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International Journal of Osteopathic Medicine (2014) xxx, xxxexxx

www.elsevier.com/ijos

RESEARCH REPORT

H-reflex responses to High-Velocity Low-


Amplitude manipulation in asymptomatic
adults
Sandro Groisman a,*, Luciano Silva a, Natalia Rocha a,
Fabrcia Hoff b, Ma
rcia Elisabeth Rodrigues a,
o Arthur Ehlers b, Leonardo Rios Diniz a
Joa

a
Brazilian Institute of Osteopathic, Rio de Janeiro, Brazil
b
Mae de Deus Hospital, Porto Alegre, Brazil

Received 15 May 2013; revised 28 March 2014; accepted 1 April 2014

KEYWORDS Abstract Background: High-Velocity Low-Amplitude (HVLA) manipulation of the


H-reflex; spine is a broadly used technique in Osteopathic Manipulative Treatment (OMT),
Osteopathic manipula- and studies have shown that spinal manipulation might lead to transient decrease
tion; in motoneuronal activity assessed through Hoffmann Reflex (H-reflex) test. Howev-
Osteopathic Manipula- er, its physiologic response is not fully understood, and there is no consensus on H-
tive Treatment (OMT); reflex responses to spinal manipulation.
Somatic dysfunction; Objective: The purpose is to assess motoneuron excitability by the H-reflex test
Spinal manipulation before and after HVLA manipulation of the lumbar spine of asymptomatic adults.
Design: Prospective controlled experimental study with pre and post-intervention
measures.
Methods: The participants were first submitted to a sacrolumbar (L5-S1) control inter-
vention and after an HVLA manipulation of the same vertebral segment. H-reflex am-
plitudes were measured before and after the procedures; the participants were
positioned lying on their left side and they did not change the position during the exper-
imental procedure.
Participants: Nineteen asymptomatic adults were recruited through public advertise-
ments and referrals from healthcare professionals.
Results: There was a variation of the H-reflex amplitude; but with no systematic
change across participants. Six out of 19 participants had a decrease on H-reflex
greater than 20% after the manipulation, and no significant change in 13 participants.
Conclusion: The results hypothesize that the electrophysiological effects of HVLA
manipulation have different results among participants, and that this variability may

alves Dias 603, apt 604 e Menino Deus, 90130-061 Porto Alegre, RS, Brazil.
* Corresponding author. Rua Gonc
E-mail address: sandrogroisman@gmail.com (S. Groisman).

http://dx.doi.org/10.1016/j.ijosm.2014.04.001
1746-0689/ 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Groisman S, et al., H-reflex responses to High-Velocity Low-Amplitude manipulation in
asymptomatic adults, International Journal of Osteopathic Medicine (2014), http://dx.doi.org/10.1016/j.ijosm.2014.04.001
2 S. Groisman et al.

be due to dysfunction at the level manipulated, changes in autonomic tone and/or


technical issues delivering the technique.
2014 Elsevier Ltd. All rights reserved.

