**
P (2-tailed)
.103
<.001
33
33
P (2-tailed) N 2-y
N
Estimated Marginal Means
PTV, Periotest value. *P<.05 and **P<.01.
Table 3. Repeated-measures ANOVA: PTV measurements and implant stability
3.00 2.00
Time
Mean
Standard Error
F
1.00
Placement
0.809
0.500
12.510*
0.00
Follow-up
2.229
0.701
1y
-2.688
0.638
–1.00
2y
-2.691
1.257
–2.00
3y
-3.045
1.118
PTV, Periotest value. Repeated-measures ANOVA test performed. Sphericity assumed (F=16.85, *P<.01).
–3.00 Placement Follow up
1
2
3
Time (y) Figure 3. Repeated-measures test for Periotest values.
placement, 0.427 at first follow-up (3 to 6 months after insertion), −2.170 at 1 year, −2.652 at 2 years, and 3.166 at 3 years after implant insertion. A significant correlation was found between PTVs at placement and PTVs at the first follow-up (3 to 6 months after insertion) and 1 year of follow-up. In addition, a significant correlation was found between PTVs at 1-year follow-up and PTVs at all annual follow-up time points (up to and including 3 years). A significant correlation was obtained with high-strength correlation coefficient R (R=0.984) between the PTVs at the 2-year and 3-year follow-up time points (Table 2). The repeated-measures ANOVA revealed a significant change in PTVs throughout the follow-up time points. An increase in PTVs demonstrated a decrease in stability at the second follow-up (1 year after restoration) time point. However, a sharp decrease in the values at the third follow-up time point (2 years after restoration) showed greater stability 1 year after implant insertion. At the 2-year and 3-year follow-up time points, the PTVs stabilized (Fig. 3; Table 3). Radiographic evaluation of the implants revealed a mean distance from the implant shoulder to the crestal bone level of 1.1 mm at first follow-up time point (3 to 6 months after insertion), 1.732 mm at 1 year, 1.738 mm at THE JOURNAL OF PROSTHETIC DENTISTRY
2 years, and 1.964 mm at 3 years. A significant correlation was found between bone loss values at all follow-up time points. A positive correlation was obtained with highstrength correlation coefficient R (R>0.7) at all follow-up time points (Table 4). The repeated-measures test identified a significant change in bone loss values throughout the study period. The bone loss rate was most notable in the first period (3 to 6 months after implant insertion), while it decreased at the follow-up time points of 1 year, 2 years, and 3 years (F=16.85, P<.01) (Fig. 4). The Pearson test showed a statistically significant correlation between PTVs at placement and bone loss values at all follow-up time points. A similar result was found in the PTVs at follow-up (Table 5). The independent samples t test identified no significant difference between the maxilla and the mandible or between the anterior and the posterior areas in terms of PTVs and the amount of bone loss. Patient age, sex, and health status did not have a significant impact on the PTVs or on bone loss values during the follow-up time points. DISCUSSION In this study, Periotest values at implant placement, as well as at the follow-up time point of 3 to 6 months later, were significantly correlated with bone loss values at all follow-up time points, which is a prognostic indicator in determining implant success. The results of this study Khalaila et al
-
2019
5
Table 4. Pearson correlations between bone loss values Bone Loss
1-y Follow-up Bone Loss
2-y Follow-up Bone Loss
3-y Follow-up Bone Loss
Pearson correlation
.817*
.709*
.881*
P (2-tailed)
.000
.001
.000
33
13
13
d
.992*
.982*
.000
.000
33
33
d
.997*
Follow-up
N 1-y follow-up Pearson correlation P (2-tailed) N 2-y follow-up Pearson correlation
d
P (2-tailed)
.000
N
33
Estimated Marginal Means
*P<.01.
2.50
Table 5. Pearson correlations between PTV and bone loss values PTV
2.00
1-y Follow-up 2-y Follow-up 3-y Follow-up Bone Loss Bone Loss Bone Loss
Placement
1.50 1.00
Pearson correlation
.381*
.556**
.614**
.791**
P (2-tailed)
.015
.001
.009
.002
40
33
33
33
Pearson correlation
.343*
.409*
.600*
.834**
P (2-tailed)
.03
.02
.011
.001
N
40
33
33
33
N Follow-up
0.50 0.00
Follow-up Bone Loss
Placement Follow up
1
2
3
Time (y) Figure 4. Repeated-measures test for estimated bone loss (mm).
