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Article history: Objective. The lack of a PDL, which acts as an energy absorber, is a contributor to implants’
Received 17 November 2019 early failure; however, these discrepancies are not well understood because of limited in vivo
Received in revised form research. This study investigated the discrepancy in biomechanical behaviors between nat-
17 December 2020 ural teeth and dental implants by detecting micro-movements in vivo.
Accepted 18 January 2021 Methods. We designed a device that could measure precisely mechanical behaviors such as
creep, stress relaxation, and hysteresis by using load–control displacement on teeth and
implants. We also compared energy dissipation between natural teeth and dental implants
Keywords: by subtracting the area of the hysteresis loop of natural teeth from that of dental implants.
Biomechanics Results. Biphasic curves with an initial phase of rapid response and a subsequent phase of
Natural teeth slow response were confirmed in creep and stress relaxation curves for the load–time rela-
Dental implants tionship in natural teeth. By contrast, the behavior of creep or stress relaxation was less
Periodontal ligament prominent when the dental implants were tested. We observed that the periodontal liga-
Creep ment under an axial intrusive load of 300 g in a loading rate 3 g/s could dissipate the energy of
Stress relaxation 7.35 ± 1.18 × 10−2 mJ, approximately 50 times that of the dental implants (1.47 ± 1.22 × 10−3 )
Hysteresis with statistically significant (p < 0.05).
Energy dissipation Significance. We confirmed natural teeth could achieve greater energy dissipation compared
to dental implants, which owe to that natural teeth exhibited fluid and viscoelastic proper-
ties.
© 2021 The Academy of Dental Materials. Published by Elsevier Inc. All rights reserved.
∗
Corresponding author at: School of Dentistry, National Taiwan University and National Taiwan University Hospital, No. 1 Chang-Te
Street, Taipei 10048, Taiwan.
E-mail address: chunpinlin@gmail.com (C.-P. Lin).
https://doi.org/10.1016/j.dental.2021.01.003
0109-5641/© 2021 The Academy of Dental Materials. Published by Elsevier Inc. All rights reserved.
d e n t a l m a t e r i a l s 3 7 ( 2 0 2 1 ) 682–689 683
and in vivo studies have verified the importance of fluid in and research methods. The aim of the study is to design a
tissues, pressure in blood vessels, elastic behavior of the alve- sensitive device to deliver controlled loads and detect dis-
olar bone, and viscoelastic properties of connective tissue to placement changes under different loads on teeth or implants,
the periodontal support mechanism. Both loads on teeth and then confirmed the hypothesis concerning obvious differ-
the displacement of teeth in the human jaw were recorded ences that exist in biomechanical behaviors between natural
by using experimental devices [1]. A manual intrusive load teeth and implants. This device can be therefore used to
was applied gradually to increase the force at various rates understand and compare the in vivo PDL behaviors of natu-
until the expected peak force was reached. After the force was ral teeth and implants, including creep, stress relaxation, and
relieved, the teeth returned to their baseline position in two area of the hysteresis loop.
phases. In the first phase, the teeth rapidly returned toward
their baseline position almost linear with time for nearly the
same amount of time it took to reach the peak force. The sec- 2. Experimental section
ond recovery phase was slower, with displacement and time
exhibiting a logarithmic relationship [1]. This study’s primary aim was to design and manufacture a
Picton expanded on Parfitt’s research and published his new device to measure slight microscale displacements of
results for human teeth by detecting subsequent tooth move- teeth and implants in vivo. When fixed to the lower dentition
ment of the first premolars of the upper jaw while chewing of a beagle, the developed device applies an axial intrusive
with the first molars of the lower jaw [2,3]. Their load–tooth force to a single tooth or an implant while recording the con-
displacement curve for tooth displacement was similar to the current forces and displacement to determine the mechanical
findings in Parfitt’s study. However, the relationship between behavior difference between nature tooth and dental implant.
