FROM:
Chiropractic & Manual Therapies 2021 (Feb 5); 29: 6 ~ FULL TEXT
Christopher A. Malaya, Joshua Haworth, Katherine A. Pohlman & Dean L. Smith
Center for Neuromotor and Biomechanics Research,
University of Houston,
Houston, TX, USA.
Background: Previous research demonstrated that manipulation of the extremities was associated with changes in multisegmental postural sway as well as improvement in a lower extremity balancing task. We were interested if these effects would extend to an upper extremity task. Our aim in this study was to investigate whether extremity manipulation could influence dual task performance where the explicit suprapostural task was balancing a water filled tube in the frontal plane.
Methods: Participants were healthy volunteers (aged 21-32 years). Upper- or lower-extremity manipulations were delivered in a participant and assessor blinded, randomized crossover, clinical trial. Postural (center of pressure) and suprapostural (tube motion) measurements in the frontal plane were made pre-post manipulation under eyes open and eyes closed conditions using a BTrackS™ force plate and a Shimmer inertial measurement unit, respectively. Pathlength, range, root mean square and sample entropy were calculated to describe each signal during the dual task performance.
Results: There was no main effect of manipulation or vision for the suprapostural task (tube motion). However, follow-up to interaction effects indicates that roll pathlength, range and root means square of tube motion all decreased (improvement) following lower extremity manipulation with eyes open. Regarding the postural task, there was a main effect of manipulation on mediolateral center of pressure such that pathlength reduced with both upper and lower extremity manipulation with larger decreases in pathlength values following upper extremity manipulation.
Conclusion: Our findings show that manipulation of the extremities enhanced stability (e.g. tube stabilization and standing balance) on performance of a dual task. This furthers the argument that site-specific manipulations influence context specific motor behavior/coordination. However, as this study focused only on the immediate effects of extremity manipulation, caution is urged in generalizing these results to longer time frames until more work has been done examining the length of time these effects last.
Trial registration: Clinicaltrials.gov
NCT03877367, Registered 15 March 2019. Data collection took place July 2019.
Keywords: Chiropractic manipulation; Coordination; Extremity; Motor control; Postural balance.
From the FULL TEXT Article:
Background
Maintaining an upright stance requires torques to be
generated around the ankles, knees, hips and even the
upper extremities. [1–4] Movement of one part of the
body entails compensatory adjustments elsewhere for bipedal
individuals to maintain their center of mass above
their base of support and thus remain standing. In both
posture and goal directed “suprapostural” activities, such
as reaching or balancing an object with the upper extremities,
the control of movement depends on the continuous
and accurate regulation of many muscles, joints
and limbs. [5, 6] It has been suggested that during these
dynamic activities, the arms and trunk may be used to
generate restorative torques to reduce the angular momentum
of the body [1], which would require proprioceptive
information relating to the position of not only
the limbs, but also the trunk and head. Accordingly, dynamic
postural control seems to require whole body
coordination.
Evidence for neurologically based mechanisms of action
for spinal manipulative therapy include central
changes in sensorimotor and cortical integration [7, 8], as well as peripheral changes to volitional elbow flexor
activity [9] and joint position sense. [10] While it has
been suggested that chiropractors examine posture from
a dynamic perspective, including suprapostural behaviors [4], few research studies have been conducted in this
area. There are even fewer research studies exploring
the effects of extremity joint manipulation on postural
dynamics and/or sensorimotor integration.
Human postural control is tantamount to one’s ability
to find and maintain bipedal balance in an environment,
and the neuromusculoskeletal system is the mediator of
and primary responder to corrective movements meant
to maintain stability. It is important then, that health research
examine topics that will add to our basic understanding
of how people’s movements and behaviors, as
well as their anatomy and physiology, change with joint
manipulations. We previously conducted a study that
examined the effect of upper and lower extremity manipulation
on posture and balance. [11] We found that
lower extremity manipulation influenced several dynamic
measures of postural sway while standing on both
the ground and rocker board. That is, extremity joint
manipulation of the lower extremities improved the
organization of sway for the trunk (anterior-posterior
direction) and rocker board (medial-lateral direction)
and extremity manipulation of the upper extremities reduced
roll range and pathlength on the lower extremitybased
rocker board task. We postulated that these effects
could be due to a change in sensory input and respective
motor output leading to behavioral modifications such
as restorative torques and postural sway. Furthermore,
the magnitude and direction of the sensorimotor change
appeared to be responsive to the task being performed
and the joint being manipulated.
