The Biology of Manual Therapies

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BRIEF REPORT

The Biology of Manual Therapies


Brian C. Clark, PhD; James S. Thomas, PT, PhD; Stevan A. Walkowski, DO; and John N. Howell, PhD

Each year, more than 18 million adults in the United


States receive manual therapies, at a total annual out-of-
pocket cost of $3.9 billion. Although there is growing
M any scientists and clinicians have postulated that
manual therapies exert biologic effects on the
nervous system.1-16 It has been hypothesized that manual
evidence supporting the efficacy of manual therapies, therapies act mechanistically to disrupt the pain-spasm-
little is known about the mechanisms underlying these pain cycle.9,17 In brief, the conceptual basis for this cycle is
treatments. This lack of basic knowledge significantly that pain leads to muscular hyperactivity (spasm), which
limits the development of rational strategies for the use in turn causes or exacerbates pain (see Pain-Spasm-Pain
of these treatments and potentially hinders their accept- Cycle).18 Although 2 distinct neural pathways have been
ance by the wider scientific and health care communities. proposed to support this model,19 each pathway operates
Many authors have hypothesized that manual therapies on the basis of the same concept, namely, that increased
act by disrupting the pain-spasm-pain cycle, but relatively excitatory input to the -motoneuron pool leads to more
little experimental evidence has supported this hypoth- sustained and intense muscle activity. More than 3 decades
esis. The authors have tested this hypothesis and sum- ago, Korr7 hypothesized that manual therapies act to dis-
marize their work on the biology of manual therapies. rupt the pain-spasm-pain cycle by reducing the excitability
J Am Osteopath Assoc. 2012;112(9):617-629 of the monosynaptic stretch reflex (also known as myotatic
reflex, deep tendon reflex, or muscle spindle reflex). How-
ever, relatively few studies have quantified the effects of
manual therapies on muscle activity20-24 or stretch reflex
excitability in humans,4,25-28 and thus, there are still limited
empirical data describing the effects and consequences of
manual therapies.
Our work has focused on the mechanistic effects of
manual therapies. The studies profiled here tested the
hypothesis that manual therapies act to disrupt the pain-
spasm-pain cycle. In this article, we review our latest work
on the biology of manual therapies. We will briefly review
the anatomy and physiology of muscle spindles, then dis-
cuss the pain-spasm-pain cycle, and finally present the
findings from these studies, providing our perspectives
on key questions to be addressed in future research.
From the Ohio Musculoskeletal and Neurological Institute (Drs Clark, Thomas,
Walkowski, and Howell), the Department of Biomedical Sciences (Drs Clark,
Thomas, and Howell), the Department of Family Medicine (Dr Walkowski), Muscle Spindles
and the School of Rehabilitation and Communication Sciences (Dr Thomas) The scientific knowledge and understanding of human
at Ohio University in Athens. muscle and nerve physiology has grown exponentially
Dr Clark delivered a presentation highlighting these findings at The
Osteopathic Research Centers 10th annual conference, Using Manual and during the past several decades with the advent of non-
Conventional Therapies to Enhance Musculoskeletal Health, which was held invasive methodologies to study in vivo characteristics.
April 27 through April 29, 2012, in Fort Worth, Texas. For example, at the start of the 20th century, the classic
Financial Disclosures: None of the authors have any potential conflicts
to disclose related to the opinions of data in the current study. The work works by Hoffmann29 describing the Hoffmann reflex (H-
presented in this article was supported by grants from the Osteopathic Her- reflex) and by Liddell and Sherrington30 describing the
itage Foundations and the American Osteopathic Association. stretch reflex led to a plethora of studies that expanded
Address correspondence to Brian Clark, PhD, Ohio University, OMNI and
Department of Biomedical Sciences, 236 Irvine Hall, Athens, OH 45701. our understanding of spinal and muscle reflex properties.
E-mail: [email protected] Today, the term sensorimotor control highlights the
inseparable coupling that exists between proprioceptive
Submitted July 15, 2012; revision received August 6, 2012; accepted August
8, 2012. sensory feedback and motor command. Sensory input