confirm the research hypothesis that a significant correlation exists between PTVs and bone loss. In clinical practice, long-term follow-up assessments of implants are essential because changes in implant stability and bone levels are expected after the initial osseointegration of implants; for example, bone remodeling is accomplished mainly after 1 year.3 As the clinical success of implants depends on initial and ongoing stability after implant insertion, the development of a noninvasive method that provides an assessment of implant stability and possible prognostic information about future stability and bone loss is of benefit to clinicians. Resonance analysis instruments such as Osstell have been reported to provide an objective assessment of implant stability.8,9 The main drawback of RFA devices is that they can be used only in the early stages of implant insertion when the implant is not attached to the definitive restoration. In the present study, the use of the Periotest device allowed the evaluation of implant stability after the definitive restoration was attached. The mean PTV recorded at implant placement was −0.1605, which was consistent with the mean PTV of −0.27 reported
Khalaila et al
*P<.05 and **P<.01.
by Adell et al.16 A significant reduction in implant stability was found at the 3- to 6-month follow-up, which was then followed by a significant increase in stability at the 1-year follow-up. The dynamic changes in stability (as measured by PTVs) can be explained by the transition from the primary mechanical stability provided by the implant design to the biological stability provided by the newly formed bone as osseointegration occurs, which takes place during early wound healing.25 Additionally, the significant correlations between PTVs between each follow-up time point confirm findings from past studies showing that the Periotest is a reliable clinical tool for evaluating implant stability.24 The study findings also demonstrated that PTVs stabilized after the 1-year after-restoration time point, which significantly correlates with PTVs recorded at all other follow-up time points.24,26-28 One of the limitations of the Periotest device is its ability to measure only in the facial-lingual direction. The thin labial or buccal bone plate may impair the measurement results. A study that compared different implant diameters (3.7, 4.2, 6.0 mm) and the surrounding bone volume reported that only the 6.0-mm-diameter
THE JOURNAL OF PROSTHETIC DENTISTRY
6
Volume
implant had any validity on stress exerted on the surrounding bone.29 This type of implant was not used in this study. In addition to implant stability, peri-implant marginal bone loss is an essential treatment outcome measure. Bone loss measurement has been reported to be a reliable indicator of bone response to the surgical procedure and subsequent occlusal loading.14,15 In this study, the greatest amount of peri-implant bone loss was noticed between the time point of implant insertion and 3 to 6 months later, with an average loss 1.1 mm. This can be explained by bone remodeling, which starts immediately after implant insertion and represents the phase of active bone change. The mean bone loss values recorded in this study were greater than those in previous studies.20-22,30,31 This may be related to differences in measurement and statistical methods, implant macrostructure design, surgical technique, or random variability. There are some limitations in this study including sample size and measuring only implants inserted in healed bone. Further studies assessing long-time implant stability in grafted bone and in immediate implant placement are needed.
10. 11. 12. 13. 14. 15. 16. 17.
18. 19. 20.
21.
CONCLUSIONS Based on the findings of this clinical study, the following conclusions were drawn:
22. 23.
1. The Periotest device provided a reliable assessment of implant stability and predictive information about marginal bone level changes around an implant. 2. PTVs may be useful as a predictive tool for assessing long-term implant success, as well as serving as a surrogate marker for bone loss. REFERENCES
24. 25. 26. 27. 28.
1. Ivanoff CJ, Sennerby L, Lekholm U. Influence of initial implant mobility on the integration of titanium implants. An experimental study in rabbits. Clin Oral Implants Res 1996;7:120-7. 2. de Souza JG, Neto AR, Filho GS, Dalago HR, de Souza Junior JM, Bianchini MA. Impact of local and systemic factors on additional peri-implant bone loss. Quintessence Int 2013;44:415-24. 3. Molly L. Bone density and primary stability in implant therapy. Clin Oral Implants Res 2006;17 Suppl 2:124-35. 4. Huang HM, Pan LC, Lee SY, Chiu CL, Fan KH, Ho KN. Assessing the implant/bone interface by using natural frequency analysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:285-91. 5. Boronat-Lopez A, Penarrocha-Diago M, Martinez-Cortissoz O, MinguezMartinez I. Resonance frequency analysis after the placement of 133 dental implants. Med Oral Patol Oral Cir Bucal 2006;11:E272-6. 6. Sullivan DY, Sherwood RL, Collins TA, Krogh PH. The reverse-torque test: a clinical report. Int J Oral Maxillofac Implants 1996;11:179-85. 7. 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;14:437-43. 8. Meredith N, Book K, Friberg B, Jemt T, Sennerby L. Resonance frequency measurements of implant stability in vivo. A cross-sectional and longitudinal study of resonance frequency measurements on implants in the edentulous and partially dentate maxilla. Clin Oral Implants Res 1997;8:226-33. 9. Herrero-Climent M, Albertini M, Rios-Santos J-V, Lázaro-Calvo P, Fernández-Palacín A, Bullon P. Resonance frequency analysis-reliability in
THE JOURNAL OF PROSTHETIC DENTISTRY
29. 30.
31.