intrusive force and displacement is not just a logarithmic
relationship. Picton also investigates the axial mobility and 2.1. The architecture of the intraoral detection device
changes in rest position over 3-h periods—all displayed reduc-
tions in mobility when no loads were applied. The consistent The intraoral device consists of load and displacement sen-
finding of substantial reductions in mobility with or without sor components (Fig. 1). The axial load was provided by a
extrusion accounts for changes in blood vessels, biophysical small stepper motor (model, PK513PA-H100S) with a precision
properties, and ground substance. The results of early exper- measuring screw (model, M148-104-13) capable of applying a
iments revealed a nonlinear relationship between intrusive uniaxial variable force to achieve displacement control. The
force and tooth movement, which indicated that the periodon- force was measured using a miniature cantilever force sensor
tal membrane might have viscoelastic properties [4]. Wills (model, UH-40N; resolution, 0.01N load cell). Signal acquisi-
et al. analyzed displacement-time curves following stress tion was achieved using a static/dynamic stress measurement
relaxation in monkeys [5]. They analyzed displacement–time and data acquisition system (model, LS-1020-16B/LS-AI-16-4;
curves associated with the instantaneous removal of axial force display accuracy, 0.05N; displacement display accuracy,
intrusive loads on incisors. They proposed that the three 0.5 m) for force and displacement measurement for fur-
stages of dental recovery can be understood using an expo- ther signal processing. Moreover, a dedicated signal controller
nential curve fitting technique. Initially, a simple short-term (model, LS-A0-12-4) was employed as a feedback control force
recoil of tissues and return of blood takes place over 1 or 2 min. to confirm the requisite displacement control.
Subsequently, in the medium-term following a series of load- Two linear variable differential transformers (LVDTs;
ings, there is a passive recovery of the tooth position. It may be model, TF101F; resolution, 0.06 m) were used to measure dis-
due to the re-polymerization of the ground substance. Finally, placement. LVDT1 was placed on either a targeted natural
in the longer-term (over a few hours), there is a considerable tooth or an implant, and LVDT2 was placed on another natural
biochemical turnover of the components of the collagen fiber tooth as a control reference.
meshwork. This turnover, particularly the changes in the fluid An autopolymerized acrylic appliance that covered the
content, would also have a controlling effect on the position of occlusal surfaces of the dentition was fabricated for each bea-
the tooth within its socket. However, understanding how these gle. This occlusal appliance was cemented with the measuring
different systems interact to support the teeth is still a chal- device to the dentition. A natural tooth was selected from
lenging task. Because the current hypothesis does not provide the first lateral incisors on one side of the mandible to serve
a complete description of the role played by the PDL in chew- as the target tooth. A dental implant ( 3.3 mm Straumann,
ing, tooth growth, and tooth movement, future research on Basel, Switzerland) was inserted and allowed to heal for three
the periodontal mechanism should integrate mathematical, months on the contralateral side of the mandible. An adja-
biological, and mechanical perspectives and offer a complete cent central incisor served as the reference tooth to reduce
description of the PDL mechanism. the long arm’s influence of deformity during the detection of
Implants have been widely used for more than 50 years and micromovement.
engineered for osteointegration, leading to their success and In order to determine the effect of the PDL on the displace-
wide acceptance among patients. However, bone loss due to ment of the target tooth during loading, a reference tooth was
stress concentration leads to mechanical failure in the long used as a baseline to calculate the discrepancy between the
term. This problem may result from differences in the biome- target tooth and reference tooth. The device was fixed to the
chanical behaviors of natural teeth and dental implants. appliance, which was mounted on a tooth other than the tar-
Differences in biomechanics between natural teeth and get tooth (or implant) or the reference tooth. The loading rod
implants have rarely been compared due to a lack of devices was placed on the edge of the target tooth. The two sensors
684 d e n t a l m a t e r i a l s 3 7 ( 2 0 2 1 ) 682–689
Fig. 1 – Overview of the new load–displacement measurement device for natural teeth and implants. (a)The device was
secured in an acrylic appliance cemented on teeth, and (b) The device setup for detection on a natural tooth or an implant in
a beagle, and (c) The beam is actuated by a stepper motor to apply a vertical load on a tooth or implant. Two LVDTs are used
to measure the displacement of a tooth (or an implant), one for the target tooth (or implant) and another as a reference. The
precise displacement of the object tooth is indexed by subtracting the reference from the object.