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BRIEF REPORT

arises from a variety of sources, and one key input to spinal and the static nuclear bag fibers transmit only information
and cortical processing of sensory information arises from about muscle length.36 The excitability of the muscle spin-
the muscle spindles, which is easily demonstrable by the dles is regulated by the activity of -motoneurons.36 When
illusions of movement that are created when the activity -motoneurons fire, they cause the intrafusal muscle fibers
of these sensors are manipulated.31-33 Figure 1 illustrates to contract, which makes the muscle spindle more taut
the key anatomic features and neuropathways of muscle and in turn increases the overall excitability of the spindle
spindles. Additionally, we refer the reader to the Web site (ie, increases the afferent discharge rate).
maintained by Arthur Prochazka, PhD, of the University
of Alberta for an interactive model explaining muscle Pain-Spasm-Pain Cycle
spindle behavior: http://www.angeltear.com/spindle The pain-spasm-pain cycle is the concept whereby pain
/spindle.html. leads to muscular hyperactivity (spasm), which in turn
Muscle spindles relay sensory information on the causes or exacerbates pain.18 The theoretical rationale for
length of and changes in the length of a muscle.34,35 Muscle the pain-spasm-pain cycle is illustrated in Figure 2. Two
spindles are collections of specialized muscle fibers (ie, potential neural pathways have been posited as the basis
intrafusal muscle fibers) that are not part of the high-force of the pain-spasm-pain cycle.19 In one of the proposed
producing muscle mass itself (ie, extrafusal muscle fibers pathways, nociceptive afferents directly transmit to exci-
that are innervated by -motoneurons).35 Although intra- tatory interneurons and then to -motoneurons, resulting
fusal fibers do not contribute substantially to the force pro- in increased muscle activation (spasm). In the other pro-
duced during muscle contraction, they do have contractile posed pathway, the muscle spindles serve as a key
elements at their ends that are innervated by -motoneu- anatomic structure involved in a feed-forward loop. The
rons.35 Muscle spindles reside parallel to extrafusal muscle loop begins when nociceptive fibers provide excitatory
fibers, stretching alongside these muscle fibers during both input to the -motoneurons that increase the sensitivity
active and passive movements. Muscle spindles contain of muscle spindles. This increased spindle sensitivity
nuclear chain and dynamic and static nuclear bag fibers, heightens spindle afferent activity and thus increases exci-
which have different shapes and convey different types tatory input to the -motoneurons, further increasing
of information.35 Group Ia afferents (primary afferents) muscle activation and pain.
have annulospiral endings that wrap around the central Numerous neurophysiologic studies have been con-
portion of all 3 types of intrafusal fibers and transmit infor- ducted to verify the existence of the pain-spasm-pain cycle
mation about both length and rate of length change.36 and the underlying neural pathways involved. A complete
Group II afferents (secondary afferents) have flower spray discussion of this evidence can be found in articles by van
endings that innervate the ends of the nuclear chain fibers, Dien et al19 and Knutson.6 The majority of these studies
examined whether nociceptive sub-
stances that increase the discharge
rate of the chemosensitive group III
and IV muscle afferents (eg, arachi-
Type II donic acid, bradykinin, lactate) also
Afferent increased the discharge rate of
Type Ia muscle spindle afferents. A series of
Afferent Intrafusal elegant studies37-43 conducted by sci-
Muscle Fibers entists at the Centre for Muscu-
loskeletal Research at Swedens
National Institute for Working Life
provided strong evidence that a wide
variety of nociceptive stimuli excite
-Motoneurons
Extrafusal muscle spindle afferents in animals.
Muscle Fibers For example, a series of articles from
Djupsjbacka et al37-39 from the mid-
-Motoneuron
1990s reported that injections of
arachidonic acid, lactic acid, potas-
sium chloride, and bradykinin
increased the firing rate of primary
and secondary muscle spindle affer-
Figure 1. Anatomic and neural pathways of the muscle spindle. ents in cats.37-39 A follow-up study41

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BRIEF REPORT

A B of the pain-spasm-pain cycle in certain


models and muscle groups, that evi-
dence is sometimes disputed.