demonstrated that spinal manipulation might


Implications for clinical practice normalize H-reflex responses.
Floman et al.16 investigated the H-reflex re-
 High velocity low amplitude manipulation is sponses in participants with L5-S1 unilateral disc
commonly used in daily practice to treat back herniation before and after lumbar spine manip-
pain. ulation in side-lying position. At pre-manipulation
 It is paramount to understand its physiological phase the H-reflex mean amplitude was signifi-
effects and how it affects the body. cantly lower on the side of disc herniation, and
 Our study shows evidence that the results of after lumbar manipulation the H-reflex increased
this type of manipulation are variable and this significantly on the affected side while the values
brings a need for new studies using appro- on the healthy side remained unchanged.17
priate samples to assess the effects of high These findings diverge from the study of Dish-
velocity low amplitude manipulation on so- man et al.18,19 who assessed the effects of spinal
matic and/or neurovegetative dysfunctions. manipulation on tibial nerve H-reflex recorded
 Understanding the mechanisms of how oste- from the gastrocnemius muscle in 17 healthy par-
opathic manipulative therapy works, when ticipants. They observed the suppression of
properly applied, should contribute to tech- motoneuron activity after lumbar (L5-S1) manipu-
nique selection and thus the potential to offer lation; but the experimental protocol involved
better treatment to our patients. changing the position of spinal manipulation and
H-reflex testing.18,19
Suter et al.17 investigated healthy participants
and patients with low back pain and observed no
significant changes in H-reflex amplitude in
Introduction healthy participants receiving manipulation to the
sacroiliac joint (SIJ) e with participants in the
High-Velocity Low-Amplitude (HVLA) manipula- same position, i.e., the participants were not
tion of the spine is a widely used technique in moved during the procedure. They concluded that
Osteopathic Manipulative Treatment (OMT) for H-reflex responses after SIJ manipulation are sen-
acute and chronic low-back pain.1e3 There is sitive to movement/repositioning, and that the H-
moderate evidence that spinal manipulation may reflex depression after manipulation documented
reduce pain and improve function in chronic and in previous studies were movement artifacts rather
acute low back pain in the short term when than treatment effects. However, participants
compared with sham spinal manipulation.4,5 with low back pain presented changes in motor
However, the therapeutic mechanisms are not neuron excitability after SIJ manipulation,
thoroughly understood.6 because the H-reflex amplitude response
The monosynaptic stretch reflex can play a decreased 20% after treatment compared with the
major role in motion restriction, and it had been measures before treatment. It is noteworthy that
suggested that OMT could restore range of motion the protocol used by Dishman et al.18 was L5-S1
by resetting the stretch receptor gain.7e10 manipulation and the protocol used by Suter
The H-reflex is an estimate of alpha moto- et al.17 was SIJ manipulation.
neuron (aMN) excitability and can be used to Dishman et al.18 reported the H-reflex attenu-
investigate whether an intervention such as spinal ation after L5-S1 spinal manipulation, where a
manipulation changes the H-reflex intensity by constant prone position was utilized during the
altering the monosynaptic reflex transmission whole experiment. Nevertheless they changed the
within the spinal cord.11,12 Studies show that direction of the applied force vectors when per-
patients with spinal cord injuries, and with acute forming the procedures. In a recent study Orakifar
or chronic low back dysfunction have altered H- et al.21 also demonstrated H-reflex attenuation
reflex responses when compared with healthy after SIJ manipulation, and they attributed it to
participants.13,14 Furthermore, Humphreys et al.15 inhibited Ia afferents discharge.

Please cite this article in press as: Groisman S, et al., H-reflex responses to High-Velocity Low-Amplitude manipulation in
asymptomatic adults, International Journal of Osteopathic Medicine (2014), http://dx.doi.org/10.1016/j.ijosm.2014.04.001
H-reflex responses to High-Velocity Low-Amplitude manipulation 3