-
Issue
-
third generation instruments: Osstell mentor®. Med Oral Patol Oral Cir Bucal 2012;17:e801-6. 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;21:255-61. Schulte W, Lukas D. Periotest to monitor osseointegration and to check the occlusion in oral implantology. J Oral Implantol 1993;19:23-32. Schulte W, Lukas D, Erenst E. Periotest values and tooth mobility in periodontal disease. Quintessence Int 1990;21:289-93. 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. Ma S, Payne AG. Marginal bone loss with mandibular two-implant overdentures using different loading protocols: a systematic literature review. Int J Prosthodont 2010;23:117-26. Ormianer Z, Matalon S, Block J, Kohen J. Dental implant thread design and the consequences on long-term marginal bone loss. Implant Dent 2016;25: 471-7. Adell R, Lekholm U, Rockler B, Branemark PI. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10:387-416. Krebs M, Schmenger K, Neumann K, Weigl P, Moser W, Nentwig GH. Long-term evaluation of ANKYLOS(R) dental implants, part i: 20-year life table analysis of a longitudinal study of more than 12,500 implants. Clin Implant Dent Relat Res 2015;17 Suppl 1:e275-86. Vazquez Alvarez R, Perez Sayans M, Gayoso Diz P, Garcia Garcia A. Factors affecting peri-implant bone loss: a post-five-year retrospective study. Clin Oral Implants Res 2015;26:1006-14. Cassetta M, Pranno N, Calasso S, Di Mambro A, Giansanti M. Early periimplant bone loss: a prospective cohort study. Int J Oral Maxillofac Surg 2015;44:1138-45. cepanovic M, Todorovic A, Markovic A, Patrnogic V, Milicic B, Moufti AM, S et al. Immediately loaded mini dental implants as overdenture retainers: 1-Year cohort study of implant stability and peri-implant marginal bone level. Ann Anat 2014;199:85-91. Flichy-Fernández AJ, Ata-Ali J, Palma-Carrio C, Peñarrocha-Oltra D, Conejero J, Peñarrocha J. Radiological assessment of peri-implant bone loss: a 12-month retrospective study. J Clin Exp Dent 2011;3:e430-4. Pikner SS, Grondahl K, Jemt T, Friberg B. Marginal bone loss at implants: a retrospective, long-term follow-up of turned Branemark System implants. Clin Implant Dent Relat Res 2009;11:11-23. Wagenberg B, Froum SJ. Long-term bone stability around 312 roughsurfaced immediately placed implants with 2-12-year follow-up. Clin Implant Dent Relat Res 2015;17:658-66. Aparicio C. The use of the Periotest value as the initial success criteria of an implant: 8-year report. Int J Periodontics Restorative Dent 1997;17: 150-61. Raghavendra S, Wood MC, Taylor TD. Early wound healing around endosseous implants: a review of the literature. Int J Oral Maxillofac Implants 2005;20:425-31. Berthold C, Holst S, Schmitt J, Goellner M, Petschelt A. An evaluation of the Periotest method as a tool for monitoring tooth mobility in dental traumatology. Dent Traumatol 2010;26:120-8. Meredith N. Assessment of implant stability as a prognostic determinant. Int J Prosthodont 1998;11:491-501. Noguerol B, Munoz R, Mesa F, de Dios Luna J, O’Valle F. Early implant failure. Prognostic capacity of Periotest: retrospective study of a large sample. Clin Oral Implants Res 2006;17:459-64. Ormianer Z, Patli A, Demiralp B, Heller G, Lewinstrin I, Khayat P. Implant supported first molar restoration: correlation of finite element analysis with clinical outcomes. Int J Oral Maxillofac Implants 2012;27:e1-12. Mangano C, Mangano F, Piattelli A, Iezzi G, Mangano A, La Colla L. Prospective clinical evaluation of 1920 Morse taper connection implants: results after 4 years of functional loading. Clin Oral Implants Res 2009;20: 254-61. Bratu E, Chan HL, Mihali S, Karancsi O, Bratu DC, Fu JH, et al. Implant survival rate and marginal bone loss of 6-mm short implants: a 2-year clinical report. Int J Oral Maxillofac Implants 2014;29:1425-8.