The Biology of Manual Therapies


The series of studies summarized in the
following subsections tested whether
manual therapies acted to disrupt the
pain-spasm-pain cycle. The first of these
studies examined the acute effects of
strain-counterstrain treatment to mod-
ulate changes in the H- and stretch-
reflexes of the plantar flexor muscles in
patients with Achilles tendinitis.4 The
second study examined the effects of
osteopathic manipulative treatment
(OMT) to reduce resting muscle activity,
as assessed by means of muscle func-
Figure 2. Two theoretical neural pathways suggested as the basis tional magnetic resonance imaging (mfMRI) in patients
of the pain-spasm-pain cycle. In panel A, nociceptive afferents (N) with acute low back pain (LBP).21 For this study, the authors
transmit feedback via excitatory interneurons (E) to the -motoneu- hypothesized that if manual therapies truly acted to disrupt
rons () that cause increased muscle activation (spasm). In panel B,
nociceptive afferents (N) provide excitatory input on the -motoneu-
the pain-spasm-pain cycle, then one should observe a
rons () that increase the sensitivity of the muscle spindles (s), which reduction in resting muscle activity (ie, decreased resting
activate -motoneurons via excitatory interneurons (E) further muscle hyperactivity/spasm). The third study examined
increasing muscle activation and pain. Reprinted from van Dien et the effects of high-velocity, low-amplitude (HVLA) spinal
al19 with permission from Elsevier. manipulation on the amplitude of stretch reflexes and
motor evoked potentials (assessed by means of transcranial
magnetic stimulation) of the erector spinae muscles in
patients with chronic LBP.25 The most recent study,51 in
from this group found that an injection of bradykinin in 2012, focused on the effects of nonthrust manual therapies
combination with muscle stretch induces potent and long- (ie, treatment techniques that use a low-velocity, low-force
lasting excitatory effects on muscle spindle afferents, indi- approach) on the erector spinae short-latency stretch reflex.
cating that stretch-sensitive nerve endings are sensitized
by nociceptive stimuli. Interestingly, these data suggest Study 1. Stretch reflex and Hoffman reflex
that the nociceptive inputs are acting on the -efferent neu- responses to OMT in patients with Achilles
rons rather than acting directly on the muscle spindles, as tendinitis4
the effects were observed in homo- and heteronymous The purpose of this study was to determine if strain-coun-
muscles, including contralateral muscles.38,41 Conversely, terstain manual therapy reduced the sensitivity of the
other studies of animals report no change in muscle spindle short-latency (ie, monosynaptic) stretch reflex or the H-
afferent activity in response to nociceptive stimuli.44-46 reflex. The stretch reflex, a rapid excitatory response of a
Data on the existence of the pain-spasm-pain cycle in muscle following stretch, is a complex muscle reaction
humans are also conflicting. For instance, Matre et al8 consisting of multiple excitatory responses occurring at
reported that a 5% hypertonic saline infusion to the soleus different latencies following muscle stretch, with the short-
and tibialis anterior muscles (experimentally inducing latency response being an involuntary (re)action that
muscle pain) increased stretch reflex in the painful muscles. occurs in a matter of milliseconds following muscle stretch
Similar observations, at least in resting muscles, have also (eg, the latency time for a biceps brachii reflex is approxi-
been reported by others.47,48 However, Zedka et al49 observed mately 20 milliseconds following the onset of stretch).52,53
that a hypertonic saline infusion into the human lumbar The neural pathway mediating the short-latency stretch
erector spinae muscles did not modulate the stretch reflex reflex consists primarily of a pathway with a single synapse
in the back muscles, and Birznieks et al50 observed that in the spinal cord separating the Ia-afferent fiber from the
experimental muscle pain did not influence muscle spindle homonymous -motoneuron.30,54,55 The H-reflex, which is
afferent activity recorded by means of microneurography. elicited by electrical stimulation of a peripheral nerve, acti-
Thus, although there is clear evidence supporting existence vates the Ia-afferent nerve fibers from the muscle spindles

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BRIEF REPORT

to produce a reflex contraction (Figure 3).56,57 Howell et al4 Table, revealed that the strain-counterstrain treatment pro-
state the following: duced a 23.1% decrease in the amplitude of the stretch
reflex of the soleus (P<.05) in patients with Achilles ten-
The H-reflex is similar to the stretch reflex except for the fact dinitis. Similarly significant responses were observed in
that the H-reflex bypasses these muscle spindles, which serve the stretch reflexes of the lateral and medial heads of the
to initiate the stretch reflex.58 Because the H-reflex bypasses gastrocnemius muscles. The treatment did not alter the
the spindles, it cannot be modulated by the gamma efferent H-reflex. Additionally, subjective ratings of symptom
system, which modulates the stretch reflex.59 If an experi- severity (ie, soreness, stiffness, and swelling) were lower
mental or clinical intervention alters the stretch reflex, but following treatment. In control participants, neither reflex
not the H-reflex, alteration of spindle sensitivity is generally
was significantly affected by sham manipulative treatment.
suggested, whereas if an intervention alters both reflexes,
the mechanism is more likely to relate either to altered [-
In summary, the results of this study4 indicated that
motoneuron] excitability or to altered presynaptic inhibition the amplitude of the stretch reflex in patients with Achilles
at Ia afferent fiber endings on the [-motorneurons]. With tendinitis decreased after strain-counterstrain manual
this stated the idea that the stretch reflex and H-reflex are therapy. This finding suggests that a single strain-coun-
identical, except for the participation of the spindles, has terstain treatment reduces the excitability of the stretch
been in retreat in recent years. reflex, which the authors postulated was because of the
treatment decreasing nociceptor activity and subsequently
In this study,4 the authors quantified the amplitude of the decreasing the excitability of -motoneurons. Theoretically,
short-latency stretch reflex and H-reflex in the triceps surae a reduction in the overall excitability of the stretch reflex
muscles (ie, the soleus together with the lateral and medial could lead to a reduced level of involuntary muscle activity.
heads of the gastrocnemius) in 16 patients with Achilles Indeed, the basic tenet of the pain-spasm-pain model is
tendinitis both before and after a single strain-counterstrain that pain will result in more sustained and increased
session. Additionally, these measurements were also made muscle activation.19 Here, the pain-spasm-pain model pre-
in 15 asymptomatic control participants before and after dicts that muscle activity levels will be high during sub-
sham manipulative treatment. The results, detailed in the maximal tasks and under resting conditions. As such, the
authors of a follow-up study21 (see study
2) sought to address this issue. Studies
14 and 4,51 however, focused on identi-
fying the mechanisms of manual ther-
apies in the context of LBP. The key
EMG Amplifier
Stimulator rationale for shifting focus to the mech-
-Motoneuron anisms of manual therapies in LBP were
as follows:
Sensory
Ia-Afferent Axone 1. Low back pain is clinically signifi-
2
3 cant. One of the most common rea-
EMG Recording sons for seeking medical care, LBP
Electrodes 1
Spinal Cord
accounts for more than 3.7 million
1
Stimulus physician visits each year in the
-Motoneuron Axone Electrode United States. Ninety percent of
adults will experience LBP in their
Muscle
lifetime, 50% will experience recurrent
LBP, and 10% will develop chronic
pain and related disability.60-63
2. Low back pain is the most common
Figure 3. Schematic illustration of the Hoffmann-reflex (H-reflex) neural pathway. When reson for seeking manual therapies.
the peripheral nerve is electrically stimulated (1), action potentials are elicited selectively According to a 2007 national survey,
in the axones of the sensory Ia afferents because of their large axone diameter (2). The more than 18 million US adults aged
evoked action potentials propagate to the spinal cord, where they give rise to excitatory
postsynaptic potentials, in turn eliciting action potentials that travel in the -motoneuron
18 years or older received manual
axones toward the muscle (3). Subsequently, following a brief latency, the volley of afferent therapies in 2007, at a total annual
action potentials is recorded in the muscle as an H-reflex. Abbreviation: EMG, electromyo- out-of-pocket cost of $3.9 billion.64
gram. Reprinted from Aagaard et al57 with permission from The American Physiological The most common reason for seeking
Society. these treatments was LBP.64

