Archives of Oral Biology 83 (2017) 327–333

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Archives of Oral Biology

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Research Paper

Human pulpal blood flow in different root formation stages measured with MARK
transmitted-light plethysmography
⁎
Khongorzul Ganbolda, Satoko Kakinoa, , Hideharu Ikedab, Michiyo Miyashina
a
Department of Pediatric Dentistry, Division of Oral Health Science, Graduate School, Tokyo Medical and Dental University, Japan
b
Department of Pulp Biology, Division of Oral Health Science, Graduate School, Tokyo Medical and Dental University, Japan

A R T I C L E I N F O A B S T R A C T

Keywords: Objectives: To determine the pulp vitality after traumatic injury, dentists often use pulp sensitivity tests, which
Pulp vitality test can be ambiguous in young permanent teeth with incomplete root formation. Transmitted-light plethysmo-
Root formation stages graphy (TLP) is a non-invasive objective method that uses a 525-nm LED to detect blood volume change in the
Young permanent teeth pulp. The present study aimed (1) to investigate pulpal blood flow with TLP and optical characteristics in healthy
Transmitted-light plethysmography (TLP)
permanent maxillary incisors in different root formation stages, and (2) to assess the influences of body growth
Optical density
of the children and tooth color on the TLP amplitude.
Tooth colour
Design: Seventy-eight fully erupted maxillary central incisors were divided into four groups, according to the
root formation stages. Group 1: root with wide-open apex, Group 2: root completed in length with open apex,
Group 3: root with half-closed apex, Group 4: root with complete formation. The TLP amplitude, optical density,
electric pulp testing, and cervical tooth color measurements of each group were compared using a one-way
analysis of variance followed by the Bonferroni method. The correlation between the weights/heights of children
and TLP amplitudes was analyzed using Pearson coefficient.
Results: The TLP amplitude was significantly higher in Group 3 than in the other groups. The amplitude was
correlated with the weights/heights of children, but not with the tooth color. Optical density and electric sen-
sitivity increased with tooth maturation.
Conclusion: The amplitude of TLP and optical density may be affected by growth and development in children
and indicate changes in the vascular dynamics of the pulp and hard tissue maturation during root formation
stages.

1. Introduction Webber, & Walker, 1991).

Pulp vitality tests are essential for the proper treatment and favor-
able prognosis of patients with traumatized teeth. In order to evaluate
the pulp vitality, dentists often use sensitivity tests, such as electric and
thermal tests. However, pulp vitality testing based only on the neuronal
response is deficient, as this response greatly depends on a patient’s
subjective sensation (Ikeda & Suda, 1998). It may therefore not be sui-
table for diagnosing the developing teeth of children, due to possible
false negative results (Otawa, Fujii, Kubota, & Machida, 1986).
Transmitted-light plethysmography (TLP) is a non-invasive and
objective optical method that utilizes a single light-emitting diode
(LED) to detect blood volume changes in the dental pulp (Ikawa,
Horiuchi, & Ikawa, 1994; Kakino, Takagi, & Takatani, 2008; Schmitt,
It has been reported that the TLP signal is less likely to be con-
taminated by the blood circulation of surrounding tissues than laser
Doppler flowmetry (LDF) (Matthews, Ikawa, & Horiuchi, 1996). The
TLP amplitude has a significant negative correlation with age in chil-
dren, and the vital teeth had a significantly higher amplitude than the
non-vital teeth with no pulse signal (Miwa, Ikawa, Iijima,
Saito, & Takagi, 2002).
Our previous studies using an extracted tooth model have clarified
that dentin thickness, pulp chamber size, LED wavelength, and blood
concentration are substantial factors affecting the transmission of light
through the teeth, and that changes in both the TLP amplitude and
optical density (OD) are indicators of pulpal circulation (Kakino et al.,
2007, 2008). Furthermore, the clinical application of TLP to

Abbreviations: TLP, transmitted-light plethysmography; LED, light emitting diode; EPT, electric pulp test; LDF, laser doppler flowmetry; OD, optical density; AC, alternating current; DC,
direct current; PWV, pulse wave velocity; PTT, pulse transition time; CA, arterial compliance
⁎
Corresponding author at: Department of Pediatric Dentistry, Division of Oral Health Science, Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku,
Tokyo 113-8549, Japan.
E-mail address: satokopd.pedo@tmd.ac.jp (S. Kakino).