Corresponding author: Dr Zeev Ormianer Department of Oral Rehabilitation School of Dental Medicine Tel Aviv University Ramat Aviv, Tel Aviv 69978 ISRAEL Email: [email protected] Copyright © 2019 by the Editorial Council for The Journal of Prosthetic Dentistry. https://doi.org/10.1016/j.prosdent.2019.08.023
Khalaila et al
Evaluation of the relationship between Periotest values, marginal bone loss, and stability of single dental implants: A 3-year prospective study Waseem Khalaila, DMD,a Minaem Nasser, DMD,b and Zeev Ormianer, DMDc
ABSTRACT Statement of problem. Although the Periotest has been shown to provide reliable information about initial implant stability, whether Periotest values (PTVs) can be correlated with the stability of implants in function for several years is unclear. Purpose. The purpose of this prospective clinical study was to investigate implant stability by using PTVs, as well as changes in stability and peri-implant marginal bone levels (as measured by radiographs) over a 3-year follow-up period. The exploratory hypothesis was that there is a significant correlation between PTVs and bone loss around the implant and that PTVs can provide predictive information about marginal bone-level changes and implant stability over time. Material and methods. The study population included patients who needed single-tooth replacement with restoration of cemented fixed partial dentures. Clinical data, PTVs, and periapical radiographs were collected at the time points of implant placement, 3 to 6 months after insertion, and 1 year, 2 years, and 3 years after the final definitive prosthetic restoration. Pearson correlation coefficient tests were performed to estimate the correlation between the PTVs received at the first follow-up time point and the subsequent PTVs received during the followup period (up to 3 years after the restoration). The Pearson test was applied, as well as the t test and repeated-measures ANOVA, to evaluate PTVs and bone loss changes over time. The Pearson test was also applied to estimate the correlation between the bone loss values measured at the first follow-up visit and the subsequent bone loss values at the annual follow-up time points (up to and including 3 years after the restoration). Results. A total of 43 implants were inserted in 34 patients (26 men and 8 women); the average patient age was 52.8 years. A significant reduction in implant stability was detected between implant insertion and the 3- to 6-month follow-up time point, which was then followed by a significant increase in stability at the 1-year follow-up time point and then stabilized during the 2- and 3-year follow-up time points (P<.014). Furthermore, a significant correlation was found between PTVs at the 1-year follow-up and the PTVs at all measured follow-up time points (P<.05). A positive correlation was obtained with high-strength correlation coefficient R (R>0.7) at all follow-up time points. Bone loss changes during the follow-up time points were significantly different and correlated with PTVs (P<.001). Conclusions. The Periotest is a reliable device for assessing implant stability and providing predictive information about marginal bone level changes around an implant. (J Prosthet Dent 2019;-:---)
Obtaining stability of a dental implant during insertion is considered a critical factor for implant success.1 When an implant is stable, new bone is expected to fill the bone-implant connection area, and therefore most of the implant surface will eventually be in direct contact with vital bone tissue.1 Measuring initial implant stability provides important prognostic information, which can
assist in establishing the treatment plan and loading protocol.2 Stability has been defined as “measuring the difficulty of removing an object from a balancing point.”3 Clinically, the initial stability of an implant is conventionally understood as immobilization of the implant immediately after insertion.3 Historically, different methods have
a
Graduate student, Department of Oral Rehabilitation, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel. Graduate student, Department of Oral Rehabilitation, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel. c Senior Lecturer, Department of Oral Rehabilitation, The Maurice and Gabriela Goldschleger School of Dental Medicine, Tel Aviv University, Tel Aviv, Israel. b
THE JOURNAL OF PROSTHETIC DENTISTRY
1
2
Volume
Clinical Implications Although further confirmatory studies are needed, Periotest values (PTVs) may be useful as a predictive tool to assess long-term implant success, as well as potentially serving as a surrogate marker for bone loss.
been used to measure implant stability at the time of insertion, including subjective evaluation by the treating surgeon,4,5 percussion tests,5 invasive reverse-torque tests,6 resonance frequency analyzers (Osstell AB), and electronic devices developed for testing tooth mobility (Periotest; Salvin Dental Specialties, Inc). The unique characteristic of the last 2 methods is the ability to measure implant stability in a noninvasive manner which does not damage the bone-implant interface. A resonance frequency analysis (RFA) instrument such as Osstell provides a measurement representing implant stability which is determined by the rigidity of the bone-implant complex.7-9 One of the drawbacks of the initial stability measurement with RFA is the lack of agreement regarding the correlation between the implant stability quotient (ISQ) values and the short- and longterm implant outcomes, mostly with regard to implants with low primary stability.10 RPA can be measured during the implant restoration phase but not after the implant-supported restoration is delivered if the prosthesis cannot be detached. The Periotest device was originally intended to measure the characteristics of the periodontal ligament (PDL) and thus determine the degree of tooth mobility.11,12 Results are digitally displayed in Periotest units (Periotest values [PTVs]) on a scale ranging from 8 (low mobility) to 50 (high mobility). Regarding implant mobility, the scale values are narrower and range between -5 and +5.13 The Periotest device can measure values even when an abutment or crown is attached to the implant. This enables monitoring of the stability of the implant even after loading and over time. An essential contributing factor that affects long-term implant stability is bone loss around the implant. While the implant is in function, bone loss and absorption of crestal bone occur at a varying level, independent of implant type, time of loading, and occlusal forces.14,15 Past research has shown that, even in successful implants that have been in function for a decade or more, cumulative bone loss is a substantial factor in compromising long-term success.16 Bone loss has been reported to be a cumulative value at the end of a follow-up period.2,17,18 The challenge of reviewing these results is understanding initial bone loss rates versus later bone loss rates. The bone loss value at THE JOURNAL OF PROSTHETIC DENTISTRY