As a follow-up to that study, we examined the effects
of upper and lower extremity joint manipulations on an
upper body task, holding a water-filled tube parallel to
the ground. Given that holding a tube while standing is
a dual task, we assessed participant’s performance with
both posturography and an inertial measurement unit
(IMU). Our aim was to investigate whether extremity
manipulation could influence dual task performance
where the explicit suprapostural task was balancing a
water filled tube in the frontal plane by the upper extremity.
Since vision influences tactile processing [12, 13], we tested participants while standing with both eyes
open and closed. We hypothesized: 1) both upper and
lower extremity manipulation would reduce tube roll parameters,
as well as mediolateral postural sway; 2) upper
extremity manipulation would reduce tube roll to a
greater extent, and that lower extremity manipulation
would reduce postural sway to a greater extent; 3) the
presence or absence of vision would also influence task
performance.
Methods
Participants
A sample of 23 healthy chiropractic students (78% male)
between the ages of 21 and 32 (mean age ± standard deviation:
27.4 ± 2.7 years) were recruited. Participants
were recruited from the Parker University student body
with flyers posted around campus. Interested participants
contacted the study coordinator from information
listed on the flyer and were scheduled for screening.
Screening and testing occurred on the same day. Eligible
participants were between the ages of 18 and 35, were
not pregnant, had no known musculoskeletal, neurological
or visual impairments that could impact their
ability to stand upright and were asked to refrain from
any chiropractic manipulations outside of the study itself.
Written informed consent was obtained from each
participant prior to the start of experimental procedures.
Approval to conduct this study was granted by the Institutional
Review Board at Parker University (#A-00186),
in accordance with the Declaration of Helsinki. All
testing was performed at Parker University’s Research
Center. This study was registered at ClinicalTrials.gov;
(NCT number: NCT03877367). Data collection took
place July 2019.
The within subjects sample size for this study was
based on a power analysis conducted by an independent
biostatistician. The sample size for this study was based
on pre-post standard deviations (SDs) of mean changes
in mediolateral (ML) rocker board sample entropy
(SampEn) from our previous study. [11] As such, twenty
participants per group would provide at least 80% power
to detect a medium to large effect size of 0.335 at a 0.05
level of significance.
Study design
Figure 1
|
This was a crossover trial. We used a within-subjects
study design to determine the influence of each of the
conditions on our dependent variables and to control for
the potential influence of individual differences. The
study chiropractor and data collectors were blinded. The
study chiropractor was aware of treatment assignment
but was blinded to the values of the measurements
taken. Data collectors were aware of measurement
values but were blinded to treatment assignment. Participants
were enrolled by the study coordinator after
which they were block randomized into two different
groups by a custom MATLAB script. The script was run
and results delivered to the doctor performing the interventions
by a graduate student not involved in data
collection. Group one received an upper extremity
manipulation series on the first day and, after a 24-h
washout period, returned and received a lower extremity
manipulation series. Group two received a lower extremity
manipulation on the first day and an upper extremity
manipulation series on the second day (see Figure 1). Participants
were assessed on dual task performance no
more than 2 min before and no more than 2 min after
receiving joint manipulations on both days.
The joint manipulations were performed distally to
proximally and were distal radioulnar, humeroulnar, and
glenohumeral (upper extremity series) and tibiotalar,
tibiofemoral, and coxofemoral joints (lower extremity
series), respectively. Both series were performed bilaterally
for each participant and all manipulations were
performed by an experienced chiropractor with greater
than 10 years clinical experience.
Dual task
Figure 2
|
Participants were asked to stand comfortably on a
Balance Tracking System (BTrackS™, San Diego, CA)
force plate with their elbows bent at 90 degrees and
hands in line with elbows. They were then handed a
capped 2" diameter PVC tube (60.5" long, weight:
4.60 lbs) half-filled with water (see Figure 2). Previous
research using a similar water filled tube has found
that when lifted, water within the tube moves and
immediately demands control, stabilization and
greater muscle engagement particularly with paraspinal,
deltoid, and abdominal muscles. [14] Participants
wore comfortable, athletic shoes during the
testing sessions and the same pair of shoes across
days. This was to ensure that standing test conditions
mirrored normal, everyday standing as closely as possible.
Wearing a standard/athletic shoe compared to
barefoot does not seem to significantly affect postural
balance or range of motion particularly on a firm surface. [15–17]
Participants were instructed to “hold the tube level
with the ground”. Participants held the tube for 30 s
each under the eyes closed and eyes open conditions.
Visual condition was randomized by participant using a
custom MATLAB script, and this test order was maintained
for the duration of the study. Data capture began
immediately after the study associate released the tube
into the participants hands.
