Examiner’s finger-mounted nearinfrared spectroscopy is feasible toanalyze cerebral and skeletal muscle
oxygenation in conscious Chihuahuas
Keisuke Hiwatashi
Kimiaki Doi
Risuke Mizuno
Makoto Yokosuka

Keisuke Hiwatashi, Kimiaki Doi, Risuke Mizuno, Makoto Yokosuka, “Examiner’s finger-mounted nearinfrared spectroscopy is feasible to analyze cerebral and skeletal muscle oxygenation in conscious
Chihuahuas,” J. Biomed. Opt. 22(2), 026006 (2017), doi: 10.1117/1.JBO.22.2.026006.
Downloaded From: http://biomedicaloptics.spiedigitallibrary.org/ on 03/02/2017 Terms of Use: http://spiedigitallibrary.org/ss/termsofuse.aspx

Journal of Biomedical Optics 22(2), 026006 (February 2017)

Examiner’s finger-mounted near-infrared
spectroscopy is feasible to analyze cerebral
and skeletal muscle oxygenation in
conscious Chihuahuas
Keisuke Hiwatashi,a,b,† Kimiaki Doi,c,† Risuke Mizuno,d and Makoto Yokosukaa,*aNippon Veterinary and Life Science University, Laboratory of Comparative Medicine, School of Veterinary Medicine, Musashino, Tokyo, Japan
Animal Medical Center of Gotemba Inter, Gotemba, Shizuoka, Japan
Doi Pet Clinic, Fujieda, Shizuoka, Japand
Tsukuba International University, Department of Medical Technology, Faculty of Health Sciences, Tsuchiura, Ibaraki, Japanbc

Abstract. To measure regional saturation of oxygen (rSO2 ) of hemoglobin and total hemoglobin index (HbI) in
the brain (through the molera of the head) and skeletal muscle (musculus gracilis) of conscious Chihuahua dogs
using an examiner’s finger-mounted near-infrared spectroscopy (NIRS) device, Toccare, we investigated brain
and skeletal muscle NIRS in 48 Chihuahuas without severe disease. To measure rSO2 and total HbI, a Toccare
probe was placed on the molera of the head and musculus gracilis of each dog for real-time recording. Stable
NIRS values were obtained within 10 s. We also examined the effect of anesthesia on rSO2 and total HbI of a
Chihuahua. Cerebral rSO2 values (59%  7%) were significantly lower than those obtained at femoral regions(67%  6%), whereas total HbI values in the brain (0.38  0.09) were significantly higher than those of themusculus gracilis (0.20  0.05). Sedation with a combination of medetomidine and ketamine decreased cerebralrSO2 along with a corresponding reduction in heart rate. Sevoflurane anesthesia with 100% O2 maintained rSO2
in the brain with an even lower heart rate. In conclusions, we measured brain and skeletal muscle rSO2 of hemoglobin in conscious Chihuahuas using a newly developed NIRS device, Toccare, and found that changes incerebral oxygenation levels were associated with administration of anesthetics. © The Authors. Published by SPIE
under a Creative Commons Attribution 3.0 Unported License. Distribution or reproduction of this work in whole or in part requires full attribution of
the original publication, including its DOI. [DOI: 10.1117/1.JBO.22.2.026006]

Keywords: brain; microcirculation; hemoglobin; imaging.
Paper 160764R received Nov. 4, 2016; accepted for publication Jan. 26, 2017; published online Feb. 15, 2017.