-
Issue
-
the 1-year follow-up time point has been reported to represent initial bone loss that originates from a combination of mechanical and biological factors.19 Initial bone loss after 1 year of loading has been measured in several studies and reported to range from 0.4 to 0.83 mm of loss. Because of the importance of ascertaining implant stability at this 1-year postloading mark, it is important to develop and evaluate clinical methods to achieve an accurate implant prognosis.20-23 Although research has reported that PTV measurements made immediately after implant insertion could be correlated with later implant failure,24 whether PTVs can be correlated with bone-level changes, specifically marginal bone loss, has not been well established. The Periotest has been shown to provide reliable information about initial implant stability. Whether PTVs can be correlated with the stability of implants in function for several years is even less well established. The purpose of this prospective study was to investigate implant stability by using PTVs, as well as changes in stability and peri-implant marginal bone levels over a 3-year follow-up period. The research hypothesis was that a significant correlation would be found between PTVs and bone loss around the implant and that PTVs can provide predictive information about marginal bonelevel changes and implant stability over time. MATERIAL AND METHODS This study was approved by an ethics committee on January 3, 2014. The study population included patients who needed single-tooth replacement with restoration of an abutment-supported, cement-retained implant crown. Implants were to be inserted in healed bone without the use of bone grafts or in an edentulous area at least 3 months after extraction. All patients had to have American Society of Anesthesiologists (ASA) physical status classification of either 1 or 2. The study patients were enrolled from the predoctoral clinic at the School of Dental Medicine in Tel-Aviv University. Clinical data, PTVs, and periapical radiographs were collected at the following time points: baseline value (initial implant placement, immediately after insertion); first follow-up (at implant exposure, 3 to 6 months after insertion); second follow-up (1 year after definitive restoration); third follow-up (2 years after definitive restoration); and fourth follow-up (3 years after definitive restoration). Information was also collected regarding age, sex, and health status. Implant stability measurements were recorded by using the Periotest device as follows: a transfer coping was attached to the implant, and the head of the patient was stabilized so that the implants were perpendicular to the floor; the Periotest was held parallel to the floor for a more reliable result. The test point was 2 mm coronal to Khalaila et al
-
2019
3
Figure 1. A, Periotest device. B, Implant Periotest value measurement. Patient sitting in upright position and device located on coronal aspect of implant transfer coping.
Table 1. Implant characteristics
Jaw Maxilla
the implant-transfer connection point (Fig. 1). When a restoration was attached, it was placed 2-mm coronal to the implant-crown connection point. Each measurement was performed 3 times, and the average value was recorded for each implant. To assess marginal bone loss, radiographs were made by using a film holder (XCP Biteblock; Dentsply Sirona); the images were then scanned and saved in a personal computer. The peri-implant marginal bone level was measured at the time of implant insertion (baseline) and at the follow-up time pointsd3 to 6 months, 1 year, 2 years, and 3 years after implant restoration and loading. The ImageJ program (NIH Image; National Institutes of Health) was used to measure the images. Crestal bone changes were registered as modifications in the distance from the implant shoulder to the bone level on the mesial and distal sides (Fig. 2). To correct dimensional distortion, the apparent dimension of each implant was measured by using the program and then compared with Khalaila et al
Position
Mandible
Anterior
Posterior
10
11.5
13
16
3.75
4.2
5
30
6
37
12
7
21
3
19
16
8
13
Figure 2. Bone loss measurement. Blue line indicates implant length from coronal part to apex. Yellow line displays bone loss.
Implant Diameter (mm)
Implant Length (mm)
the real implant length. In addition, for each implant, mesial-distal bone level measurements were made and averaged. Statistical analyses were performed by using a statistical software program (IBM SPSS Statistics, v25; IBM Corp) (a=.05). The Pearson correlation coefficient tests were performed to estimate the correlation between the PTVs received at the first follow-up time point and the subsequent PTVs during the follow-up period (up to 3 years after restoration). The Pearson test was applied, as well as the t test and repeated-measures ANOVA, to evaluate PTVs and bone loss changes over time. The Pearson test was also applied to estimate the correlation between the bone loss values measured at the first follow-up time point and the subsequent bone loss values at the annual follow-up time points (up to and including 3 years after restoration). RESULTS A total of 43 implants were inserted in 34 patients (26 men and 8 women). In 9 patients, 2 implants were inserted in areas that met the inclusion criteria. The average patient age was 52.8 years. The average diameter of the inserted implants was 4.15 mm (range: 3.75 to 5.0 mm), and the average length was 12.12 mm (range: 10 to 16 mm). Among the 43 implants, 13 (30%) were placed in the maxilla, and 30 (70%) were placed in the mandible (Table 1). Implant stability (measured by PTVs) ranged from −7.25 to 20 with a mean value of −0.165 at implant
THE JOURNAL OF PROSTHETIC DENTISTRY
4
Volume
-
Issue
-
Table 2. Pearson correlations between Periotest values Follow-up PTV (3 to 6 mo After Insertion)
1 y After Restoration PTV
2 y After Restoration PTV
3 y After Restoration PTV
Pearson correlation
.699**
.573**
-.095
-.090
P (2-tailed)
<.001
<.001
.717
.781
40
33
33
33
.573**
d
PTV Placement
N 1-y Pearson correlation
.584*
.593*
.001
.014
.042
33
17
12
Pearson correlation
.409
d
.984**
P (2-tailed)
.103
<.001
33
33
P (2-tailed) N 2-y
N
Estimated Marginal Means
PTV, Periotest value. *P<.05 and **P<.01.
