Altern Ther Health Med 2011 (Nov); 17 (6): 12–17 ~ FULL TEXT
Takeshi Ogura, DC, PhD; Manabu Tashiro, MD, PhD; Mehedi Masud, MD, PhD;
Shoichi Watanuki; Katsuhiko Shibuya, MS; Keiichiro Yamaguchi, MD, PhD;
Masatoshi Itoh, MD, PhD; Hiroshi Fukuda, MD, PhD; Kazuhiko Yanai, MD, PhD
Takeshi Ogura,DC, PhD
Division of Cyclotron Nuclear Medicine,
Cyclotron and Radioisotope Center,
Tohoku University, Sendai, Japan
Background: Chiropractic spinal manipulation (CSM) is an alternative treatment for back pain. The autonomic nervous system is often involved in spinal dysfunction. Although studies on the effects of CSM have been performed, no chiropractic study has examined regional cerebral metabolism using positron emission tomography (PET).
Objective: The aim of the present study was to investigate the effects of CSM on brain responses in terms of cerebral glucose metabolic changes measured by [18F]fluorodeoxyglucose positron emission tomography (FDG-PET).
Methods: Twelve male volunteers were recruited. Brain PET scanning was performed twice on each participant, at resting and after CSM. Questionnaires were used for subjective evaluations. A visual analogue scale (VAS) was rated by participants before and after chiropractic treatment, and muscle tone and salivary amylase were measured.
Results: Increased glucose metabolism was observed in the inferior prefrontal cortex, anterior cingulated cortex, and middle temporal gyrus, and decreased glucose metabolism was found in the cerebellar vermis and visual association cortex, in the treatment condition (P < .001). Comparisons of questionnaires indicated a lower stress level and better quality of life in the treatment condition. A significantly lower VAS was noted after CSM. Cervical muscle tone and salivary amylase were decreased after CSM.
Conclusion: The results of this study suggest that CSM affects regional cerebral glucose metabolism related to sympathetic relaxation and pain reduction.
From the FULL TEXT Article
Chiropractic spinal manipulation (CSM) is an alternative
treatment for ailments such as neck, back, and
lower back pain. For >100 years, chiropractors have
asserted that overall health can be improved through
spinal manipulative therapy. [1–5] Research on CSM has
been extensively performed worldwide, and its efficacy on musculoskeletal
symptoms has been well documented. The autonomic nervous
system has been invoked in constructing mechanisms that
account for the effect of spinal dysfunction.  Previous studies documented
a potential relationship between the vertebral subluxation
complex and the function of the autonomic nervous system. [1, 6–13]
These studies mainly discussed the autonomic effects on cardiovascular
function in relation to CSM. [9, 11–13] A recent study using heart
rate variability analysis documented that chiropractic adjustment
affects the autonomic nervous system.  However, literature search
showed no study using positron emission tomography (PET) to
examine regional cerebral metabolic changes related to autonomic
responses resulting from CSM.
Only one available neuroimaging study on CSM using single
photon emission computed tomography (SPECT) indicated
decreased regional cerebral blood flow in the left cerebellum related
to adverse reactions after treatment.  Since this study focused on
the adverse reactions, the brain effects and the clinical effects of
CSM have remained unknown. Recent chiropractic research documented
the need for a functional neuroimaging study regarding the
effects of spinal manipulation for deeper understanding of the neurophysiological effects of CSM.  Thus, we hypothesized that one
CSM might induce metabolic increase or decrease (activation or deactivation)
in the brain regions associated with autonomic nervous
functions in response to CSM intervention: the limbic and paralimbic
regions such as prefrontal cortex, orbitofrontal cortex, cingulate
gyrus, striatum and thalamus, cerebellum, and brain stem.