http://dx.doi.org/10.1016/j.archoralbio.2017.08.010
Received 23 May 2017; Received in revised form 30 July 2017; Accepted 20 August 2017
0003-9969/ © 2017 Elsevier Ltd. All rights reserved.
K. Ganbold et al.
traumatized teeth has shown that the TLP amplitude changes during the
follow-up period, depending on the prognosis of the trauma (Kakino,
2010).
Dental trauma often occurs in growing children. There have been
several studies on age-dependent changes in the pulpal blood supply
using various non-invasive methods (Ikawa, Komatsu, Ikawa,
Mayanagi, & Shimauchi, 2003; Komatsu, Ikawa, & Mayanagi, 2007;
Miwa et al., 2002; Stella et al., 2015). However, throughout the root
formation period, the pulpal chamber size vary in children of the same
age (Moorrees, Fanning, & Elizabeth, 1963). To our knowledge, there
are no clinical studies regarding pulpal blood supply changes in dif-
ferent root formation stages. In addition, discoloration often accom-
panies traumatized teeth. Although we were able to collect TLP pulse
wave signals from discolored traumatized teeth (Kakino, 2010), the
effects of tooth color on the TLP amplitude has not been studied yet.
Furthermore, the processes of growth and development of the whole
body vary from child to child, and the effects of these processes on the
TLP amplitude have not been documented either. Without proper un-
derstanding of the normal condition in healthy teeth, diagnosing trau-
matized teeth will be difficult.
Thus, the aims of the present study were (1) to investigate pulpal
blood flow with TLP and the optical characteristics in different root
formation stages in healthy permanent maxillary central incisors and
(2) to assess the influences of body growth of children and cervical
tooth color on the TLP amplitude.
2. Materials and methods
2.1. Subjects and selected teeth
This cross-sectional study was approved by the Ethics Committee of
the Graduate School of Tokyo Medical and Dental University (No. 914).
The subjects were 31 children aged 6–17 years who visited the pediatric
dental clinic of the Dental Hospital, Tokyo Medical and Dental
University, and 10 adult volunteers aged 25–36 years. Informed consent
was obtained after explaining the purpose and methodology of the
study to all participants and their guardians. The selection criteria for
teeth were healthy, fully erupted maxillary central incisors without
dental caries, restorations, periodontal disease, visible discoloration
and a history of trauma. Subjects with systemic diseases, a history of
orthodontic treatment and adults with smoking habits were excluded
from the study.
2.2. Group classification
Intraoral radiographs of the subjects’ teeth were taken to evaluate
the root formation stages. The teeth were divided into four groups
(G1–G4) according to their developmental stage (Fig. 1). The number of
subjects, teeth, and mean age in each group are shown in Table 1.
2.3. Measurement of TLP and OD
A TLP system with a 525 nm green LED (prototype system, J. Morita
Corp., Kyoto, Japan) was used to measure the pulpal blood flow of the
maxillary central incisors. Fig. 2 shows the experimental setup of the
present study. In the preceding pilot study we examined the effect of
opaque black rubber dam on the signal from surrounding tissues in
Group 4 teeth. There was no statistically significant difference between
measurements with and without a rubber dam. Therefore, all mea-
surements in the present study were done without any isolation. Prior
to measurement, a silicone impression was taken to make an individual
acrylic resin cap for each tooth. Two holes were made in the cap to hold
an LED (Ø 3 mm OSPG 3131 P, OptoSupply International) on the pa-
latal side of the tooth and a photodiode on the labial side. We used a
typical Si-PIN photodiode with specifications of spectral sensitivity of
450–1110 nm, and a peak wavelength of 920 nm (HPS 304AL,
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Archives of Oral Biology 83 (2017) 327–333
Kodenshi Corp., Tokyo, Japan). The sensitivity at 525 nm was around
0.23 A/W (Fig. 3). Each measurement lasted 90 s, while the subjects
were in the supine position, and finger plethysmogram was recorded
simultaneously to obtain the heartbeat signals. An amplified trans-
mitted light signal, i.e. TLP pulse waves (alternating current: AC) and
transmitted light intensity (direct current: DC), appeared on the oscil-
loscope connected to a TLP system. The average amplitude of 30 wa-
velengths was measured using a signal processing software program
(LabChart, AD Instruments Pty., Ltd., Australia). The ratio of the pul-
satile (AC) and non-pulsatile (DC) transmitted light intensities was
calculated as a percentage of the TLP amplitude as follows:
TLP amplitude (%) = 100 (AC (V)/DC (V))
For the OD measurement, the same light source LED and individual
acrylic resin cap were used to obtain transmitted light from the exact
same position as TLP measurement. A mini-spectrometer (model
C10082CA, SpecEvaluation software; Hamamatsu Photonics K.K,
Hamamatsu, Japan) was used to detect the incident and transmitted
light intensities. The OD of the teeth was calculated using the following
formula, where Io is the incident light and It is the transmitted light:
OD = ln (Io/It)
2.4. Tooth color measurements
A Crystaleye Spectrophotometer® (Olympus Corp., Tokyo, Japan)
was used to record the color of the cervical area on the labial surface.
Since the LED and photodetector were positioned approximately 3 mm
from the gingival margin, the color of the cervical area on the labial
surface was recorded. The CIELAB color scale was applied to obtain
L*a*b* parameter values, where L* is lightness (0 is black, 100 is pure
white), a* is red (+a*) to green (−a*) hue, and b* is yellow (+b*) to
blue (−b*) hue. A disposable mouth piece was used in each subject to
fix the tooth position, and the device was calibrated before each mea-
surement.
2.5. Electric pulp test (EPT)
A Sybron Endo vitality scanner ™ (model 2006; Sybron Endo Dental
Specialties, Glendora, CA, USA) was used for electric pulp vitality
testing. After the tooth had been isolated with cotton rolls and air dried,
the electrode was placed on the labial center of the enamel surface. EPT
values from 0 (no output) to 80 (maximum output) were recorded when
each subject could perceive any sensation.
2.6. Body weight and height measurements
The body weight and height of the children were measured on the
same day with optical measurements.
2.7. Statistical analyses
The comparisons of the TLP amplitude, OD values, EPT values, and
tooth color indicators (L*, a*, and b*) between Groups 1 to 4 were
analyzed using a one-way analysis of variance and the Bonferroni
method. The Pearson correlation coefficient was calculated between
tooth color, weight, height, and TLP amplitudes. P values less than
0.005 were considered statistically significant. All statistical analyses
were performed using the SPSS software program, version 23.0 (IBM
Corp., Armonk, NY, USA).
3. Results
Fig. 4 shows examples of tooth and finger plethysmograph record-
ings in each group as real-time monitoring. During the TLP
K. Ganbold et al. Archives of Oral Biology 83 (2017) 327–333