Table 3. Repeated-measures ANOVA: PTV measurements and implant stability
3.00 2.00
Time
Mean
Standard Error
F
1.00
Placement
0.809
0.500
12.510*
0.00
Follow-up
2.229
0.701
1y
-2.688
0.638
–1.00
2y
-2.691
1.257
–2.00
3y
-3.045
1.118
PTV, Periotest value. Repeated-measures ANOVA test performed. Sphericity assumed (F=16.85, *P<.01).
–3.00 Placement Follow up
1
2
3
Time (y) Figure 3. Repeated-measures test for Periotest values.
placement, 0.427 at first follow-up (3 to 6 months after insertion), −2.170 at 1 year, −2.652 at 2 years, and 3.166 at 3 years after implant insertion. A significant correlation was found between PTVs at placement and PTVs at the first follow-up (3 to 6 months after insertion) and 1 year of follow-up. In addition, a significant correlation was found between PTVs at 1-year follow-up and PTVs at all annual follow-up time points (up to and including 3 years). A significant correlation was obtained with high-strength correlation coefficient R (R=0.984) between the PTVs at the 2-year and 3-year follow-up time points (Table 2). The repeated-measures ANOVA revealed a significant change in PTVs throughout the follow-up time points. An increase in PTVs demonstrated a decrease in stability at the second follow-up (1 year after restoration) time point. However, a sharp decrease in the values at the third follow-up time point (2 years after restoration) showed greater stability 1 year after implant insertion. At the 2-year and 3-year follow-up time points, the PTVs stabilized (Fig. 3; Table 3). Radiographic evaluation of the implants revealed a mean distance from the implant shoulder to the crestal bone level of 1.1 mm at first follow-up time point (3 to 6 months after insertion), 1.732 mm at 1 year, 1.738 mm at THE JOURNAL OF PROSTHETIC DENTISTRY
2 years, and 1.964 mm at 3 years. A significant correlation was found between bone loss values at all follow-up time points. A positive correlation was obtained with highstrength correlation coefficient R (R>0.7) at all follow-up time points (Table 4). The repeated-measures test identified a significant change in bone loss values throughout the study period. The bone loss rate was most notable in the first period (3 to 6 months after implant insertion), while it decreased at the follow-up time points of 1 year, 2 years, and 3 years (F=16.85, P<.01) (Fig. 4). The Pearson test showed a statistically significant correlation between PTVs at placement and bone loss values at all follow-up time points. A similar result was found in the PTVs at follow-up (Table 5). The independent samples t test identified no significant difference between the maxilla and the mandible or between the anterior and the posterior areas in terms of PTVs and the amount of bone loss. Patient age, sex, and health status did not have a significant impact on the PTVs or on bone loss values during the follow-up time points. DISCUSSION In this study, Periotest values at implant placement, as well as at the follow-up time point of 3 to 6 months later, were significantly correlated with bone loss values at all follow-up time points, which is a prognostic indicator in determining implant success. The results of this study Khalaila et al
-
2019
5
Table 4. Pearson correlations between bone loss values Bone Loss
1-y Follow-up Bone Loss
2-y Follow-up Bone Loss
3-y Follow-up Bone Loss
Pearson correlation
.817*
.709*
.881*
P (2-tailed)
.000
.001
.000
33
13
13
d
.992*
.982*
.000
.000
33
33
d
.997*
Follow-up
N 1-y follow-up Pearson correlation P (2-tailed) N 2-y follow-up Pearson correlation
d
P (2-tailed)
.000
N
33
Estimated Marginal Means
*P<.01.