were adjusted such that one of the sensors rested gently on which was maintained at a constant load, and displacement
the surface of the loading rod, and the other touched the ref- recorded for up to 120 s.
erence tooth without imposing any stress on the tooth. The
discrepancy between the target tooth (or implant) and the 2.4. Stress relaxation test
reference tooth was equivalent to the axial displacement of
LVDT1 and LVDT2, and the actual displacement of the tar- The amount of received force was observed by maintaining a
get tooth while loading was thus determined. Beagles (N = 3) stable amount of displacement for a specific period. We set
with the target tooth on one side and the implant on the other the displacement rate as 1.5 m/s until the intrusive axial dis-
side were used in this study. All experimental procedures were placement of 40 m was met and held in the position for 120 s.
approved by the Institutional Animal Care and Use Commit- The experiment was also performed to maintain the intru-
tee (IACUC NO. 20100147) of the Medical College of National sive axial displacement of 60 or 80 m for 120 to ascertain the
Taiwan University. This study conforms to ARRIVE (Animal force–time relationship. Three measurements were made on
Research: Reporting of in vivo Experiments) guidelines (please each tooth/implant to confirm.
see Supplemental Information).
2.5. Hysteresis loop and energy dissipation
2.2. Determining the displacement–load relationship We set the loading rate as 3 g/s and the non-loading dis-
between natural teeth and dental implants placement rate as 1.5 m/s for the hysteresis tests. Using the
load–displacement relationship, we assessed the hysteresis
The displacement of natural teeth under an axial force is loop and calculated the energy dissipation by using Microsoft
approximately 200 m [6]. Our device owns the load resolution Excel (Microsoft Excel 2016, Microsoft Inc, USA). The analysis
of 0.05 N and displacement resolution of 0.5 m. The variation results for variables are presented as the mean and standard
in the displacement of natural teeth approximately within ten deviation (mean ± SD). Differences in the measured properties
m, in contrast to that of implants, which is negligible, indi- among the groups were evaluated using a one-way analysis of
cating that the displacement-measuring device can provide variance with 95% confidence intervals. A p value of less than
an adequate measurement at the micrometer level. .05 indicated statistical significance.
The creep test was conducted to measure the displacement 3.1. Creep test results of natural teeth
of the dog’s natural teeth under different axial loads (100, 200,
300, and 500 g). The force was gradually increased at a con- In the creep test, a constant force was maintained for 120 s
stant incremental rate (3 g/s) until it reached an assumed load, so that the behavior of the object being measured could be
d e n t a l m a t e r i a l s 3 7 ( 2 0 2 1 ) 682–689 685
Fig. 2 – Detection of the biomechanical properties of natural beagle teeth. (a) Displacement–time relationship of natural dog
teeth in the creep test, (b) load–time curves of the stress relaxation test, and (c) load–displacement relationship of natural
dog teeth in the hysteresis test, and (d) energy dissipation of natural teeth in the hysteresis test. (For interpretation of the
references to colour in the text, the reader is referred to the web version of this article).