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BRIEF REPORT

3. Manual therapies are effective in Table.


reducing LBP and disability. During Normalized Stretch Reflex and H-Reflex Amplitudes
the past decade, there has been for Triceps Surae Muscles in Patients With Achilles Tendinitis Before and After
growing scientific evidence supporting a Single Strain-Counterstrain Manual Therapy Treatment (n=16)
the clinical effectiveness of manual Stretch Reflexa H-Reflexa
therapies for LBP.65-72 Muscle Before After Change, % b
Before After Change, %
Soleus 0.078 0.062 -23.08 0.500 0.485 -3.17
Moreover, the pain-spasm-pain cycle has
M. gastrocnemius 0.043 0.036 -18.30 0.278 0.261 6.43
been postulated in the etiologic process L. gastrocnemius 0.025 0.019 -25.73 0.185 0.168 -9.31
of LBP,19 and as such, we believe that LBP
not only serves as a great model to study a
The respective reflex values were expressed as the ratio of measured reflex amplitude relative to
the mechanistic effects of manual thera- the maximum M-wave amplitude evoked by means of supramaximal electrical stimulation in the
same subject.
pies, but also that understanding the b
Significant differences between pre-treatment and post-treatment stretch reflexes were noted for
mechanisms in the context of LBP will all 3 muscles (P.05). No significant differences were noted between pretreatment and post-
treatment H-reflexes.
inform and impact the way practitioners
use manual therapies in clinical practice. Abbreviations: H-reflex, Hoffmann-reflex; M. gastrocnemius, medial gastrocnemius; L. gastrocnemius,
lateral gastrocnemius.

Study 2. Muscle functional magnetic


resonance imaging and acute LBP21 scale, 3.02 [2.81]) and 9 age- and sex-matched asymptomatic
21
In this study, Clark et al sought to determine whether controls participated in this study. All participants under-
patients with acute LBP exhibited differences in their levels went MRI, and subsequently the patients with LBP received
of resting trunk muscle activity compared with healthy, a single session of OMT and then underwent another MRI.
asymptomatic controls. The authors also sought to deter- The LBP participants reported back for an additional MRI
mine if a single treatment session of OMT alters the level 48 hours following their initial visit. The MRI data were
of resting muscle activity. They wrote the following21: used to calculate T2 and T2 asymmetry (ie, side-to-side
differences) as an index of muscle activity from regions of
Numerous studies have utilized electromyography (EMG), interest in the psoas, quadratus lumborum, multifidus,
mainly surface EMG, to examine whether patients with LBP and iliocostalis lumborum/longissimus thoracis muscles.
exhibit differences in their muscle activation patterns under Results indicated that there were no differences between
resting conditions, with the majority not observing differences the LBP patients and healthy controls when T2 was aver-
between patients with LBP and controls,73-77 although some aged for the left- and right-sided muscles. However, the
have observed differences.78 Unfortunately, technical limita-
quadratus lumborum muscle showed a significantly greater
tions of surface EMG, such as the attenuation in the myo-
electric signal attributed to subcutaneous tissue and
mean (SD) T2 asymmetry in patients with acute LBP com-
crosstalk among muscleshave limited the ability to precisely pared with controls (29.1% [4.3%] vs 15.9% [4.1%]; P=.05)
quantify and localize the muscle activity of specific lumbar (Figure 4). The psoas muscle also displayed a relatively
muscles.79,80 [MRI], on the other hand, possesses outstanding large, albeit nonsignificant, mean difference (22.7% [6.9%]
spatial resolution that allows for the investigation of individual vs 9.5% [2.8%]; P=.11). In the patients with LBP, psoas T2
muscles. Muscle functional MRI allows noninvasive meas- asymmetry was significantly reduced immediately after
urement of the metabolic and hemodynamic responses of the OMT (25.3% [6.9%] to 6.1% [1.8%], P=.05) (Figure 4),
skeletal muscle by observing changes in the contrast prop- and the change in pain immediately following treatment
erties of certain MR images that occur in skeletal muscle was correlated with the change in psoas T2 asymmetry
with activity.81-83 Specifically, mfMRI measures the transverse (r=0.75, P=.02). The side exhibiting the greater baseline T2
relaxation time (T2) of skeletal muscle protons and allows
value exhibited the greatest reduction in T2 activity, whereas
for determination of the spatial pattern of muscle activa-
tion.81-83 Muscle activity has been shown to increase T2, with
the side with the lower baseline T2 value seemed to increase
T2 changes within a muscle being sensitive to as few as 2 slightly. In Figure 5, 3 MRI images illustrate the differences
repetitions of resistance exercise84 and strongly related to the in T2 asymmetry patterns between a healthy control patient
magnitude of isometric torque produced by skeletal muscle.85 and a patient with LBP, including the changes following
OMT.
Accordingly, the authors used mfMRI to gain insight into In summary, the authors observed that OMT decreased
whether manual therapies affect resting activation patterns T2 asymmetry with the most notable reduction occurring
of the trunk muscles. in the psoas muscle. Additionally, the side with the higher
Nine patients with nonspecific acute LBP (mean [stan- T2 at baseline was reduced following treatment, and the
dard deviation (SD)] score on a 0 to 10point visual analog normalization of the T2 asymmetry was associated with