2.50
Table 5. Pearson correlations between PTV and bone loss values PTV
2.00
1-y Follow-up 2-y Follow-up 3-y Follow-up Bone Loss Bone Loss Bone Loss
Placement
1.50 1.00
Pearson correlation
.381*
.556**
.614**
.791**
P (2-tailed)
.015
.001
.009
.002
40
33
33
33
Pearson correlation
.343*
.409*
.600*
.834**
P (2-tailed)
.03
.02
.011
.001
N
40
33
33
33
N Follow-up
0.50 0.00
Follow-up Bone Loss
Placement Follow up
1
2
3
Time (y) Figure 4. Repeated-measures test for estimated bone loss (mm).
confirm the research hypothesis that a significant correlation exists between PTVs and bone loss. In clinical practice, long-term follow-up assessments of implants are essential because changes in implant stability and bone levels are expected after the initial osseointegration of implants; for example, bone remodeling is accomplished mainly after 1 year.3 As the clinical success of implants depends on initial and ongoing stability after implant insertion, the development of a noninvasive method that provides an assessment of implant stability and possible prognostic information about future stability and bone loss is of benefit to clinicians. Resonance analysis instruments such as Osstell have been reported to provide an objective assessment of implant stability.8,9 The main drawback of RFA devices is that they can be used only in the early stages of implant insertion when the implant is not attached to the definitive restoration. In the present study, the use of the Periotest device allowed the evaluation of implant stability after the definitive restoration was attached. The mean PTV recorded at implant placement was −0.1605, which was consistent with the mean PTV of −0.27 reported
Khalaila et al
*P<.05 and **P<.01.
by Adell et al.16 A significant reduction in implant stability was found at the 3- to 6-month follow-up, which was then followed by a significant increase in stability at the 1-year follow-up. The dynamic changes in stability (as measured by PTVs) can be explained by the transition from the primary mechanical stability provided by the implant design to the biological stability provided by the newly formed bone as osseointegration occurs, which takes place during early wound healing.25 Additionally, the significant correlations between PTVs between each follow-up time point confirm findings from past studies showing that the Periotest is a reliable clinical tool for evaluating implant stability.24 The study findings also demonstrated that PTVs stabilized after the 1-year after-restoration time point, which significantly correlates with PTVs recorded at all other follow-up time points.24,26-28 One of the limitations of the Periotest device is its ability to measure only in the facial-lingual direction. The thin labial or buccal bone plate may impair the measurement results. A study that compared different implant diameters (3.7, 4.2, 6.0 mm) and the surrounding bone volume reported that only the 6.0-mm-diameter
THE JOURNAL OF PROSTHETIC DENTISTRY
6
Volume
implant had any validity on stress exerted on the surrounding bone.29 This type of implant was not used in this study. In addition to implant stability, peri-implant marginal bone loss is an essential treatment outcome measure. Bone loss measurement has been reported to be a reliable indicator of bone response to the surgical procedure and subsequent occlusal loading.14,15 In this study, the greatest amount of peri-implant bone loss was noticed between the time point of implant insertion and 3 to 6 months later, with an average loss 1.1 mm. This can be explained by bone remodeling, which starts immediately after implant insertion and represents the phase of active bone change. The mean bone loss values recorded in this study were greater than those in previous studies.20-22,30,31 This may be related to differences in measurement and statistical methods, implant macrostructure design, surgical technique, or random variability. There are some limitations in this study including sample size and measuring only implants inserted in healed bone. Further studies assessing long-time implant stability in grafted bone and in immediate implant placement are needed.
10. 11. 12. 13. 14. 15. 16. 17.
18. 19. 20.
21.
CONCLUSIONS Based on the findings of this clinical study, the following conclusions were drawn:
22. 23.
1. The Periotest device provided a reliable assessment of implant stability and predictive information about marginal bone level changes around an implant. 2. PTVs may be useful as a predictive tool for assessing long-term implant success, as well as serving as a surrogate marker for bone loss. REFERENCES
24. 25. 26. 27. 28.
1. Ivanoff CJ, Sennerby L, Lekholm U. Influence of initial implant mobility on the integration of titanium implants. An experimental study in rabbits. Clin Oral Implants Res 1996;7:120-7. 2. de Souza JG, Neto AR, Filho GS, Dalago HR, de Souza Junior JM, Bianchini MA. Impact of local and systemic factors on additional peri-implant bone loss. Quintessence Int 2013;44:415-24. 3. Molly L. Bone density and primary stability in implant therapy. Clin Oral Implants Res 2006;17 Suppl 2:124-35. 4. Huang HM, Pan LC, Lee SY, Chiu CL, Fan KH, Ho KN. Assessing the implant/bone interface by using natural frequency analysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000;90:285-91. 5. Boronat-Lopez A, Penarrocha-Diago M, Martinez-Cortissoz O, MinguezMartinez I. Resonance frequency analysis after the placement of 133 dental implants. Med Oral Patol Oral Cir Bucal 2006;11:E272-6. 6. Sullivan DY, Sherwood RL, Collins TA, Krogh PH. The reverse-torque test: a clinical report. Int J Oral Maxillofac Implants 1996;11:179-85. 7. 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;14:437-43. 8. Meredith N, Book K, Friberg B, Jemt T, Sennerby L. Resonance frequency measurements of implant stability in vivo. A cross-sectional and longitudinal study of resonance frequency measurements on implants in the edentulous and partially dentate maxilla. Clin Oral Implants Res 1997;8:226-33. 9. Herrero-Climent M, Albertini M, Rios-Santos J-V, Lázaro-Calvo P, Fernández-Palacín A, Bullon P. Resonance frequency analysis-reliability in
THE JOURNAL OF PROSTHETIC DENTISTRY
29. 30.