observed. Fig. 2a presents the displacement–time relationship displacement was maintained at 60 m for 45 s following max-
under four force conditions (100, 200, 300, and 500 g), indi- imum loading, the condition of the stress relaxation curve
cating that the final displacement values gradually increased presented as a steep relaxation phase with a rapid logarith-
with force. The displacement–time diagram clearly shows the mic decline(y = −23.95ln(x) + 147.62) and a flat relaxation phase
creep phenomenon in a natural dog tooth. We determined with a slow logarithmic decline (y = −15.72ln(x) + 112.97) When
the relationship between the displacement and time under the displacement was maintained at 80 m for 60 s following
a controlled load. When the load was up to 100 g, the dis- maximum loading, the stress relaxation was observed as a
placement was always 75 microns, regardless of the final curve with a steep relaxation phase and a rapid logarithmic
load value. In this test, when the load reached 100 g, the dis- decline y = −33.51ln(x) + 227.38 (−33.51) and a flat relaxation
placement remained at approximately 75 m regardless of the phase with a slow logarithmic decline y = −19.96ln(x) + 160.84
load–control displacement, whether it was at 100, 200, 300, (−19.96). The force-time diagram clearly shows the stress
or 500 g. All curves for the load–time relationship showed an relaxation phenomenon in a natural dog tooth.s
initial phase with a steep slope, followed by a gradual plateau.
3.3. Hysteresis loop of natural teeth
3.2. Stress relaxation of natural teeth
The load–displacement relationship of natural dog teeth in the
In the stress relaxation test, a fixed displacement was main- hysteresis test is shown in Fig. 2c. The results suggested that
tained for 120 s so that the behavior of the object being as the applied load increased, the inner area of the hystere-
measured could be observed. Fig. 2b illustrates the force–time sis loop increased, signifying greater energy absorption by the
relationship under three displacement conditions. After var- PDL under a heavier load. The energy dissipation of the natu-
ious fixed displacement values (40, 60, and 80 m) were ral teeth in the hysteresis test is shown in Fig. 2d. The energy
maintained for 120 s each time, the force gradually decreased dissipation levels of the natural dog teeth at 100, 200, 300, and
with an increase in the time. The blue curve showed stress 500 g were 1.97 × 10−2 , 4.52 × 10−2 , 7.35 × 10−2 , and 13.94 × 10−2
relaxation when the natural tooth displacement was main- mJ, respectively. The increase in energy absorbed with load is
tained at 40 m. In the beginning, the rate of relaxation to be expected.
under a load was higher; subsequently, the rate of relax-
ation decreased gradually. Under load application wherein the 3.4. Creep of dental implants
displacement was maintained at 40 m for 30 s following max-
imum loading, the condition of the stress relaxation curve The effect of load on the displacement–time relationship in
presented as a steep relaxation phase with a rapid logarith- the creep test is presented in Fig. 3a. In general, the dis-
mic decline (y = −7.85ln(x) + 49.05)) and a flat relaxation phase placement of the implant was less than 10 m. Hence, a
with a slow logarithmic decline (y = −5.120ln(x) + 37.97). A sim- sawtooth wave is evident in these displacement-time curves,
ilar graph pattern was observed when the displacement was which was considered to be the device’s inherent noise, which
maintained at 60 and 80 m under load control. When the can be determined by making measurements on non-loaded
686 d e n t a l m a t e r i a l s 3 7 ( 2 0 2 1 ) 682–689
Fig. 3 – Detection of the biomechanical properties of dental implants in beagles. (a) Displacement–time curves of the creep
test, (b) load–time curves of the stress relaxation test, (c) load–displacement curves of the hysteresis test, and (d) energy
dissipation of dental implants in the hysteresis test. (For interpretation of the references to colour in the text, the reader is
referred to the web version of this article).