Fig. 1. Classification of the groups, regarding their root formation stages observed on the radiograph.
(a) Group 1. Half to three-quarters developed roots with a wide-open apex.
(b) Group 2. Root completed in length with open apex.
(c) Group 3. Completed root development, with half-closed apex.
(d) Group 4. Adult mature teeth with fully closed apex.

Table 1
Subjects and teeth of each group.

Subjects (N) Age (years) Teeth (n)

Group 1 N=8 7.7 ± 1.0 n = 16

Group 2 N = 13 10.6 ± 1.9 n = 25
Group 3 N = 10 14.2 ± 2.3 n = 18
Group 4 N = 10 30.4 ± 3.6 n = 19

Age: means ± standard deviations.

measurements, the tooth and finger plethysmogram showed synchro-

nized rhythmic activities. The TLP amplitude increased as the root
development stage progressed from Group 1 to 3, and Group 3 had the
highest amplitude at 0.102% ± 0.056%. Once the root matured, the
TLP amplitude showed a statistically significant decrease, with Group 4
showing the lowest value at 0.043% ± 0.027% (Fig. 5a).
OD values showed a similar pattern to TLP amplitude. During the Fig. 3. Spectral sensitivity characteristics of the photodiode.
root formation periods, the OD increased significantly, with the lowest
value (5.7 ± 0.7) in Group 1, and the highest value (7.1 ± 0.7) in EPT tests showed that the scores decreased as the root development
periods progressed. Group 1 had the highest value (50.3 ± 15.9) and
Group 3 (p < 0.005). The OD of Group 4 tended to be lower than that
of Group 3, albeit not to a significant degree (Fig. 5b). Group 4 the lowest value (21.3 ± 5.9) (Fig. 5c). There was a statisti-
cally significant difference between the groups (p < 0.005).