Current literature shows controversial results electrode contact. Before attaching the recording
in the measurement of the H-reflex before and electrodes, the skin was shaved and cleansed with
after spinal manipulation, and this is mainly alcohol. The electrodes were placed approxi-
because of different methodologies. Therefore mately 2 cm to the distal end of the medial and
the present study intends to investigate H-reflex lateral gastrocnemius and superior to the Achilles
responses to HVLA manipulation of L5-S1 verte- tendon to measure the H-reflex response.22
bral segment in healthy participants, without The optimal stimulation voltage was individually
changes in the body position between spinal determined by performing stimulations of
manipulation and H-reflex measurement, i.e., the increasing intensity from 0 to 100 V in 2-volt in-
participants remained lying on their left side crements. The Hmax recruitment curve was
throughout the procedures. generated by increasing stimulus intensity until a
maximal H-wave and minimal M-wave response
was reached, where M-wave is the response of the
Methods muscle in relation to electric stimulation. Ten H-
reflex amplitude measurements were recorded
Participants before and after spinal manipulation and control
intervention.23
Healthy participants with no history of low back The EMG signal was bandpass filtered
pain within the last 3 months, no radiculopathy or (10 Hze10 kHz) and amplified using the Synergy N-
neuropathy of the lower limbs, or other musculo- EP Biolink EMG system. The evoked EMG responses
skeletal disorders were eligible to participate in were collected using an analog-to-digital con-
the study. They were recruited through public verter (12-bit resolution) interfaced to a computer
advertisements and referrals from healthcare and the sampling rate was 5 kHz per channel. The
professionals. All participants signed an informed deliverance of the peripheral nerve stimulus was
consent and the study was approved by the Medi- controlled through the computers digital output
cal Ethics Committee of the Ma e de Deus hospital port interface. The Synergy software was used for
under the number: 209/08. data acquisition and the EMG amplitudes of H-re-
Exclusion criteria: neoplasm, lower limbs sur- flex responses were detected and stored in a data
gery; manipulative treatment of the foot, ankle output file for statistical analysis.
and/or lumbar spine within the last 4 months. All Participants were asked not to talk and to keep
participants were submitted to neurological ex- their head, arms, and lower extremities relaxed
amination (dermatomes, muscle function and deep during the experimental to minimize changes in H-
tendon reflexes) to exclude participants with rad- reflex response because of muscle contraction,
iculopathy or peripheral neuropathy. change in joint position, or tonic reflexes. The
whole procedure lasted 10 min.
Experimental protocol
Spinal manipulation and control
The procedures were delivered with the partici- intervention
pants lying on their left side on a treatment table.
Every participant received the following protocol: Participants laid on their left side; the control
1) control intervention, 2) HVLA lumbar manipu- intervention was performed first and then the
lation of the right L5-S1 joint; and 3) measurement HVLA spinal manipulation. Both were performed
of H-reflex response before and after intervention. by a 5th year osteopathic medicine student. A
control intervention was performed by placing the
Measurement of the H-reflex hands on the right L5-S1 joint and taking up the
joint slack and no manipulative thrust was per-
H-reflex was measured in milivolts (mv) before and formed. For the High-Velocity Low-Amplitude
after the lumbar manipulation and control inter- (HVLA) manipulation, the clinician manually con-
vention using the standard methodology. To stim- tacted the tissues overlying the lumbar zyg-
ulate the tibial nerve, the electrical stimulator apophyseal joint, tension was increased with a
was placed on the participants skin centrally rotation force, pelvis and lumbar spine were
within the popliteal fossa between the biceps rotated towards the practitioner until motion was
femoris and semimembranosus tendons. Surface palpated at the L5-S1 segment. The participants
electrodes with a 1-cm active diameter were upper body was rotated away from the practi-
wrapped with an elastic bandage for better skin/ tioner until a sense of tension was palpated at the

Please cite this article in press as: Groisman S, et al., H-reflex responses to High-Velocity Low-Amplitude manipulation in
asymptomatic adults, International Journal of Osteopathic Medicine (2014), http://dx.doi.org/10.1016/j.ijosm.2014.04.001
4 S. Groisman et al.

Table 1 Characteristics of participants. Table 2 Data electroneurograph.


Total n 19 Hoffmann Pre Post p-Value
Age, years 31  5 reflex
Male sex 12 (63%) amplitude
Height, cm 174  6,5 Hmax, mV 2.8 (1.9e4.5) 2.5 (1.3e3.8) p 0.432
Weight, Kg 74  10 (LM)
Values in mean  SD or n (%). Hmax, mV 2.7 (1.9e3.5) 2.8 (1.5e4.1) p 0.752
(CI)
Hmax, mV 5.4 (3.5e7.0) 2.8 (2.2e4.5) p 0.002
L5-S1 segment; the leg of the participant during (PSD)
the procedure remained extended. The direction Abbreviations: Hmax, Maximun Hoffmann reflex amplitud;
of thrust was towards the table accompanied by Pre, pre lumbar manipulation; Post, post lumbar manipula-
pelvic rotation. The achievement of a cavitation tion; CI, control intervention; LM, lumbar manipulation;
was not recorded.24 PSD, participants showed a depression of the H-reflex.
Values in median (25th75th percentile). p-Values, com-
parisons by Wilcoxon signed rank test.
Data analysis