Data collection
The tube was fitted with an IMU (Shimmer Sensing)
that collected kinematic data. Data were streamed wirelessly
at 51.2 Hz to the Consenys v.1.5.0 software platform
(Shimmer Sensing) and exported for processing.
Center of pressure (COP) data were collected by a
BTrackS™ (Balance Tracking Systems) force plate.
Data were acquired through the Explore Balance software
application (Balance Tracking Systems, version
2.0.4) at 50 Hz.
Data from the tube and force plate were processed by
a custom Matlab script (Matlab R2018b:9.5.0.944444).
Trial duration for each participant was 30 s with eyes
open and 30 s with eyes closed, respectively. All sample
data were processed. SampEn, path length (pathlength),
range, and root mean square (RMS) were calculated for
the roll direction of the tube sensor (in degrees) as well
as for the ML COP of the force plate (in centimeters).
SampEn is a measure of the complexity or repeatability
of a physiological time series. [18, 19] In this study,
pathlength is the cumulative distance traveled by the
tube sensor or the participant and range is distance between
the maximum excursions of the tube or the participant’s
mediolateral CoP. [19] RMS is a measure of
the magnitude that the tube sensor or the participant’s
CoP varies with respect to the mean location. [19
Data analysis
Change scores (post minus pre) were calculated for
SampEn, pathlength, range and RMS for site of manipulation
and visual condition. These change scores served
as the dependent variable in separate analyses for the
IMU and COP measures. All upper and lower extremity
manipulation and eyes open/eyes closed change scores
were entered into the analysis. Statistical analysis of
COP and IMU data was performed using a 2 × 2 withinsubjects
ANOVA (2 factors: site of manipulation and
visual condition, with 2 levels each: upper and lower
extremity manipulation, and eyes open and eyes closed,
respectively). Post hoc tests were performed using Bonferroni
corrected pairwise comparisons. All analyses
were conducted using IBM SPSS Statistics for Windows,
Version 25.0 (IBM Corp., Armonk, NY, USA). Statistical
significance was set at an alpha value of 0.05.
Results
Participants
One participant was excluded from randomization due
to failure to meet inclusion criteria (outside of age
range). No participants were lost to follow-up and all
collected data were used in the analysis. There were no
adverse events or unintended effects during the course
of the study.
Suprapostural task
Table 1
|
There were no main effects of manipulation or vision for
any of the measured dependent variables. See Table 1
for mean change scores and standard deviations for tube
roll motion. The main effect of manipulation was not
significant for roll path length F(1,22) = 0.079, p = 0.78;
range F(1,22) = 0.31, p = 0.59; RMS F(1,22) = 0.03, p =
0.87; or SampEn F(1,22) = 0.01, p = 0.93. The main effect
of vision was not significant for roll path length F(1,
22) = 0.84, p = 0.37; range F(1,22) = 0.38, p = 0.54; RMS
F(1,22) = 0.00, p = 0.98; or SampEn F(1,22) = 0.18, p =
0.68. However, interactions for roll path length, roll
range, roll RMS and roll SampEn were all significant.
Post hoc pairwise comparisons were performed for significant
interactions with a Bonferroni adjustment applied.
For roll path length, the significant interaction, F(1,
22) = 11.92, p = 0.002, ηp2 = 0.351 with follow up comparisons showed a significant effect of lower extremity
manipulation with vision (p = 0.022). Specifically, there
was a reduction in roll path length following lower extremity
manipulation with eyes open (mean difference =
– 190.82 degrees; 95% CI, – 358.27 to – 23.37) compared
to eyes closed (mean difference = 17.74 degrees; 95% CI,
– 130.69 to 166.16).
For roll range, the significant interaction, F(1,22) =
7.27, p = 0.013, ηp2 = 0.248 with follow up comparisons
showed a significant effect of lower extremity manipulation
with vision (p = 0.030). Roll range reduced to a
greater extent following lower extremity manipulation
with eyes open (mean difference = – 6.01 degrees; 95%
CI, – 10.42 to – 1.60) compared to eyes closed (mean
difference = – 1.10 degrees; 95% CI, – 4.45 to 2.25).
For roll RMS, the significant interaction, F(1,22) =
12.89, p = 0.002, ηp2 = 0.37 with follow up comparisons
also showed a significant effect of lower extremity manipulation
with vision. Roll RMS also reduced to a
greater extent following lower extremity manipulation
with eyes open (mean difference = – 0.60 degrees; 95%
CI, – 0.99 to – 0.22) compared to eyes closed (mean difference
= – 0.15 degrees; 95% CI, – 0.48 to 0.19).
For roll SampEn, the significant interaction, F(1,22) =
4.95, p = 0.037, ηp2 = 0.184 did not produce any significant follow up comparisons.