Fig. 2. Schematic drawing of the TLP system.

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K. Ganbold et al. Archives of Oral Biology 83 (2017) 327–333

Fig. 4. Examples of each group participant’s TLP amplitude observed on the oscilloscope during the measurement. (a) Group 1. (b) Group 2. (c) Group 3. (d) Group 4.

Fig. 5. The mean ± SD of the (a) TLP amplitude, (b) OD value, and (c) EPT value of each group. The ordinate represents the group, and the abscissa represents the respective
measurements. The asterisks indicate significant differences between the groups (* p < 0.005; ** p < 0.01).

The results of tooth color measurement showed an increase in the
values of L* and b* with tooth maturation. The L* and b* values in
Group 4 were significantly higher than those in Group 1 (p < 0.005)
(Fig. 6a, c). In contrast, the value of a* decreased significantly with the
progress of tooth development (Fig. 6b). Although the L*, a*, and b*
values varied during the root formation stages, there was no significant
correlation with the TLP amplitude. The Pearson’s correlation coeffi-
cients of L*, a*, and b* were −0.051, 0.197, and 0.147, respectively
(Fig. 6d–f).
There was a statistically significant correlation between the TLP

Fig. 6. The mean ± SD of the cervical area tooth color parameters during the root development stages and their correlation with the TLP amplitude. In graphs (a)–(c) the ordinate
represents the group, and the abscissa represents the respective measurements of the tooth color parameters (L*- lightness, a*- red hue, b*- yellow hue). The asterisks indicate significant
differences between the groups (* p < 0.005; ** p < 0.01).