Functional neuroimaging techniques are powerful tools to
investigate neuronal activity in the human brain.  The PET scan
has been used for measuring regional cerebral blood flow and
regional cerebral metabolic rate using radiolabeled molecules,
which are either injected intravenously or continuously inhaled by
the participant. [15–21] In the research setting, functional neuroimaging
has been used in studies of acute brain activation, and for this purpose,
functional magnetic resonance imaging (fMRI) has replaced
PET with [15O]H2O because of its preferred spatial resolution, avoidance
of radioactive materials, and operating cost per investigation. [15, 18, 19] However, PET with 18F-labeled fluorodeoxyglucose (FDG)
has been regarded as an excellent imaging marker of brain metabolic
activity (glucose consumption).  The molecule FDG, a radioactive
analogue of glucose, is trapped metabolically into activated cells
in the brain and can be substantially used for evaluating physiological
and biomechanical functions in vivo.  Initially, this technique
was used in healthy volunteers who performed a natural running
task in upright posture.  Later, this technique was applied to daily
movement  and alternative therapy such as aromatherapy.  An
important advantage of the FDG technique is that the regional
brain activity during 30 minutes after injection is averaged and
recorded based on the biochemical property of “metabolic trapping,”  where the phases for FDG uptake and for PET measurement
can be separated (Figure 1). Another advantage of this
technique is low radiation exposure achieved by a sensitive 3–dimensional
data acquisition mode. 
We hypothesized that a CSM treatment might induce metabolic
increase or decrease (activation or deactivation) in the brain
regions associated with autonomic nervous functions in response to
CSM intervention: the limbic and paralimbic regions such as prefrontal
cortex, orbitofrontal cortex, cingulate gyrus, striatum and
thalamus, cerebellum, and brain stem. The aim of the present study
was to investigate the effects of CSM on brain responses in terms of
cerebral glucose metabolic changes using PET and FDG. In addition,
we evaluated the relation between the results of PET investigation
and the changes in autonomic function and pain intensity
induced by chiropractic treatment.
Participants and Materials
Volunteer men with cervical pain and shoulder stiffness were
recruited after researchers placed a poster on the campus of Tohoku
University. Included were men aged 20 to 40 years with cervical
pain and shoulder stiffness who did not receive any kind of manipulative
treatment for ≥1 month before the experiment.
Exclusion criteria were
(1) the presence of disc problems such as disc herniation
or significant disc degeneration and
(2) any other physical or mental
disorders or medication that might affect brain function or perfusion.
After giving informed consent, all 15 candidates were first
assigned for MRI examination of the cervical region, and 3 participants
with disc problems were excluded from the study. Medical
screening was performed to confirm absence of any disorders or
medication that might affect brain function. Therefore, 12 men
volunteers aged 21 to 40 years (mean age ± SD, 28 ± 7 y) were
included in the study. Women were not included because of the
higher risk of radiation exposure to the ovary and the physiological
fluctuation of the brain activity associated with the menstrual
cycle. The present study protocol was approved by the Ethics
Committee of Tohoku University Graduate School of Medicine,
Sendai, Japan (No. 2008–115).
The present study was conducted in crossover study design, in
which each participant was examined twice (once in the “treatment”
and the other time in the “control” [“resting”] conditions) to
compare resting regional brain activity in the 2 conditions (Figure
1). In the treatment condition, participants received a single CSM
intervention including a CMS diagnostic procedure (in total 20
minutes). Shortly after the CSM treatment, FDG-containing saline
solution was injected into the participant through the left antecubital
vein (37 MBq) in a quiet, dimly lit room. Participants were
asked to sit in a relaxed manner with their eyes closed for 30 minutes
before the scan. The brain scan was initiated 30 minutes after
the FDG injection using a PET scanner (SET2400W, Shimadzu Inc,
Kyoto, Japan). The PET scan covered the entire brain in 1 scan, taking 10 minutes for the emission scan and another 5 minutes for the
transmission scan for tissue attenuation correction (Figure 1). In the
scan for the control condition, FDG was injected into the participant
after a 20 minute resting phase instead of CSM intervention;
the scanning procedure following was identical to that for the treatment
condition (Figure 1). The radiation exposure from 1 PET scan
in this study was estimated at approximately 0.9 mSv; this was comparable
to the exposure from a chest radiograph (0.4 mSv per test)
and less than annual environmental exposure (2.4 mSv). 