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BRIEF REPORT

reduced pain. It has long been postulated that the mech- ment techniquessuch as transcranial magnetic stimulation
anism(s) of manual therapies are related to an attenuation (TMS) to elicit motor evoked potentials (MEP)3,86-88 and
of the excitability of the muscle spindle afferents that mechanically elicited stretch reflexes50,86,87have begun to
reduces reflexive contractile activity.4,7 Thus, while these be applied to the study of the human lumbar musculature.
data alone do not provide insight into specific neurologic
mechanisms of manual therapies, they do suggest that in We previously demonstrated the reliability and stability
patients with acute LBP, manual therapies may function of these measures serially.86 The authors used these neu-
to normalize psoas muscle activity by reducing the activity rophysiologic techniques to determine the effects of a single
in the hyperactive side and presumably disrupt the pain- HVLA spinal manipulation thrust on corticospinal and
spasm-pain cycle. The 2 most recent studies25,51 in this stretch reflex excitability in patients with chronic LBP and
series (see studies 3 and 4) expanded on these findings by healthy participants. Further, the authors stated the fol-
trying to identify the neurophysiologic effects of 2 different lowing25:
types of manual therapies (ie, thrust-based and nonthrust-
based manual therapies) on the erector spinae muscles. In addition to determining whether the MEP and stretch
reflex amplitude were different in individuals with and
Study 3. Neurophysiologic effects of spinal without LBP, we also examined whether these physiologic
manipulation in patients with chronic LBP25 responses depended on whether the HVLA spinal manipu-
lation caused an audible sound from the joint (ie, the pop or
In this study,25 the authors examined the neurophysiologic
cracking sound that one often associates with joint manipu-
effects of a single HVLA spinal manipulation thrust to
lations). The role of the audible response in determining
determine whether these physiologic responses were treatment effects has long been a matter of intense debate.
dependent on HVLA spinal manipulation causing an Some studies have previously reported that an audible
audible joint sound. They wrote as follows25: response is not necessary to improve clinical outcomes.89,90

The scientific understanding of the neurophysiologic char-


acteristics of the human low back muscles has historically Some have reported that biomechanical effects (eg,
been hindered by the lack of experimental techniques to increased joint laxity, motion, and gapping) are contingent
examine these muscles function in vivo. However, in recent on manipulation resulting in an audible sound.91,92 To date,
years innovative advancements in neurophysiologic assess- however, few studies have investigated whether the phys-

40

35

Figure 4. Changes in transverse relaxation time


Side-to-Side Difference, %

30 (T2) asymmetry in patients with acute low back


pain after a single osteopathic manipulative
25 treatment (OMT) session. Data were obtained
before treatment (baseline), immediately after
20
c OMT, and 48 hours after OMT. Value of T2
asymmetry was calculated as the absolute value
of the percent difference in magnetic reso-
15 nance imagingderived T2 between the left-
b and right-sided muscles. Immediately after
10 OMT, the T2 asymmetry in the psoas muscle
a
d was reduced, but it returned to baseline levels
5
f after 48 hours, although a modest effect size
e
was still observed. Conversely, 48 hours after
OMT, a small but significant increase in multi-
0 fidus T2 asymmetry was observed. The quad-
Baseline

Post-OMT

Post-OMT (48 h)

Baseline

Post-OMT

Post-OMT (48 h)

Baseline

Post-OMT

Post-OMT (48 h)

Baseline

Post-OMT

Post-OMT (48 h)

ratus lumborum and iliocostalis/longissimus


muscles exhibited modest effect sizes for
reduced T2 asymmetry associated with OMT,
although these differences failed to reach sta-
tistical significance. aP=.05, 2=0.42. bP=.06,
Psoas Quadratus Iliocostalis/ Multifidus 2=0.41. cP=.23, 2=0.19. dP=.27, 2=0.17. eP=.15,
Lumborum Longissimus 2=0.19. fP=.01, 2=0.67. Reprinted from Clark
et al.21