330
K. Ganbold et al.
amplitude and body weights and heights of children (n = 59), with
Pearson’s correlation coefficient of 0.37 (p = 0.004) and 0.45
(p = 0.0004), respectively (Fig. 7).
4. Discussion
In this study, we first investigated the pulpal blood volume change
and factors possibly affecting tooth plethysmography in different stages
of root development in young permanent teeth.
4.1. TLP amplitude
Each root formation stage had a distinct TLP amplitude which in-
creased as tooth development progressed, and decreased after complete
maturation (Fig. 5a). Despite our expectations that Group 1 would have
the highest TLP amplitude due to the abundant blood vessels
(Kishi & Takahashi, 1990), Group 3 had the highest amplitude. Since
the TLP amplitude is influenced by multiple factors, we assume that the
changes among the stages in children could be induced by two aspects:
local pulpal factors and general body factors.
Regarding local pulpal factors, dental pulp has several ways of
maintaining homeostasis in the pulpal circulation (Ikeda & Suda, 2012).
One is neuronal regulation, which is controlled by sympathetic and
sensory nervous system. Sympathetic nerve terminals were found to be
in close association with smooth muscles in the walls of arterioles, but
not all vessels have these nerve terminals (Okamura et al., 1994; Pohto,
1972). In addition, newly erupted teeth have fewer nerve endings than
older teeth (Johnsen, Harshbarger, & Rymer, 1983). Therefore, we
speculate that immature neuronal regulation of arteriolar vasocon-
striction might be insufficient, and so the pulpal blood volume change
was not significant enough to induce higher TLP amplitudes.
Regarding general body factors, the TLP pulsation may be asso-
ciated with cardiovascular systemic changes in children. Studies using
photoplethysmography have shown an increase in the brachioradial
pulse wave velocity (PWV) and peripheral pulse transition timing (PTT)
with age and body growth in healthy children (Cheung, Brogan, Pilla,
Dillon, & Redington, 2002; Foo et al., 2005). Furthermore, Senzaki et al.
(2002) estimated the arterial compliance (CA) in subjects 6–20 years of
age and reported that CA increases mainly due to general growth in
arterial size. The pulp vessel distensibility and compliance changes are
uncertain, because the surrounding hard tissue makes it difficult to
perform measurements. However, the present results showed that the
pulsatile blood volume change could be measured, and the TLP am-
plitude increased with growth in children (Fig. 7). There have been no
reports regarding age-related cardiovascular systemic changes in pulpal
blood vessels. We speculate that changes occurring in the pulpal cir-
culation may be related to body growth spurts, especially in children/
adolescents in Group 3. Further studies are required to examine the
pulpal vessel properties through PWV and PTT as possible indicators of
elasticity in subjects of different ages.
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Archives of Oral Biology 83 (2017) 327–333
Fig. 7. The scattergram shows correlation between
weight/height of the children and TLP amplitude.
Group 4 with adult teeth had the lowest TLP amplitude, which was
in concordance with the LDF studies reported by Ikawa et al. (2003).
The decreasing number of pulpal blood vessels (Kishi & Takahashi,
1987) and age-related cardiovascular transitions, such as the increase in
arterial stiffness and decrease in vessel distensibilty, might explain this
finding (Allen & Murray, 2002).
4.2. OD
According to the present results, the OD of the teeth increased with
root formation. On radiographs, the hard tissue became thicker and
pulp chamber size narrower with tooth maturation (Fig. 1). Group 1
teeth with thinner dentin and a larger pulp chamber had the lowest OD,
while Group 3 teeth with thicker dentin and a narrower pulp chamber
had the highest OD (Fig. 4b). This result supports the finding of a
previous in vitro report that the whole tooth optical characteristics are
determined primarily by dentin, with pulpal blood having a minor role
(Kakino et al., 2007).
As for the dentin optical characteristics, the dentinal tubules has
dominant factor of the light attenuation. Dentin exerts a light-guiding
effect by scattering photons to and from the pulp chamber of the teeth
(Kienle & Hibst, 2006). Groups 3 and 4 teeth had similar hard tissue
thickness, so the light attenuation through the dentin layer was com-
parable. However, we assume that the Group 3 teeth had a slightly
bigger pulp chamber size than the Group 4 teeth. Our previous study
using an extracted tooth model showed that when the pulp chamber
size increased, the amount of blocked light also increased, resulting in a
simultaneous decrease in the number of photons routing around the
pulp chamber, which caused an increase in the OD (Kakino et al.,
2008). In addition, changes in the dentinal tubule’s composition ma-
terial and structure due to maturation can affect the light transmission
properties (Nanci, 2008; Vongsavan & Matthews, 1993). The role of
blood optical characteristics was also observed in our study. Group 4
teeth might had less blood volume due to aging (Kishi, Kai, Toris,
Tsumuraya, & Takahashi, 1989) than Group 3 teeth, resulting in a
slightly lower OD value. Based on these findings, varying pulpal blood
volume changes are represented by the TLP amplitude, whereas the OD
of the whole tooth indicates the absolute optical property, reflecting
tooth maturation, aging, and pathological conditions such as pulp canal
obliteration and calcification.
4.3. Tooth color
Clinically, discoloration of traumatized teeth is often observed. To
evaluate the relationship between the color of traumatized teeth and
pulpal circulation, we quantified the color of healthy central incisors as