objects. We determined the relationship between force and 3.7. The discrepancy in biomechanics between natural
displacement under different loads applied for more than teeth and dental implants
160 s. When the load was up to 100 g, the displacement
was always 75 microns, regardless of the final load value. Fig. 4a shows the relationship between stress and displace-
All displacement–time relationship curves showed an initial ment for implants and natural teeth with the loading rate
phase involving a steep slope, followed by a subsequent phase as 3 g/s in the creep test. Although, presumably, not all the
involving a shallow slope. Some displacement peaks at 30−40 s displacement of natural teeth was due to creep, some could
may be caused by involuntary movements of the dogs, such as be due to the PDL’s nonlinear elastic response. The implants
breathing. exhibited almost no creep with a displacement of approxi-
mately four m under a load of 100 g. However, the natural
teeth exhibited creep and displacement of approximately
3.5. Stress relaxation of dental implants 60 m under a load of 100 g. When a force of 200 g was applied,
the observed implant displacement was approximately 5 m,
In Fig. 3b, the blue curve shows stress relaxation when the whereas the observed natural tooth displacement was approx-
natural tooth displacement was maintained at 8 m. Once the imately 86 m. When a force of 500 g was applied, the observed
controlled displacement reached 8 m, the rate of relaxation implant displacement was approximately 13 m, whereas
decreased marginally. Similar stress relaxation curves were the observed natural tooth displacement was approximately
also noted when the load control displacement increased to 127 m. The force–displacement relationship followed a lin-
and maintained at 9 and 10 m. ear equation for the implants and a quadratic equation for
the natural teeth. Fig. 4b shows the energy dissipation for the
natural teeth and implants in the hysteresis test. After energy
conversion, the energy dissipation of the hysteresis loop under
3.6. Hysteresis loop of dental implants a load of 100 g was 1.97 ± 1.05 × 10−2 mJ for the natural teeth
and 8.2 ± 7.52 × 10−4 mJ for the implants with statically signif-
The load–displacement relationship of the implants in the icant difference (p = 0.011). Under a load of 200 g, the energy
hysteresis test is shown in Fig. 3c. The results suggest that dissipation of the hysteresis loop was 4.52 ± 0.92 × 10−2 mJ for
as the applied load increased, the inner area of the hys- the natural teeth and 1.34 ± 0.93 × 10−3 mJ for the implants
teresis loop increased, indicating greater energy absorption. with statically significant difference (p = 0.023). The hys-
The energy dissipation of implants in the hysteresis test was teresis loop’s energy dissipation under a load of 300 g was
considerably lower because of limited viscoelastic displace- 7.35 ± 1.18 × 10−2 for the natural teeth and 1.47 ± 1.22 × 10−3
ment, as illustrated in Fig. 3d. The energy dissipation levels mJ for the implants with statically significant difference
of the natural dog teeth at 100, 200, and 300 g were 8.2 × 10−4 , (p = 0.036).
1.34 × 10−3 , and 1.47 × 10−3 mJ, respectively.
d e n t a l m a t e r i a l s 3 7 ( 2 0 2 1 ) 682–689 687
Fig. 4 – The discrepancy in biomechanics between natural teeth and dental implants. (a) Load–displacement curves of
natural teeth and implants. The load was increased from 0 to 500 g. (b) Energy dissipation of natural teeth and implants
during the hysteresis test.
ation also occurred within 2 min of our relaxation time. Dorow and hysteresis, occurred in natural teeth and dental implants.
and Komatsu et al. have performed stress relaxation experi- However, the degree of such phenomena was determined to
ments using PDL and alveolar bone specimens of rabbit teeth; be considerably lower for a dental implant than that of a nat-
the relationship between stress relaxation and time revealed ural tooth. And our findings support that PDL can absorb the
three exponential decay terms. Their findings indicated that energy impact on the tooth through the energy dissipation of
the PDL’s relaxation reaction might require several minutes the periodontium’s viscoelastic property.