1

Introduction

Near-infrared spectroscopy (NIRS) is a unique visualization
technology used to measure tissue oxygen saturation of hemoglobin at the capillary level.1 Although pulse oximetry detects
the oxygen saturation of hemoglobin in pulsatile arterial bloodof the finger or ear,2 it cannot be used to analyze the oxygen
saturation in nonpulsatile environments including low-pressure
areas and the peripheral microcirculation system. NIRS is thus aclinically useful and advantageous tool for detecting oxygenation levels in local and microcirculatory spaces through the skinand bones and has been used as a noninvasive clinical methodin human patients.3,4 Several investigators have conducted
experimental NIRS studies of skin5 and skeletal muscle6–9 indogs. There are a few reports to evaluate cerebral oxygenationlevel using canine brain NIRS10 in comparison with human
medicine.1,3
Neuronal cells, astrocytes, pericytes, and capillary endothelial cells in the central nervous system constitute a neurovascular unit.11 Neuronal activity and metabolism are closely
related to regulation of the cerebral microcirculation, indicating*Address all correspondence to: Makoto Yokosuka, E-mail: mayokosuka@nvlu.ac.jp†

These authors equally contributed to this study.

Journal of Biomedical Optics

that brain autoregulation mechanisms play significant roles inmaintaining vital functions of the central nervous system.12
Recently, Kanayama and Niwayama13 developed an extremely
small and mobile NIRS (Toccare, an examiner’s finger-mountedtype) that is suitable for human fetuses and neonates, and they
were able to noninvasively measure fetal cerebral tissue oxygenation levels.14 It is very important to determine local brain
oxygen saturation of hemoglobin in a conscious condition
because sedation and anesthesia decisively affect cerebral circulation and neuronal activity/metabolism.15
Among companion dogs, most Chihuahuas have a molera of
the head, and the lacuna may remain open throughout life.
Therefore, we realized that a Chihuahua molera is a bonelesslocus and, consequently, NIRS beams easily reach the cerebral
cortex by passing through the molera in the scalp, and is, therefore, ideal for a pilot study of canine brain NIRS in conscious
state. In this study, we attempted to measure brain oxygenationlevels in conscious Chihuahuas by applying a Toccare probe to
the molera of the head. The objectives of this study were as follows: (1) to measure regional saturation of oxygen (rSO2 ) andtotal hemoglobin index (HbI) in the cerebral region of conscious
Chihuahuas using an examiner’s finger-mounted NIRS (Toccare),(2) to compare results between brain and femoral NIRS, and (3) toevaluate the effects of anesthesia on cerebral and femoral NIRS
values.

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Hiwatashi et al.: Examiner’s finger-mounted near-infrared spectroscopy. . .

2Materials and Methods

2.1

Animals

Forty-eight Chihuahuas that were hospital outpatients at Animal
Medical Center of Gotemba Inter in Gotemba City or Doi
Pet Clinic in Fujieda City, Shizuoka Prefecture, Japan, were
evaluated in this study. The dogs visited the clinics for regular
health examinations and/or vaccinations. By veterinarian physical examinations, we confirmed that 48 dogs demonstrated nosevere pathophysiological symptoms, although some (29%) had
mild symptoms including dermatitis, arthritis, gastroenteritis,
blepharitis, or a slipped disk. They did not take any drugs ortreatments before the NIRS measurements.

2.2

NIRS Equipment

The Toccare tissue oxygenation monitor (model KN-15) and its
NIRS probe were used in this study. The measurement methodof this device depends on spatially resolved NIRS with two LED
light sources (770 and 830 nm).13 Toccare enabled us to measurerSO2 (0% to 99%) and total HbI (0 to 1.0) of each organ at 5-mm
depth with a sampling interval of 0.5 s. Values of rSO2 and total
HbI were directly displayed on the monitor of the Toccare andalso recorded on a secure digital memory card. To perform
NIRS, we did not need to prepare a dark room and shading component due to the high power of the Toccare LED.