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BRIEF REPORT

Figure 5. Transaxial magnetic resonance images of a 69-year-old


A woman without back pain (A) and a 69-year-old woman with acute
low back pain before (B) and immediately after (C) osteopathic
Psoas manipulative treatment. These images of the L3-L4 region illustrate
the spatial orientation of the psoas, quadratus lumborum, iliocostalis
Quadratus lumborum/longissimus thoracis, and multifidus muscles. Ten-mil-
Lumborum limeter thick transaxial images were obtained from the lumbar
region with a 2000-millisecond repetition time, 30-millisecond and
Iliocostalis/ 65-millisecond echo times, and a 10-mm slice-to-slice interval. These
Longissimus
derived images were used to calculate the transverse relaxation
Multifidus time (T2) and allow for a noninvasive measurement of the metabolic
and hemodynamic responses of skeletal muscle in association with
muscle activity. Note the similar signal intensity in the left and right
lumbar muscles of the control subject (A), the asymmetry in the
B psoas and quadratus lumborum muscles before treatment (B), and
the attenuation of this asymmetry immediately after treatment (C).
Reprinted from Clark et al.21

duced an audible response (regardless of whether they


had LBP) exhibited a 20% decrease in the stretch reflex
but no change in the MEP amplitude (Figure 8).
In summary, the authors observed that a single HVLA
C spinal manipulation treatment did not systematically alter
MEP or short-latency stretch reflex amplitude of the erector
spinae muscles in patients with chronic LBP or asympto-
matic controls, at least when assessed approximately 10
minutes after treatment. However, when the authors looked
at the data regarding whether HVLA spinal manipulation
caused an audible joint sound, they observed that study
participants exhibiting an audible response exhibited a
substantial reduction in the short-latency stretch reflex
regardless of patient group. This finding provides further
insight into the mechanisms of action of manual therapies
and suggests that in certain cases they act by down-regu-
iologic response is dependent on the manipulation causing lating the excitability of the muscle spindles or the various
an audible joint sound. segmental sites of the Ia-reflex pathway. The follow-up
Ten patients with chronic LBPdefined by usual investigation51 (study 4) focused on examining the effects
rating of mean (SD) 4.0 (1.2) on a 0 to 10 visual analog of nonthrust manual therapy on changes in the short-
scaleand 10 age-, sex-, and body mass indexmatched latency stretch reflex.
asymptomatic control participants were enrolled in this
study. The effects of a single HVLA spinal manipulation Study 4. Nonthrust manual therapy reduces erector
thrust on MEP and short-latency stretch reflex amplitude spinae short-latency stretch reflex asymmetries in
of the erector spinae muscles were assessed before and patients with chronic LBP51
approximately 10 minutes after treatment (Figure 6 and The purpose of this study51 was to determine if nonthrust
Figure 7). The results, expressed as mean (SD), indicated manual therapy attenuates the short-latency stretch reflex
that HVLA spinal manipulation did not alter the erector of the erector spinae muscles in patients with chronic
spinae MEP amplitude in patients with chronic LBP (0.80 LBP. Nine subjects with chronic LBPdefined by usual
[0.33] to 0.80 [0.30] V) or in asymptomatic controls (0.56 LBP rating of mean (SD) 3.7 (0.5) on a 0 to 10point visual
[0.09] to 0.57 [0.06] V). Similarly, HVLA spinal manipu- analog scaleparticipated in this study. The effects of a
lation did not alter the erector spinae stretch reflex ampli- single session of nonthrust manual therapy on the short-
tude in patients with chronic LBP (0.66 [0.12] to 0.66 [0.15] latency stretch reflex amplitude were assessed before
V) or in asymptomatic controls (0.60 [0.09] to 0.55 [0.08] and approximately 10 minutes after treatment. The non-
V). Interestingly, study participants whose treatment pro- thrust manual therapy procedures consisted of a com-