31.
-
Issue
-
third generation instruments: Osstell mentor®. Med Oral Patol Oral Cir Bucal 2012;17:e801-6. 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;21:255-61. Schulte W, Lukas D. Periotest to monitor osseointegration and to check the occlusion in oral implantology. J Oral Implantol 1993;19:23-32. Schulte W, Lukas D, Erenst E. Periotest values and tooth mobility in periodontal disease. Quintessence Int 1990;21:289-93. 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. Ma S, Payne AG. Marginal bone loss with mandibular two-implant overdentures using different loading protocols: a systematic literature review. Int J Prosthodont 2010;23:117-26. Ormianer Z, Matalon S, Block J, Kohen J. Dental implant thread design and the consequences on long-term marginal bone loss. Implant Dent 2016;25: 471-7. Adell R, Lekholm U, Rockler B, Branemark PI. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Oral Surg 1981;10:387-416. Krebs M, Schmenger K, Neumann K, Weigl P, Moser W, Nentwig GH. Long-term evaluation of ANKYLOS(R) dental implants, part i: 20-year life table analysis of a longitudinal study of more than 12,500 implants. Clin Implant Dent Relat Res 2015;17 Suppl 1:e275-86. Vazquez Alvarez R, Perez Sayans M, Gayoso Diz P, Garcia Garcia A. Factors affecting peri-implant bone loss: a post-five-year retrospective study. Clin Oral Implants Res 2015;26:1006-14. Cassetta M, Pranno N, Calasso S, Di Mambro A, Giansanti M. Early periimplant bone loss: a prospective cohort study. Int J Oral Maxillofac Surg 2015;44:1138-45. cepanovic M, Todorovic A, Markovic A, Patrnogic V, Milicic B, Moufti AM, S et al. Immediately loaded mini dental implants as overdenture retainers: 1-Year cohort study of implant stability and peri-implant marginal bone level. Ann Anat 2014;199:85-91. Flichy-Fernández AJ, Ata-Ali J, Palma-Carrio C, Peñarrocha-Oltra D, Conejero J, Peñarrocha J. Radiological assessment of peri-implant bone loss: a 12-month retrospective study. J Clin Exp Dent 2011;3:e430-4. Pikner SS, Grondahl K, Jemt T, Friberg B. Marginal bone loss at implants: a retrospective, long-term follow-up of turned Branemark System implants. Clin Implant Dent Relat Res 2009;11:11-23. Wagenberg B, Froum SJ. Long-term bone stability around 312 roughsurfaced immediately placed implants with 2-12-year follow-up. Clin Implant Dent Relat Res 2015;17:658-66. Aparicio C. The use of the Periotest value as the initial success criteria of an implant: 8-year report. Int J Periodontics Restorative Dent 1997;17: 150-61. Raghavendra S, Wood MC, Taylor TD. Early wound healing around endosseous implants: a review of the literature. Int J Oral Maxillofac Implants 2005;20:425-31. Berthold C, Holst S, Schmitt J, Goellner M, Petschelt A. An evaluation of the Periotest method as a tool for monitoring tooth mobility in dental traumatology. Dent Traumatol 2010;26:120-8. Meredith N. Assessment of implant stability as a prognostic determinant. Int J Prosthodont 1998;11:491-501. Noguerol B, Munoz R, Mesa F, de Dios Luna J, O’Valle F. Early implant failure. Prognostic capacity of Periotest: retrospective study of a large sample. Clin Oral Implants Res 2006;17:459-64. Ormianer Z, Patli A, Demiralp B, Heller G, Lewinstrin I, Khayat P. Implant supported first molar restoration: correlation of finite element analysis with clinical outcomes. Int J Oral Maxillofac Implants 2012;27:e1-12. Mangano C, Mangano F, Piattelli A, Iezzi G, Mangano A, La Colla L. Prospective clinical evaluation of 1920 Morse taper connection implants: results after 4 years of functional loading. Clin Oral Implants Res 2009;20: 254-61. Bratu E, Chan HL, Mihali S, Karancsi O, Bratu DC, Fu JH, et al. Implant survival rate and marginal bone loss of 6-mm short implants: a 2-year clinical report. Int J Oral Maxillofac Implants 2014;29:1425-8.
Corresponding author: Dr Zeev Ormianer Department of Oral Rehabilitation School of Dental Medicine Tel Aviv University Ramat Aviv, Tel Aviv 69978 ISRAEL Email: [email protected] Copyright © 2019 by the Editorial Council for The Journal of Prosthetic Dentistry. https://doi.org/10.1016/j.prosdent.2019.08.023
Khalaila et al