2.3

Experimental Protocol

This study was performed following informed consent fromowners and animal care approval from the Shizuoka Veterinary
Medical Association. Figure 1 shows CT images (left panel,
three-dimensional reconstruction; right panel, coronal plane)of the anatomical distribution and location of the molera in a
Chihuahua under inhalation isoflurane anesthesia. The Toccare
probe was applied to the molera of the head [Figs. 2(a) and 2(b)]and the left or right gracilis muscle. To tightly adhere the probe
against the skin, we gently pushed hair aside using a hairbrushand wetted cotton. In the protocols for the conscious condition,

dogs were sitting on the examination table during brain NIRS
measurements and standing on the table during skeletal muscle
NIRS. After attaching the NIRS probe, we could obtain a stablevalue of the brain and femoral NIRS within 10 s in conscious
Chihuahuas.
To evaluate effects of anesthesia on the brain and femoral
NIRS in a Chihuahua [Fig. 2(c)], inhalation of sevoflurane(1%) with 100% O2 was used for a minor surgery (castration)
after sedation with a combination of medetomidine [30 μg∕kg,
im (intramuscular injection)] and ketamine (2 mg∕kg, im).
Mask anesthesia was used for the castration. After the surgery,
we injected atipamezole (75 μg∕kg, im) into a dog to antagonize
the medetomidine-mediated sedation. We measured the NIRS
values, heart rates (beats/min), and respiratory times (times/min)
before and after anesthesia. In this protocol, we placed the dog
in appropriate positions, such as standing, sitting, or prone, corresponding to sedative and anesthetic conditions.

2.4

Statistical Analysis

We evaluated the data for 48 Chihuahuas, and the resulting
values are presented as the mean  SD, with n indicating thenumber of animals. Significant differences (P < 0.05) were
determined using paired Student’s t-test for comparisons
between cerebral and femoral values or unpaired Student’s t-test
for comparisons between genders. A regression analysis was
also performed using KaleidaGraph version 4.5.1 software.

3

Results

3.1

Age, Gender, and Body Weight of Chihuahuas

Chihuahuas in this study were between the ages of 0.3 and 16.5
years, with a mean age of 6.6  3.7 years (n ¼ 48). Fifteen dogs
(31%) were female, including some that were neutralized. The
body weights of the dogs were between 1.6 and 6.0 kg, witha mean body weight of 3.5  1.2 kg (n ¼ 48). There wereno significant relationships between age and body weight of
Chihuahuas (Fig. 3), indicating that there are neither linear
nor sigmoidal distributions.

Fig. 1 Computed tomography images (left panel, three-dimensional reconstruction; right panel, coronalplane) of a Chihuahua under intratracheal isoflurane anesthesia with 100% O2 . A nonwhite area over theskull indicates the distribution of the molera (green arrowheads in right panel). L and P in left panel indicate left and posterior, respectively. The yellow line in the right panel represents a length of 5 mm.

Journal of Biomedical Optics

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Hiwatashi et al.: Examiner’s finger-mounted near-infrared spectroscopy. . .
Table 1 NIRS parameters (rSO2 and total HbI) in cerebral and femoral parts of male and female dogs.
Male (n ¼ 33)

Female (n ¼ 15)

Parts

rSO2 (%)

Total HbIrSO2 (%)

Total HbI

Brain

58  70.37  0.09

61  60.40  0.09

Femoral

67  50.20  0.05

69  70.20  0.05

3.2

Values of r SO 2 and Total HbI in Cerebral andFemoral Regions

The femoral rSO2 (67%  6%) of the Chihuahuas was significantly higher than the cerebral rSO2 (59%  7%; P < 0.05). The
cerebral total HbI (0.38%  0.09%) of the dogs was significantly higher than the femoral total HbI (0.20%  0.05%;
P < 0.05). We also compared rSO2 and total HbI between maleand female dogs and found no significant differences in thoseparameters (Table 1).

3.3

Fig. 2 A representative picture showing measurement of canine brain
NIRS in (a) and (b) a conscious and (c) mask-anesthetized condition.
Under a tranquil environment in a consulting room, a conscious
Chihuahua was gently held by a veterinary nurse to prevent body
movement during the NIRS measurement. A Toccare NIRS probe
was placed on the molera of the head. The real-time values ofrSO2 and total HbI are displayed on the monitor of the Toccare (b)and (c).