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BRIEF REPORT

treatment), with the higher of the paraspinal sides


exhibiting a mean (SD) 100.2% (28.2%) greater value
than the lower side. After the nonthrust manual therapy,
Laser Pointer
stretch reflex asymmetry was reduced (100.2 [28.2%] to
36.6% [23.1%]; P=.03) (Figure 9). This change was largely
due to a reduced stretch reflex amplitude on the side
Double-Cone
that was higher at baseline (35% reduction following
Coil treatment; P=.05), whereas no change over time was
observed in the low side (P=.23) (Figure 10). Additionally,
there was no difference between the respective sides fol-
lowing the intervention (P=.38), indicating that the asym-
metry was normalized after treatment.
These findings provide insight into the mechanisms
of action of nonthrust manual therapy andas with the
aforementioned work on HVLA manual therapysuggest
SA that manual therapies in certain instances act by down-
regulating the excitability of the muscle spindles or the
various segmental sites of the Ia-reflex pathway. One lim-
itation of studies 3 and 4, which observed changes in
excitability for erector spinae stretch reflex was the inability
Figure 6. The experimental setup for performing transcranial mag-
netic stimulation to evoke motor-evoked potentials from the erector of the authors to distinguish changes in spindle sensitivity
spinae muscles. A representative motor potential recorded from the from the Ia-reflex pathway (as we described previously
erector spinae muscles is illustrated on the right. Abbreviation: SA, in the discussion relating to study 1).4 Unfortunately, the
stimulus artifact. Reprinted from Goss et al86 with permission from anatomy of the erector spinae muscles made it technically
Elsevier. difficult (if not impossible) to elicit readings of H-reflexes
from this muscle group. Unlike the case with the triceps
surae in study 1, the authors could not definitively identify
which anatomic substrate or segmental site was the source
bination of 3 common nonthrust-based techniques com- of observed changes. In the next section, we collectively
monly used to treat LBP: muscle energy, myofascial interpret the findings from the recent studies and provide
release, and strain-counterstrain. The results indicated our perspectives on key questions and issues that need to
that the patients with LBP exhibited a large asymmetry be addressed in the future to vertically advance our under-
in the short-latency stretch reflex at baseline (prior to standing and clinical use of manual therapies.

A B 140
Net tap force: 90 N
120
Tap rise time: 7.5 msec
Force, newtons

100

80
Figure 7. Depiction of the experimental
60
Pre-load: 30 N setup for evoking short-latency stretch
40
reflexes from the lumbar paraspinal mus-
20
cles. The tip of an electromechanical tap-
0
EMG
ping apparatus is gradually pressed into
Electrodes C SA
Short-Latency
the erector spinae tissue (A) until a pre-
Electromechanical
loaded force of 30 N is reached, after
65 V

Tapping Apparatus Stretch Reflex


which a rapid mechanical tap to the
6 msec muscle with a net force of 90 N is delivered
(B). A representative example of a short-
latency stretch reflex is then recorded from
the erector spinae muscles in response to
the mechanical tap (C). Abbreviations:
EMG, electromyogram; SA, stimulus arti-
fact. Reprinted from Goss et al86 with per-
mission from Elsevier.

624 JAOA Vol 112 No 9 September 2012 Clark et al Brief Report

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BRIEF REPORT

We postulate that manual therapies function, at least


Audible release
Change in Peak-to-Peak Amplitude, %

40 in part, by attenuating nociceptive input, which in turn


No audible release
30 reduces excitatory input to the -motoneurons, thereby
20 normalizing the excitability of the stretch reflex (Figure
10
11B). This decreased stretch reflex response, coupled with
the reduced nociceptive input, would lessen excitatory
0
input to the -motoneuron pool, ultimately decreasing
-10
muscle activity. Further, this series of events could also
-20 help to restore motion to affected tissues because the atten-
-30 uated stretch reflex response may lessen the likelihood or
-40
a severity of reflexive involuntary contractions that may
Motor-Evoked Potential Stretch Reflex occur with functional movements. Figure 11 pools data
from studies 1, 3, and 4 to support the notion that manual
Figure 8. Amplitudes of motor-evoked potential and stretch reflex therapies act to reduce the excitability of the muscle spindles
in patients with low back pain and asymptomatic patients under- (as we have observed by means of a consistent decrease
going spinal manipulation. High-velocity, low-amplitude spinal in the short-latency stretch reflex response). Data from
manipulation did not significantly alter the amplitude of the motor- study 2 show that manual therapies also reduce the activity
evoked potential recorded from the erector spinae muscles regardless of hyperactive skeletal muscles.
of whether spinal manipulation produced an audible response. Inter-
estingly, spinal manipulation significantly reduced the amplitude of Our conceptual model on the mechanisms of manual
the short-latency stretch reflex regardless of audible response. aTime therapies is far from complete, and further work is needed
group interaction; P<.05. Reprinted from Clark et al.25 to address several key questions. From a basic science
mechanistic perspective, there are several key questions
that need to be addressed, for example:

Conceptual Model on the Mechanisms of Manual Do manual therapies alter nociceptive processing and,
Therapies and Perspectives if so, in what way?
The series of studies summarized in this article provide Do manual therapies exert effects on higher brain centers
consistent evidence suggesting that a single manual therapy and, if so, in what way?
reduces the sensitivity of the muscle spindles to stretch. Do different types of manual therapies (eg, thrust-based
In Figure 11, we present our working conceptual model vs nonthrust-based) have different mechanistic actions
on the pain-spasm-pain cycle (Figure 11A), as well as an (eg, exert effects directly on muscle spindle sensitivity
integrated model where we postulate on how manual independent of nociceptive mediators)?
therapies act to disrupt the pain-spasm-pain cycle (Figure
11B). Specifically, in Figure 11A, we postulate that muscu- Answers to these questions would provide critical insight
loskeletal pain conditions (eg, LBP) are associated with on the biological effects of manual therapies. From a trans-
heightened levels of nociceptive input arising from dam-
aged tissues, such as skeletal muscle (eg, class III and IV 140
afferents), tendons, ligaments, bone, and annulus fibrosus.
We postulate that this increased nociceptive input increases 120
Side-to-Side Difference, %