The order of the 2 scans — that is, “control–treatment” and
“treatment–control” — was counterbalanced to minimize an “order
effect.” Order effect occurs because study participants tend to feel
psychophysiological stress more in the first scan than in subsequent
scans. Therefore, the protocol was prepared to minimize this orderassociated
effect. As a result, the first scan was performed in the
treatment condition in half of the participants and vice versa. The
interval between the first and second scans was ≥1 week to eliminate
residual effects of treatment; the interval between conditions
(scans) ranged from 1 to 6 weeks (mean interval ± SD, 22 ± 13 d).
The CSM was performed by the same chiropractor, an advanced
proficiency-rated doctor of activator methods.
Questionnaires were used for subjective evaluation.
Participants were requested to answer questions related to the
Stress Response Scale (SRS-18) and European Organization for
Research and Treatment of Cancer Quality of Life Questionnaire-
Core 30 (EORTC QLQ-C30) immediately after the CSM treatment
and before FDG injection. Results of SRS-18 and EORTC QLQ-C30
were examined using Wilcoxon signed-rank test for statistical analysis.
In addition, intensity of subjective pain sensation was evaluated
using a visual analogue scale (VAS) (0, no pain; 10, maximum possible
pain) before and after CSM intervention. Wilcoxon signed-rank
test was performed for analysis of the VAS results, as well. Cervical
muscle tone was measured bilaterally at the superior part of the trapezius
muscle (Muscle Meter PEK 1, Imoto Inc, Kyoto, Japan).
Salivary amylase was determined (Amylase Monitor, Nipro Inc,
Osaka, Japan) as a measure of changes in autonomic nervous system
function. The measurements of muscle tone and salivary amylase
were performed before and after the 20–minute treatment or
resting phase (Figure 1). Paired t tests were performed on measurements
of muscle tone and salivary amylase to determine differences
in before and after measurements between the resting and treatment
18F-labelled Fluorodeoxyglucose Positron Emission Tomography
The PET brain images were analyzed to identify regional
changes in glucose metabolic rate using a software package
Statistical Parametric Mapping 2 (SPM2, Functional Imaging
Laboratory, London, United Kingdom). [25, 26] Positional errors
between the two scans were corrected for each participant, using
the realignment function of the SPM2. The FDG brain template
(Montreal Neurological Institute, McGill University, Canada)  was
used for anatomical standardization (spatial normalization) of the
PET images by applying linear and nonlinear transformations,
which minimized the intersubject differences in gyral and functional
anatomy. The size of each voxel is converted into 2 mm (for x, y,
and z axes) in the normalized image. The normalized data were
smoothed using isotropic Gaussian kernel of 12 mm (for x, y, and z
axes) to increase the signal-to-noise ratio by suppressing high frequency
noise in the images.
Voxel-by-voxel analysis (such as Statistical Parametric
Mapping) is the standard tool for detecting regional changes in
radioactivity levels in certain brain regions. The most popular contrast
in these studies has been to contrast “resting” with “task or
stimulus.” For statistical analysis, all voxel values were normalized
to an arbitrary global mean value of 50 mg/100 mL/min by analysis
of covariance to exclude the effects of intersubject variability in
global cerebral glucose metabolism. A paired t test was applied to
each voxel; only voxel clusters were maintained with voxels corresponding
to P < .001 in a single test (height threshold for voxel values)
in 2 ways. 
Usually, statistically significant voxels tend to
appear in a group since each neural substructure has a certain volume
in human brain (eg anterior cingulate cortex). The size of the
voxels group (cluster size) is described by the number of voxels
showing statistical significance together. Based on the fact that each neural substructure has a certain volume, a very small cluster with
just a few voxels is not physiological and often produced by noises
in images. Thus, an extent threshold for the voxel cluster size is
additionally defined (10 to 50 voxels minimum).  The statistical
significance of a regional metabolic change was given in z scores.