to more than an hour to reach equilibrium [9,10]. However, In clinical practice, long-term implant prosthodontic fail-
their experiments involved an in vitro specimen composed of ure may be due to mechanical complications; improper
teeth, the alveolar bone, and the PDL; therefore, their results loading design leads to bone resorption, peri-implantitis, or
cannot represent the entire mechanical behavior of the PDL. implant fracture. A dental implant in the clinical application
Similar in vitro results have been obtained in a human study usually considers a light occlusal contact scheme with its den-
[11], a mouse study [12], and pig studies [13,14]. The aforemen- tal antagonists. Be cautious of the dental implant’s mechanical
tioned in vitro experiments could reveal only a small part of failure was emphasized since it has small energy dissipation
the PDL behavior. The contribution of fiber, liquid, blood, and than a natural tooth. Improving energy dissipation in dental
overall PDL composition remains unclear. No in vivo study has implants while chewing is a necessary feature in the design
been conducted on tooth stress relaxation, and our study is the of future implants. Many authors have attempted to develop
first to identify the stress relaxation phenomenon in a bea- such implants, but they may require original or biomechanical
gle tooth model. When the teeth were released from the load, parameters as a reference for abutment fixtures to mimic the
they gradually and slowly returned to their original positions. biomechanical behavior of natural teeth. The role of the PDL in
The hysteresis analysis results indicate that the relationships biomechanics has always been a subject of considerable con-
between load and displacement during the tooth depression cern in the literature. Our method and device may be adapted
and recovery phases were considerably different. The energy and expanded for humans to establish a database of parame-
dissipation in the area could be calculated between the initial ters related to the mechanics of the PDL; such a database can
and return phases. be applied in finite element analysis for dental and implant-
In this study, we used the aforementioned device to exam- related research. Our method provides an easy approach to
ine natural teeth and dental implants. Fig. 4 shows the determine the load and displacement of a natural tooth. This
discrepancy in biomechanics between the natural teeth and method can be used to determine parameters for further finite
dental implants, demonstrating that as the applied force element construction.
increased, the inner area of the hysteresis loop increased,
consequently signifying an increase in the energy absorbed
5. Conclusions
by the PDL. Based on the findings of the creep test for the
natural teeth, as the applied load increased, the resulting
We successfully designed and constructed a precise and
creep increased; however, no significant creep was found
sensitive device that could detect natural teeth and den-
in the dental implants. The near-complete lack of creep
tal implants’ micromovement under different loads. We
performance limits energy dissipation in resorbing force or
confirmed that natural teeth’ periodontium possesses the
impact on implants during mastication. In the stress relax-
viscoelastic properties of creep, stress relaxation, and hys-
ation test, two relaxation phases in the natural dog teeth
teresis, thus achieving greater energy dissipation than dental
were noted, suggesting that the PDL of a natural tooth serves
implants.
as a stress absorber. However, this phenomenon was not
observed in dental implants. We found that the periodon-
tium under an axial load of 300 g could dissipate the energy of Author contributions
7.35 ± 1.18 × 10−2 mJ, approximately 50 times that of the dental
implants (1.47 ± 1.22 × 10-3 ). Hysteresis is used to describe the The manuscript was written through the contributions of all
stress–strain relationship during delayed or drawn-out recov- authors. All authors have given approval to the final version
ery. The hysteresis curve represents the behavior of the PDL of the manuscript.
during stress load and the release of an external force. The Study conception and design: Hao-Hueng Chang, Shang-
hysteresis loop can be used to indicate the PDL uptake and Jye Tsai, Chun-Pin Lin.
the release of required energy. When a tooth is subjected to Acquisition of data: Yin-Lin Wang, Yi-Chao Huang, Shang-
an external force, the PDL can quickly absorb and then release Jye Tsai, Yu-Ting Li, Ju-Hsuan Yang.
stored strain energy gradually based on the PDL’s viscoelas- Analysis and interpretation of data: Hao-Hueng Chang,
tic properties. If strain energy is not released, then excessive Chun-Liang Yeh.
strain energy may cause the breakage of surrounding tissues Drafting of the manuscript: Hao-Hueng Chang, Chun-Liang
[13–16]. Our experimental results reveal that the hysteresis of Yeh.
the PDL was substantially larger than that of the implants.
Occlusal loading on a natural tooth may be absorbed
or transmitted to surrounding alveolar bone by periodon- Acknowledgements
tium, owing to energy dissipation. This study describes an
innovative design and a practical method in comparing the The authors gratefully acknowledge the grant supports
biomechanical behaviors of a tooth and an implant in vivo. from the National Taiwan University Hospital (107CGN09 &
Biomechanical phenomena, including creep, stress relaxation, 109CGN07).
d e n t a l m a t e r i a l s 3 7 ( 2 0 2 1 ) 682–689 689