Figure 4 shows regression analyses for (a) and (b) age and (c)and (d) body weight (a) and (c) against rSO2 and (b) and (d) total
HbI in the cerebral (red) and femoral (blue) regions in 48
Chihuahuas. There were slightly positive linear relationships
between age and rSO2 in the femoral regions [Fig. 4(a), blueline; y ¼ 64.333 þ 0.46136x, R ¼ 0.30097], whereas the brainrSO2 remained almost the same regardless of age [Fig. 4(a),red line; y ¼ 58.789 − 0.043461x, R ¼ 0.022826]. The relationships between age and total HbI in cerebral [Fig. 4(b), redline; y ¼ 0.38471 − 0.00033282x, R ¼ 0.01372] and femoral[Fig. 4(b), blue line; y ¼ 0.20874 − 0.001348x, R ¼ 0.1017]
regions were nonlinear as were the relationships between bodyweight and rSO2 in cerebral [Fig. 4(c), red line; y ¼ 55.021 þ
0.98257x, R ¼ 0.17224] and femoral [Fig. 4(c), blue line; y ¼
69.174 − 0.50232x, R ¼ 0.10937] regions. There were slightly
negative linear relationships between body weight and total HbIin the cerebral regions [Fig. 4(d), red line; y ¼ 0.46654 −0.023736x, R ¼ 0.32658], whereas positive linear relationships
were observed in the femoral regions [Fig. 4(d), blue line;
y ¼ 0.14893 þ 0.014365x, R ¼ 0.36173].

3.4

Fig. 3 Distribution of age and body weight of Chihuahuas in this study(n ¼ 48).
Journal of Biomedical Optics

Relationships of Age or Body Weight Against
NIRS Values

Effects of Anesthesia on NIRS Values

Finally, we examined the effects of inhalation anesthesia (sevoflurane) on changes in the rSO2 and total HbI of brain and femoral muscle during minor surgery of a Chihuahua (6-month-old
male with a body weight of 2.14 kg). Figure 5 shows the timecourse of changes in rSO2 (top panel) and total HbI (middle
panel) of the cerebral (red symbols and lines) and femoral (bluesymbols and lines) regions, and heart rates (bottom panel, closed
circles) and respiratory times (bottom panel, open circles) in adog before and after sedation and anesthesia. Excessive stressincreased cerebral rSO2 (from 51% to 61%) of the dog justbefore sedation with medetomidine and ketamine. After injection of the sedative, rSO2 values gradually decreased to reach
47%. The changes in rSO2 before and after sedation corresponded with fluctuations in heart rate. During sevoflurane
anesthesia with 100% oxygen, the heart rate was still low (after

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Hiwatashi et al.: Examiner’s finger-mounted near-infrared spectroscopy. . .

Fig. 4 Regression analyses for (a) and (b) age or (c) and (d) body weight (a) and (c) against rSO2 and(b) and (d) total HbI at the cerebral (red) and femoral (blue) regions of 48 Chihuahuas.

sedation, 94 beats∕ min; during anesthesia, 82 beats∕ min),whereas rSO2 increased from 47% to 56%. The cerebral rSO2
values were relatively stable (55% to 60%) during anesthesia
and recovery at 15 min. A sudden increase in the femoral total
HbI, associated with shivering, was observed at the 0 min recovery time.

4

Discussion

In this study, we could measure cerebral oxygen saturation ofhemoglobin in conscious Chihuahuas using a newly developed
NIRS device, Toccare, for the first time. In the Toccare probe,
the distance between the emitter and detectors was 8 mm and thewidth of the detectors was 3.5 mm.13 Thus, to perform brain
NIRS in Chihuahua, we needed at least an 8 × 3.5 mm square
as a measurement window. The Toccare LED beams reached a
sub-tissue space of 5-mm depth (Fig. 1, right panel), indicatingthat we acquired oxy- and deoxyhemoglobin signals from thesurface and superficial layers of the brain cortex. These opticalcharacteristics indicate that the three-dimensional structure of
the skull and the location of the molera are important determinants for accurate detection of signals during brain NIRS in dogs
with a molera. Several dog breeds such as Maltese, Yorkshire
terrier, English bulldog, lhasa apso, pug, and Pekingese possessa molera on the head,16 indicating that the Toccare can be used tomeasure and monitor brain oxygenation levels in other dogs inaddition to Chihuahuas.
Journal of Biomedical Optics