excitatory input to the -motoneurons, which increases


100
the excitability of the muscle spindle and results in
increased muscle spindleafferent activity, particularly in 80
response to stretch or changes in muscle length. This height- a
60
ened level of muscle spindleafferent activity, along with
heightened level of nociceptive input, would theoretically 40
result in the pool of -motoneurons receiving greater exci-
tatory input. This increased level of excitatory input could 20

result in involuntary activation of -motoneurons and


0
muscle fibers (ie, spasm), or a greater probability of - Pretreatment Posttreatment
motoneurons discharging with lower levels of descending
supraspinal input (or excitatory input from any source). Figure 9. Rates of asymmetry in patients with low back pain (N=9)
Ultimately, the end-organ effect would increase muscle before and after nonthrust manual therapy. Treatment attenuated
activity, which could further exacerbate nociceptive input short-latency stretch reflex asymmetry in the erector spinae muscles.
a
and, in turn, the pain-spasm-pain cycle. P=.03. Reprinted from Goss et al52 with permission from Elsevier.

Clark et al Brief Report JAOA Vol 112 No 9 September 2012 625

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BRIEF REPORT
Figure 10. Short-latency stretch reflex reduc-
1.6
tions in patients with low back pain (N=9)
1.4 treated with nonthrust manual therapy. Treat-
ment affected the side with the higher stretch
1.2 reflex amplitude at baseline without affecting
a
the side with the lower stretch reflex amplitude
Amplitude, V

1 at baseline. aP=.05. Reprinted from Goss et al52


0.8
with permission from Elsevier.

0.6

0.4

0.2

0 Pre- Post- Pre- Post-


treatment treatment treatment treament
High-Side Stretch Reflex Low-Side Stretch Reflex

A
1. Musculoskeletal pain increases
nociceptive input 2. Excitatory input to -motoneuron pool
increases spindle sensitivity, leading to Figure 11. Conceptual model of the pain-spasm-
increased activity Ia-spindle afferents pain cycle (A) and conceptual model of manual
therapies disrupting the pain-spasm-pain cycle
Type II
Afferent (B). In panel A, musculoskeletal pain (eg, low back
pain) causes increased levels of nociceptive input
Type Ia when tissues such as muscles, tendons, or bones
Afferent Intrafusal
Muscle Fibers are damaged (1). The increased nociceptive input
transmits excitatory input to the -motoneurons
(2), which increases the excitability of muscle
spindle and muscle spindle afferents, particularly
in response to stretch or changes in muscle length.
-Motoneurons
Extrafusal Heightened levels of nociceptive input and
3. The -motoneuron pool receives Muscle Fibers
afferent activity would then transmit excitatory
excitatory input from nociceptors input to -motoneurons (3), resulting in involun-
and muscle-spindle afferents
-Motoneuron tary activation (ie, spasm) or involuntary discharge
of -motoneurons caused by lower levels of exci-
4. Increased excitatory input to -moto- tatory input from other sources (eg, descending
neuron pool results in increased muscle input) (4). Ultimately, the end-organ effect would
activity (spasm)
be increased muscle activity, which could further
exacerbate nociceptive input and, in turn, the
pain-spasm-pain cycle. In panel B, we postulate
B that manual therapies function by attenuating
1. Musculoskeletal pain increases nociceptive input (1), which in turn reduces exci-
nociceptive input 2. Excitatory input to -motoneuron pool is tatory input to the -motoneurons, thereby nor-
reduced, ultimately reducing muscle-spindle malizing the excitability of the stretch reflex (2).
(stretch) reflex excitability (studies 1, 3, and 4)
This decreased stretch reflex response, coupled
Type II
with the reduced nociceptive input, would result
Afferent in less excitatory input to -motorneuron pools
Manual
Therapies (3), ultimately decreasing muscle activity (4). Data
Type Ia
Afferent Intrafusal from studies 1, 3, and 4 support the theory that
Muscle Fibers manual therapies act to reduce the excitability
of the muscle spindles, and data from study 2
support the theory that manual therapies reduce
the hyperactivity of skeletal muscles.
-Motoneurons Extrafusal
Muscle Fibers
3. Excitatory input to -motoneuron
pool is reduced
-Motoneuron

4. Reduced excitatory input to -motoneuron pool


results in decreased muscle activity (study 2)

626 JAOA Vol 112 No 9 September 2012 Clark et al Brief Report

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BRIEF REPORT

lational science perspective, we still need to better define 14. Pickar JG, Sung PS, Kang YM, Ge W. Response of lumbar paraspinal muscles
spindles is greater to spinal manipulative loading compared with slower loading
and understand the timing of biological effects of manual under length control. Spine J. 2007;7(5):583-595.
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ments (eg, Do multiple treatments result in additive lative-like loads in the anesthetized cat. J Manipulative Physiol Ther. 2001;24(1):2-
effects?). Subsequent studies will, in the long term, assist 11.

in optimizing the frequency and duration of manual ther- 16. Sung PS, Kang YM, Pickar JG. Effect of spinal manipulation duration on low
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