reference data. The results showed no significant correlation between
the TLP amplitude and tooth color parameters (Fig. 6d–f), implying that
tooth color is not a dominant factor affecting the TLP amplitude.
However, the tooth color L*a*b* parameter values changed throughout
K. Ganbold et al.
the root formation process (Fig. 6a–c). A significant positive correlation
between age and b* (yellow hue) was recorded, which was consistent
with a previous study done by Hasegawa, Motonomi, Ikeda, and
Kawaguchi (2000) and Ten Bosch and Coops (1995). Those authors
cited the reason for the increase in yellowish color as the exposure of
dentin through the thin layer of enamel. However, in the present study,
the enamel of developing young permanent teeth was almost entirely
intact. We speculate that the increase in the yellow hue in this study
may have resulted from the thickening of the denting during tooth
maturation. The L* (lightness) value increased, but the a* (red hue)
value decreased with age or tooth maturation, and a significant dif-
ference was observed between the groups. However, this findings was
not consist with other reports (Odioso, Gibb, & Gerlach, 1999;
Hasegawa et al., 2000), which investigated subjects older than those in
the present study. Therefore, the color shift associated with healthy
tooth maturation remains to be evaluated.
4.4. EPT
EPT measurement demonstrated that sensitivity to electrical sti-
mulation increased with age and root development (Fig. 5c), which was
consistent with the findings of other studies (Brandt,
Kortegaard, & Poulsen, 1988; Klein, 1978). Most Group 1 teeth de-
monstrated no or low sensitivity to EPT, but we were able to record TLP
pulse waves. In this regard, since both EPT and TLP complement each
other, a comprehensive diagnosis with more than one pulp vitality test
may offer better outcomes.
This was the first attempt to record pulp blood flow changes in
different root formation stages utilizing tooth plethsymography. In the
clinical practice of pediatric dentistry, we often encounter cases re-
quiring a credible diagnosis of the pulp vitality of traumatized young
permanent teeth. Although these teeth often do not respond to pulp
sensitivity tests, the use of TLP allowed us to diagnose teeth with a
relatively high nerve stimulation threshold. However, TLP of trauma-
tized teeth showed a variety of amplitudes (Kakino, 2010). We suspect
that changes in the TLP amplitude may be caused by not only the
healing process of the pulp but also other factors, such as root devel-
opment, body growth, and tooth color. The present results clearly de-
monstrated dynamic changes in the pulp blood flow during different
root formation stages and may be used as reference data for a diagnosis
in young permanent teeth under pathological conditions.
A primarily limitation of the present cross-sectional study is that the
TLP data were collected from the teeth of subjects with different tooth
structures. To reduce the effects of the optical properties of the in-
dividual tooth morphology (dentin and enamel) as much as possible,
the TLP amplitudes were divided by the transmitted light intensity
(DC), following the pulse oximetry algorithm. However, contrary to soft
tissue plethysmography, the tooth plethysmogram was markedly af-
fected by the surrounding hard tissues (Kakino et al., 2007). To resolve
this problem, a longitudinal study following the teeth of the same
subjects during root development and body growth will enable the
more precise definition of the pulp blood flow changes. In addition, a
number of questions were not answered in the present study. Since our
subjects were children who were still in the early stages of body growth,
a study of young adults and elderly subjects may further improve our
understanding of the pulpal vascular changes. Furthermore, as the
present study evaluated only maxillary central incisor blood volume
change, a study on the different types of anterior teeth, which also have
a high frequency of dental trauma, is required.
Further studies are required to examine the growth and aging of
healthy teeth in a range of age groups in order to fully explore the
mechanisms underlying pulpal blood volume changes. In addition, a
study on the different types of anterior teeth will provide reference data
for diagnosing traumatized teeth. A longitudinal study of these same
subjects is also required to analyze the effect of root development on
the pulpal blood flow precisely. Considering the limitations of pulp
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Archives of Oral Biology 83 (2017) 327–333
sensitivity tests, such as the subjectivity and possible false negative
responses in young children, TLP has credible advantages based on its
objectivity and non-invasiveness.
5. Conclusion
The TLP amplitude and OD may indicate the changes in vascular
dynamics in the pulp and hard tissue maturation during the root for-
mation stages. Growth and development of the body positively corre-
late with the TLP amplitude in children. TLP can be a useful diagnostic
tool for detecting the pulp vitality of immature permanent teeth, even
in traumatized conditions.
Conflict of interest
We have no conflict of interest to declare.
Author contributions
Study conception and design: Satoko Kakino.
Acquisition of data: Khongorzul Ganbold and Satoko Kakino.
Analysis and interpretation of data: Khongorzul Ganbold and Satoko
Kakino.
Drafting of manuscript: Khongorzul Ganbold and Satoko Kakino.
Critical revision: Hideharu Ikeda and Michiyo Miyashin.
Acknowledgement
This study was supported by a Grant-in-Aid for Young Scientific
Research (B) (No. 25870201) from the Japanese Ministry of Education,
Culture, Sports, Science and Technology.
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