Originally, using Toccare, Uchida et al. measured cerebralrSO2 at the frontal region of the head of a human fetus14 because
this region of the fetal head is hairless and comprises thin bones.
The canine molera is usually located over the parietal region of
the head (Fig. 1). In dogs, the top part of the brain is considered
to be motor and somatosensory areas.17 The Brodmann areas
have been well established in humans and other primates forunderstanding neuronal connectivity and brain functions.
Unlike the classification of the feline brain,18 morphological andfunctional brain mappings in dogs remain unclear. Collectively,
the noninvasive measurement of Chihuahua brain NIRS using
Toccare may overcome the difficulty encountered in neuroscience and veterinary medicine regarding the evaluation of motorand somatosensory functions in a conscious state, although we
recognize that it is necessary to improve NIRS so that it can
detect cerebral rSO2 at increased depths. Recently, Uchida
et al.,19 demonstrated that an examiner’s finger-mounted tissue
oximetry, which is same device in this study, allowed measuring
mice brain NIRS as an experimental animal model. Collectively,
we propose here that using Toccare Chihuahua brain NIRS willintermediate between rodents and humans investigations.
Gygax et al.10 investigated NIRS of the brain functions ofconscious beagles in response to a command. In this study,
they demonstrated changes in the blood oxygenation level inthe canine frontal brain area, and they did not elucidate the percentage of oxygen saturation of hemoglobin. In this study, we
could detect rSO2 (%) in brain as well as muscle of thigh in

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Hiwatashi et al.: Examiner’s finger-mounted near-infrared spectroscopy. . .

conscious Chihuahuas. The cerebral rSO2 values were significantly lesser than those of the skeletal muscles. We speculatethat the discrepancy of rSO2 values between brain and hind leg
in the conscious condition results were because (1) brain oxygen
consumption would be maintained at a higher level comparedwith other parts of the body because neuronal activity andmetabolism strictly govern the cerebral microcirculation throughthe neurovascular unit and autoregulation mechanisms,11,12 and(2) the oxygen demand of skeletal muscles would be lessbecause the hind leg was in a resting condition. Through thisstudy, we could exhibit obvious heterogeneity of oxygenationlevels among organs in conscious dogs.
In a human study, fetal cerebral rSO2 measured using thesame device was 65.5%  8.58%,14 which is slightly higher
than that measured in canine brain and similar to the femoral
values in this study. The discrepancy between human fetal cerebral rSO2 values and the current results in canine brain is quite
intricate to explain because many factors including species
differences and conditions, e.g., body position or consciousness,need to be taken into account. We understand that measuring
area at the brain surface of Chihuahuas was anatomically different from human studies,14 and that the NIRS values obtainedin this study are a part of molera and specific parameters for
Chihuahuas. There were no significant linear relationships
between age or body weight and brain rSO2 , whereas the femoral rSO2 weakly depended on age in Chihuahuas [Figs. 4(a)and 4(c)]. We also identified the similarity of cerebral rSO2
in male and female dogs (Table 1). These results suggest thatirrespective of gender, age, or body weight, the cerebral oxygenation level of Chihuahuas is constantly maintained in the
conscious condition when dogs are kept quiet in a restful environment; in other words, anxiety or excitement in dogs will generate unusual cerebral rSO2 patterns.
We also evaluated another NIRS parameter, total HbI, in thebrain and femoral regions. It is conceivable that the total HbI
value represents the summation of oxy- and deoxy-hemoglobin
per unit area. As the hemoglobin content in red blood cells is
unchanged, the total hemoglobin may estimate the tentative
blood flow within the local and microcirculatory basin containing arterioles, capillaries, and venules. The total HbI values incerebral regions were significantly higher than those obtained at
the femoral skeletal muscles in this study, suggesting that in the
conscious state, brain blood flow per unit area may be greaterthan it is in the hind legs. Interestingly, in Fig. 4(d), the slopes ofbody weight versus total HbI of the brain and femoral regions
were negative and positive, respectively, whereas both total HbI
values were independent of age [Fig. 4(b)]. We thus assume thatan increase in body weight may reduce cerebral blood flow in
Chihuahuas, suggesting that obese subjects may be affected bydisorders related to brain microcirculatory dysfunction, such as
hypoxia or ischemia. Further investigation will be needed to
identify the physiological meaning of total HbI in a variety oforgans in the future.
Finally, we evaluated the effects of anesthesia on rSO2 andtotal HbI of cerebral and femoral regions in Chihuahuas (Fig. 5).
Using the NIRS protocol in series, we confirmed that Toccare
could detect changes in the NIRS parameters in response to
sedation and anesthesia. Cerebral oxygenation levels were
well maintained under sevoflurane inhalation with 100% O2even though the anesthetized dog exhibited a low heart rate.
Although we could detect changes in the parameters of brain
NIRS with 100% O2 inhalation, the values were not statistically
Journal of Biomedical Optics