The z score value was the difference between the treatment and control
group mean values, divided by standard deviation of the control
values [(Meantreatment-Meancontrol)/SDcontrol]. Empirically in Statistical
Parametric Mapping analysis, a z score higher than 3.0 (approximately
corresponding to P < .001) was considered statistically significant.
The location of each statistical peak was identified based on a
coplanar stereotaxic atlas of the human brain.  In the stereotaxic
atlas, the location of statistical peak is described in x,y,z axes of the
stereotaxic coordinates of the standardized human brain space.
Each location is also classified into a brain area called Brodmann’s
area (BA) defined by its histological similarity that also suggests
functional similarity.  Statistically significant areas were superimposed on the standard MRI brain template images (Figure 2).
The FDG-PET analysis revealed changes in regional cerebral
metabolism between resting and treatment (P < .001). In the treatment
condition, increased glucose metabolism was observed in the
inferior prefrontal cortex (BA 47), anterior cingulate cortex (BA 32),
and middle temporal gyrus (BA 21); decreased glucose metabolism
was observed in the cerebellar vermis and visual association cortex
(BA 19) (Table 1).
Results of subjective measures revealed significant differences
between the resting and treatment conditions. The mean SRS-18
score was significantly lower in the treatment than the resting condition
(Table 2). The mean EORTC QLQ-C30 score was also significantly
lower in the treatment than resting condition (Table 2).
Comparisons of mean VAS showed that pain was significantly
improved after treatment (Table 2). Measurements of cervical muscle
tone showed significant improvements from the resting to treatment
conditions (Table 2). A significant decrease in mean salivary
amylase was observed after chiropractic treatment (Table 2).
In the present study, participants had cervical pain at the time
of the examination as commonly experienced by many chiropractic
patients. Psychological stress may be a cause of cervical pain, and
diagnosis and management of cervical pain routinely includes psychological
stress management [28–33] because psychological stress
causes sympathetic activation. [34–36] Therefore, it is possible to compare
autonomic function in the resting and treatment conditions in
patients who have cervical pain. However, the usefulness of CSM for
cervical pain is controversial because of possible adverse reactions of
cervical adjustment, including a significant increase in neck pain and
stiffness and occasional headaches or radiating pain. [37, 38] Therefore, we
selected Activator Methods as the treatment procedure in the present
study. Activator Methods are a form of research-based spinal manipulative
therapy  in which high-velocity and relatively low force–impact
instruments known as Activator Adjusting Instruments are used. 
Activator Adjusting Instruments are in use by >50% chiropractic practitioners. [40, 41] In addition, investigations on Activator Adjusting
Instruments have been performed because of safety concerns related
to general cervical manipulation [39, 40, 42, 43]; in one study, Activator
Adjusting Instruments maximized therapeutic effects and benefits
and decreased the risk of iatrogenic injury. 
In previous studies aiming at scientific examination of the
autonomic effects of CSM intervention, cardiovascular function and
subjective feeling had been the main outcome measures. [10, 12–14]
However, it would be useful to examine the status of regional brain
activity immediately after the CSM intervention. We first applied
the FDG technique for a long-term activation study in healthy volunteers; [21–24] the regional brain activity during 30 minutes after FDG
injection was averaged and recorded based on the biochemical
property of “metabolic trapping.”  In the present study, the regional
metabolic changes in the limbic and paralimbic regions, cerebellum,
and brain stem were expected.
In the present PET investigation, the most significant change
was detected in the cerebellar vermis, which was deactivated in the
treatment condition compared to the resting condition. The cerebellar
vermis may be important in pain perception. Neuroimaging
studies have shown a pattern in cerebellar activation during the
pain response. [44–46] Glucose metabolic changes have been noted in
the cerebella of 13 of 18 patients suffering regional pain syndrome, 
and other authors have noted a similar activation pattern in the cerebellum. [47, 48] In the present study, all participants had neck pain at
the time of the experiment, and the results of VAS indicated a significantly
lower value after CSM. Thus, deactivation of the cerebellar
vermis in this study may be related to pain reduction in the participants.
The cerebellar vermis is also concerned with mental stress.