Data were analyzed using SPSS version 17.0, sta-


tistical software package. The dependent vari- percentage found by Suter et al.17 When these 6
ables were H-reflex expressed in milivolts (mv) participants were evaluated separately the H-re-
using median and percentile (25the75th). flex median amplitude (25the75th percentile)
The assumptions for the use of parametric sta- dropped from 5.4 mv (3.5e7.0) before manipula-
tistics were not satisfied for H-reflex average tion to 2.8 mv (2.2e4.5) after manipulation, with
amplitude, based on the analysis of skewness and statistical significance (p 0.002). Moreover, the
kurtosis to compare pre-intervention and post- same group of 6 participants showed no statisti-
intervention. Therefore, nonparametric analysis cally significant change before and after the con-
was necessary. The immediate changes (H-reflex trol intervention (Fig. 2).
response) before and after manipulation was
compared using median and the Wilcoxon test for
paired samples, with a significance level of 0.05. Discussion
The distribution of results are presented as median
and percentile (25the75th). Previous studies have shown an attenuation of the
H-reflex in healthy volunteers after HVLA manip-
ulation of the lumbosacral joint L5-S1, and the
Results authors attributed the results to a possible aMN
inhibition caused by zygapophyseal joint disten-
Data from one participant was excluded from the sion.25 The present study has demonstrated
analysis because it was not possible to acquire changes only in 6 out of 19 participants, and there
both M-wave and H-reflex data. Nineteen (19) was no randomization of the order of the in-
remaining participants were analyzed (12 males, terventions; because HVLA manipulation before
63.2%), the mean age was 30.8  5.5 years, weight the control intervention could modify the H-reflex
73.8  10.3 kg, height 171  6.5 cm (Table 1). response.
The median H-reflex of all 19 participants Indahl et al.,7 using a porcine model, reported
demonstrated no statistically significant changes that distension of the zygapophyseal joint by in-
after receiving lumbar manipulation. Table 2 jection of physiologic saline solution reduced the
shows the median results (25th75th percentile) amplitudes of motor unit action potentials recor-
before and after manipulation. Fig. 1 shows me- ded from the paraspinal musculature.
dian and percentile 25the75th of the H-reflex Based on these physiological effects, Dishman
amplitude before and after spinal manipulation et al. assessed H-reflex in healthy participants
and control intervention; there were no significant before and after L5-S1 manipulation and observed
differences. attenuation after manipulation.18 However, others
Six out of 19 participants showed a decrease authors did not observe H-reflex attenuation in
greater than 20% in the H-reflex amplitude imme- healthy participants receiving spinal manipulation
diately after manipulation e concurring with the when H-reflex testing and manipulation were

Please cite this article in press as: Groisman S, et al., H-reflex responses to High-Velocity Low-Amplitude manipulation in
asymptomatic adults, International Journal of Osteopathic Medicine (2014), http://dx.doi.org/10.1016/j.ijosm.2014.04.001
H-reflex responses to High-Velocity Low-Amplitude manipulation 5

Fig. 1 Changes in Hmax after the administration of a side-posture HLVA manipulation comparing nineteen partic-
ipants Values in median (25the75th percentile). Abbreviations: Hmax, Maximun Hoffmann reflex amplitude; Pre, pre
manipulation; Post, post manipulation; Manipulation, experimental procedure; Sham control procedure.

performed in the same position, i.e., the participant studies because the sensory innervation of the
was not moved during the procedure.20 Thus, these sacroiliac and lumbosacral joints are distinct. In the
authors concluded that H-reflex responses to L5-S1 region the zygapophyseal joint, ligaments and
manipulation are sensitive to movement/reposi- monoarticular muscles receive sensory and motor
tioning, and that the H-reflex depressions following inputs mainly from the L5 root e the main compo-
manipulation documented in previous studies were nent of the tibial nerve, and the SIJ receives sensory
movement artifacts, with subsequent distension of inputs from the L2-S3 roots.27,28
the z-joint capsule, rather than treatment effects.17 To minimize movement artifacts, Dishman
However, unlike the work of Dishman et al., who et al. performed an L5-S1 manipulation and the
applied a manipulation to the lumbosacral joint, measurement of the H-reflex in the same body
Cramer et al. applied the manipulation to the SIJ, position. They observed an attenuation of moto-
instead of lumbosacral joint.26 This methodological neuronal activity, and they suggest that the
difference hinders the comparison between the manipulation caused the H-reflex attenuation.20

Fig. 2 Changes in Hmax after the administration of a side-posture HLVA manipulation comparing six of the nineteen
participants that demonstrated attenuation in H-reflex median (H-reflex attenuation >20%) Values in median
(25th75th percentile). p-Values, comparisons by Wilcoxon test. Abbreviations: Hmax, Maximun Hoffmann reflex
amplitude; Pre, pre manipulation; Post, post manipulation.