Postural task
There was a main effect of manipulation for ML
pathlength, F(1,22) = 9.92, p = 0.005, ηp2 = 0.31. Premanipulation values were larger than post manipulation
values. Both manipulation types reduced ML COP pathlength.
Upper extremity manipulation reduced COP to a
greater extent (mean difference = – 7.14 cm; 95% CI, –
10.80 to – 3.47) than lower extremity manipulation
(mean difference = – 2.83 cm; 95% CI, – 5.22 to – 0.43).
No main effect of vision was found (F(1,22) = 0.05, p =
0.82), and there was no interaction of vision and manipulation
(F(1,22) = 0.15, p = 0.70).
Table 2
|
There was also a main effect of manipulation for ML
RMS, F(1,22) = 5.28, p = 0.032, ηp2 = 0.19. Mean premanipulation values were larger than post manipulation
values for lower extremity manipulations, hence lower
extremity manipulations reduced COP RMS (mean difference
= – 0.25 cm; 95% CI, – 0.52 to 0.01). Mean premanipulation
values were less than post manipulation values for the upper extremity and thus increased COP RMS (mean difference = 0.29 cm; 95% CI, – 0.054 to 0.62). No main effect of vision was found (F(1,22) = 1.31, p = 0.27), and there was no interaction of vision and manipulation either, (F(1,22) = 0.03 p = 0.87). See Table 2 for mean change scores and standard deviations for ML
force plate measurements.
The main effect of manipulation was not significant
for range F(1,22) = 3.38, p = 0.08 or SampEn F(1,22) =
3.12, p = 0.09. The main effect of vision was not significant
for range F(1,22) = 0.05, p = 0.82 or SampEn F(1,
22) = 0.04, p = 0.84. No significant main effects or interactions were found for the range (F(1,22) = 0.48, p =
0.50), or SampEn (F(1,22) = 0.00, p = 0.99) dependent
measures involving ML sway on the force plate.
Discussion
Participants in this study were asked to simultaneously
perform a postural and suprapostural dual task immediately
before and immediately after receiving either a
lower or upper extremity manipulation. Both upper- and
lower-extremity manipulation influenced dual task performance
as compared to initial testing. Lower extremity
manipulation with eyes open significantly reduced tube
motion as assessed by roll pathlength, range and RMS,
whereas both upper and lower extremity manipulation
reduced COP movement on a force plate as assessed by
ML postural sway. SampEn, a measure of movement
structure and periodicity, provided no further insight
into tube roll or postural sway, in contrast to our expectations
from previous work.
Research on spinal manipulation has shown changes
in volitional muscle activity [9], voluntary range of motion [20], biomechanical and structural changes [21],
complex whole-body motor response task [22], movement
time [23] and joint position sense. [24] As their effects
extend beyond the local anatomical area of
manipulation, it has been postulated that these changes
may be driven by downstream cortical stimulation rather
than spinal or local influences. [25] Similarly, in this
study, we found that chiropractic manipulation of the
extremities influenced both upper and lower extremitybased
task performance.
In this study, participants’ performance on the tube
balancing task was modulated by an interaction between
lower extremity manipulation and the participants’ visual
condition. In the eyes open condition, lower extremity
manipulation led to decreased values of tube roll parameters,
indicating enhanced stability. The importance of
visual information to joint manipulative effects is inherently
pragmatic/useful, as most chiropractic patients are
utilizing visual information throughout their daily activities;
however, it is still not known how the central nervous
system combines relevant somatosensory and
visual information for such control. One possibility may
be that (“noninformative”) vision improves haptic perceptions
of peripersonal space. [13] More work is
needed to better understand the relationship between
manipulation and vision.
The interplay between the visual and somatosensory
systems has been elicited in many postural studies, particularly
in work concerning muscle and tendon vibration.
Mancheva et al. [26] found that motor evoked
potentials from transcranial magnetic stimulation during
tendon vibration varied depending on whether subjects’
eyes were open or closed. [26] Lackner and Levine [27]
showed simultaneous vibration of the neck and Achilles
tendons could induce nystagmoid eye movements and
Bove et al. [28] found that vibration over postural muscles
could alter proprioceptive integration, leading to
changes in body tilt and rotation. [27, 28] From our
findings, we propose that joint manipulation of the extremities
may stimulate the same primary and secondary
afferents stimulated by muscular and tendon vibration
and that these changes in somatosensation can facilitate
cortical changes and alter motor outputs. [25, 29–31]
According to Pacheco et al. [32] in the ecological theory
of perception and action, enhanced stability (e.g.