Fig. 5 Time-dependent changes in rSO2 (top panel) and total HbI(middle panel) of cerebral (red symbols and lines) and femoral(blue symbols and lines) regions of a Chihuahua before and after
sedation/anesthesia. The bottom panel shows the heart rate (HR;closed circles) and respiratory times (RT; open circles) during thesame time course. Arrows indicate canine behaviors.

analyzed due to only one dog data, indicating that further investigation will be needed to identify changes in the brain NIRS
values in response to O2 inhalation and anesthesia. In human
medicine, NIRS is beginning to be used to monitor cerebral oxygenation levels under general anesthesia.20 These results suggest

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Hiwatashi et al.: Examiner’s finger-mounted near-infrared spectroscopy. . .

that, in the future, NIRS may be advantageous for monitoring
cerebral oxygenation in the brains of anesthetized dogs. Other
than anesthesia, we anticipate Toccare can be used as an oxygenation monitoring device in a variety of situations including
ischemia and reperfusion of organs, e.g., liver and kidney, during surgery. Given Toccare’s mechanical characteristics including its size and weight, use of AAA batteries, mobility, ease ofoperation, and data storage capabilities, NIRS will enable us tomeasure and monitor rSO2 and total HbI in the open air during
emergency and critical care. Rather than nuclear scanning forfunctional brain analysis, NIRS represents a clinically simple,
safe, and noninvasive technique for detection of tissue andorgan oxygenation levels in the microcirculation system.

5

Conclusions

The salient findings of this study are that we could measure oxygen saturation of hemoglobin in brain and skeletal muscle inconscious Chihuahuas using a newly developed NIRS, Toccare,and found that significant differences of rSO2 existed between
organs and changes in brain oxygenation levels are associatedwith anesthesia. We believe that Toccare NIRS will be used asa noninvasive method for monitoring vital oxygenation levels,
especially in brain, in medicine during surgery and emergency
and critical care.

Disclosures
All authors declare that there are no financial or other relationships that might lead to conflict of interest.

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Keisuke Hiwatashi graduated from Department of Veterinary
Science, Nippon Veterinary and Animal Science University, Tokyo,
Japan, in 1996. He received Japan national license of DVM from
MAFF in 1996. From 1996–1998, he worked at the Animal Medical
Center of Southern California, LA, USA. From 1998–1999, he worked
at the Tazi Animal hospital, Japan. In 1999, he opened the Animal
Medical Center of Gotemba Inter as the hospital director.
Kimiaki Doi graduated from Department of Veterinary Science,
Nippon Veterinary and Animal Science University, Tokyo, Japan, in
1993. He received Japan national license of DVM from MAFF in 1993.
From 1993–2004, he worked at the Morishita Animal hospital, Japan.
In 2004, he opened the Doi Pet Clinic, Fujieda, Japan, as the hospital
director.
Biographies for the other authors are not available.

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