Please cite this article in press as: Groisman S, et al., H-reflex responses to High-Velocity Low-Amplitude manipulation in
asymptomatic adults, International Journal of Osteopathic Medicine (2014), http://dx.doi.org/10.1016/j.ijosm.2014.04.001
6 S. Groisman et al.

In the present study, the lumbosacral HVLA was Future studies should investigate the H-reflex
performed in the same body position as the mea- changes in symptomatic participants and poten-
surement of the H-reflex. Compared with previous tially measure the autonomic nervous system var-
authors, H-reflex attenuation was demonstrated iables to assess their relationship to the H-reflex.
only in 6 out of 19 participants. It is possible that
these results are due to pre-synaptic inhibition or
other synaptic processes within the spinal cord. Conclusion
A proposed after-effects mechanism would
explain these outcomes, i.e. after HVLA manipula- The present study provides preliminary data on
tion, a post-activation depression phenomenon the short-term effects of HVLA manipulation on
occurred which was triggered by the mechanical the H-reflex. The findings suggest that the
strain of the ligament-muscular system of the spine, response to manipulation varies and depends on
subsequently inhibiting the alpha motoneuron ac- the individual; because it changes in some but not
tivity.29 Mechanical strain associated with the in all participants. The results support the hy-
application of an HVLA could change the mechanical pothesis that H-reflex attenuation differs be-
and neural properties of the muscle spindle. tween people.
The mechanoreceptors and free nerve endings Future studies on neurophysiologic effects of
in the annulus fibrosus, zygapophyseal joint lumbar manipulation should consider the presence of
capsule and ligaments of the spine are potentially somatic and autonomic dysfunction in order to
involved as are the group Ib, III and IV muscle af- investigate the H-reflex variations between
ferents from receptive fields within and near the participants.
facet join capsule. Mechanical stimulation (i.e.
through HVLA manipulation) might inhibit aMN and
stimulate gamma motoneurons (gMN) as well as Authors contributions
the sympathetic nervous system.30,31
The absence of cavitation during HVLA manip- Natalia Rocha, Sandro Groisman, Luciano Silva,
ulation, or to cavitation occurring in a spinal Fabrcia Hofff, Marcia Rodrigues conceived the
segment above L4/L5, could account for those idea for the study, contributed to the design and
participants who did not demonstrate attenuation planning of the research.
of the H-reflex in the present study. This variable All authors were involved in data collection.
was not assessed because the physiological Sandro Groisman, Luciano Silva and Fabrcia
response with or without cavitation was not our Hofff analyzed the data. Joa o A Ehlers, Sandro
objective. Groisman, Luciano Silva and Leonardo Diniz were
Gibbons & Tehan25 describe cavitation as the involved in H-reflex collection.
aim of HVLA manipulation, and Bereznick33 et al. Sandro Groisman, Luciano Silva, Fabrcia Hofff
define cavitation as a result of a drop in the in- wrote the first draft of the manuscript and coor-
ternal joint pressure without an increase in the dinated funding for the project. Leonardo Diniz
size of the joint space and gas. revised the final manuscript after Journal review.
Gas is found inside the joint and is reabsorbed All authors edited and approved the final
into the synovial fluid within 15e30 min e this version of the manuscript.
period is known as the refractory period. Widening All authors were involved in literature search,
of lumbar zygapophyseal joints post manipulation figures, study design, data analysis, data
has been demonstrated by magnetic resonance interpretation.
imaging following lumbar osteopathic manipula-
tion.26 It could be the combination of cavitation
with distension of the joint capsule generating Conflicts of interest statement
changes in the stimulation of the motoneurons.
A limitation of the current study stems from the None declared.
use of the gastrocnemius muscle H-reflex as an index
of motoneuronal excitability of the lumbar spine.
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Please cite this article in press as: Groisman S, et al., H-reflex responses to High-Velocity Low-Amplitude manipulation in
asymptomatic adults, International Journal of Osteopathic Medicine (2014), http://dx.doi.org/10.1016/j.ijosm.2014.04.001
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Please cite this article in press as: Groisman S, et al., H-reflex responses to High-Velocity Low-Amplitude manipulation in
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