tube stabilization) occurs from the attunement of the
perceptual systems to task dynamics together with modifications
of action as task and intrinsic dynamics cooperate
and/or compete. Chiropractic manipulation may
then modulate the properties of the perceptual-motor
workspace of participants. The prevailing thought on the
neurophysiological impact of spinal/extremity manipulation
is one of perceptual attunement brought about by
mechanisms related to greater afferentation by peripheral
receptors [33–35]; however, our consistent interaction
effects suggest the modulation of visual
perception may also be a possibility. Furthermore, the
action capabilities of the participant are likely promoted
by enhanced neural drive through supraspinal, spinal or
extremity-based mechanisms. [25, 36, 37]
As described in the introduction, previous work by this
team found that ipsilateral upper and lower extremity
manipulations affected participant performance during a
lower extremity balance task (standing on a rocker
board). [11] In that study, both upper and lower extremity
manipulations led to decreased pathlength as measured
on a rocker board. While participants in the
current study stood on a force plate (rather than a
rocker board), again, both upper and lower extremity
manipulation led to decreased ML pathlength (in this
case COP pathlength). This is particularly interesting as
this effect is found irrespective of whether the manipulations
involved a single limb (previous study) or both
limbs (current study). While comparing the magnitudes
of single vs bilateral limb manipulation effects would be
overly speculative given the differences between the two
studies, this is an interesting question that could be addressed
in future studies.
It is important to note that we did not capture the segmental
(or multi-segmental) strategies used by participants
in this study. Collecting such data may be able to
resolve why contrary to our hypothesis, upper extremity
manipulation had no effect on tube stabilization, but did
reduce ML postural sway. Such information would also
likely explain why lower extremity manipulation consistently
aided tube stability. Despite the opacity of strategies
utilized, participant performance is still consistent
with an ecological model; joint manipulation afforded
participants greater stability during dual task performance.
We suggest that further research is necessary to
understand how extremity manipulations afforded the
aforementioned improvement in performance. Nonetheless,
we feel these results are exciting as they represent
some of the initial steps in understanding a non-invasive
means of potentially altering an individual’s sensory integrative state. As manual therapy, including extremity
manipulation, may have a role to play in improving postural
stability [38], we feel this work could lead to new
and beneficial therapies aimed at preserving movement
and coordination, and mitigating falls and fall risk in affected
populations.
While these results are novel, they require replication.
This study is also limited in that it examined only
healthy, asymptomatic, adult participants. While many
interesting effects can become more pronounced in clinical
populations, many effects can also disappear entirely.
These results do not currently, and may not necessarily
generalize beyond a healthy, asymptomatic population.
Future work should investigate these effects in special
populations, and, particularly, the elderly, where balance
and falls are major factors in injury and loss of independence.
We also did not examine the effects of chiropractic
manipulation beyond an immediate (less than 2
min) time frame. Future research should investigate the
temporal effects of extremity manipulation on dual task
performance beyond an immediate time frame. It is also
possible that manipulation applied to different joints can
elicit individual responses of potentially differing
magnitudes. In this study, the order of manipulation (by
series) was also kept constant. Future work should investigate
any potential differences in the order and location
of selected manipulations.
Conclusion
Joint manipulations of the upper and lower extremities
enhanced stability across a postural / suprapostural dual
task in the presence of visual information. Extremity manipulations
also appear to influence motor behavior beyond
the local anatomical area of the joint being
manipulated. These results suggest that a centrally integrative
mechanism – similar to that of spinal manipulation
– is also present with manipulation of the extremity
joints. The length of time that these changes last, however,
is unclear beyond an immediate effect.
Abbreviations
IMU: Inertial Measurement Unit; SD: Standard Deviation; ML: Medial to lateral;
SampEn: Sample Entropy; COP: Center of Pressure; Pathlength: Path Length;
RMS: Root Mean SquareANOVAAnalysis of Variance
Acknowledgements
The authors would like to thank Dr. Mike Raper, Dr. Jordan Palmer and Dr.
Frank Lopez for their assistance in data collection.
Authors’ contributions
CM, DS, JH and KP conceived the study. CM, DS, JH and KP designed, coordinated the study and drafted the manuscript.
CM, DS, JH and KP were
involved in the study-implementation, CM, DS, JH and KP performed the
data analysis.
CM, DS, JH and KP interpreted the findings.
All authors read and revised the manuscript critically and approved the final manuscript.
Funding
No funding was obtained for this study.
Ethics approval and consent to participate
Ethical approval to conduct this study was granted by the Institutional Review Board at Parker University (#A-00186). Written informed consent was obtained from each participant prior to the start of experimental procedures.
Competing interests
The authors declare that they have no competing interests.
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