Painful heat activates the anterior cerebellum around the vermis,
and a sensory cue that anticipates the painful stimulation results in
activation of the posterior cerebellar vermis. [45, 46] In addition, the cerebellar
vermis is involved with the autonomic nervous system.
Previous studies have suggested that the cerebellum is involved in
the regulation of autonomic responses in aversive conditioning. [44, 49, 50]
Removal of the cerebellum impairs performance of autonomic
functions including salivary, cardiac, and respiratory
conditioning. [44, 49, 50] These effects on aversive conditioning can be
localized to the cerebellar vermis.  Stimulation of the cerebellar vermis,
not the hemispheres, inhibits vasomotor tone previously
increased by peripheral stimulation. [44, 51] Thus, deactivation of the
cerebellar vermis in the present study may have been related to a
decrease in sympathetic tone. Mental stress causes sympathetic activation, [34–36] and stress-related disorders are frequently accompanied
by increased sympathetic activity and muscle tone.  Some studies
have shown that chronic activation of the sympathetic nervous system
in chronic stress facilitates tonic and painful muscle contractions,
as has been suggested for chronic tension-type headaches and
work-related myalgia. [34, 52, 53] In the present study, measurement of
muscle tone indicated a significantly lower value after CSM at which
point the cerebellar vermis was deactivated. Therefore, we suggest
that deactivation of the cerebellar vermis may be preceded by
decreases in sympathetic tone, muscle tone, and pain.
The anterior cingulate cortex, inferior prefrontal cortex, and
middle temporal gyrus were activated in the treatment condition in
the present study. The cingulate cortex is involved in the generation
of autonomic responses, [34, 54, 55] and performance of relaxation tasks
may elicit maximal activation in the anterior cingulate region.  This
region of the limbic cortex has been implicated in cognitive and
emotional processing and as part of the midline attentional system
that involves the dorsolateral prefrontal cortex. [56–58] The lateral prefrontal
regions are deactivated during various cognitive tasks compared
to resting. [59–63] It is possible that the lateral prefrontal regions
are activated during the relaxed condition. Activation of the inferior
prefrontal cortex in the treatment condition may indicate a relaxation
effect. Thus, the results of the present study suggest that activation
of the anterior cingulate cortex and inferior prefrontal cortex
may arise from sympathetic relaxation.
Measurement of salivary amylase in the present study revealed
significantly lower values after CSM and increased values in the resting
condition. Salivary measures have become increasingly important
in psychoneuroendocrinological research on stress.  A
parameter of salivary measures thought to reflect stress-related
changes in the body is the salivary enzyme alpha-amylase. [64–68] Authors
have documented an increase in salivary amylase in people undergoing
psychological stress. [64, 65] Thus, it is possible that a decrease in salivary
amylase is observed in people in a relaxed condition. Regarding
the results of PET analysis, the reduction in salivary amylase in the
present treatment condition may be related to activated areas and
deactivated areas may be related to sympathetic relaxation.
The limitations of this study include the limited number of participants
and absence of a control group, though many clinical PET studies
have been done without control groups based on test-retest reproducibility.  Furthermore, some of the results in this study are based on subjective
evaluations of the participants. An additional limitation is that
the chiropractic treatment was performed by a single practitioner.
Another disadvantage of this technique would be radiation exposure,
though the exposure was as low as reasonably achievable.
In summary, the present study demonstrated sympathetic
relaxation and corresponding regional brain metabolic changes, as
well as reduced muscle tone and decreased pain intensity following
a chiropractic spinal manipulation. FDG-PET seems to be a very
promising tool for elucidating the underlying mechanism of clinical
effects of the chiropractic treatment. Further neuroimaging studies
are needed to support the results because the number of participants
was small in the present study.
Authors would like to thank Kazuko Takeda, of the Department of Cyclotron Nuclear Medicine, Cyclotron and Radioisotope Center,
Tohoku University, for her technical support on this study. The
authors also would like to thank the Japan Chiropractic Doctor
College for its contribution of funding to this study.
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