www.elsevier.com/ijos
RESEARCH REPORT
a
Brazilian Institute of Osteopathic, Rio de Janeiro, Brazil
b
Mae de Deus Hospital, Porto Alegre, Brazil
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.
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.
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.
The authors chose this technique because the L4/5 References
nerve root forms the tibial nerve, and the use of
healthy participants. Thus, it is not possible to 1. Licciardone JC, Brimhall AK, King LN. Osteopathic manip-
extrapolate the results to patients suffering from low ulative treatment for low back pain: a systematic review
back pain. In addition, there was not any cavitation and meta-analysis of randomized controlled trials. BMC
during the HVLA manipulation for all participants. Musculoskelet Disord 2005;6:43e5.
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 7
2. Rubinstein SM, van Middelkoop M, Assendelft WJJ, de 17. Suter E, McMorland G, Herzog W. Short-term, effects of
Boer MR, van Tulder MW. Spinal manipulative therapy for spinal manipulation on H-reflex amplitude in healthy and
chronic low-back pain (Review). Cochrane Database Syst symptomatic participants. J Manipulative Physiol Ther
Rev 2011;2. http://dx.doi.org/10.1002/14651858. 2005;28:667e97.
3. Licciardone JC, Minotti DE, Gatchel RJ, Kearns CM, 18. Dishman JD, Bulbulian R. Spinal reflex attenuation associ-
Singh KP. Osteopathic manual treatment and ultrasound ated with spinal manipulation. Spine J 2000;25:2519e24.
therapy for chronic low back pain: a randomized controlled 19. Dishman JD, Burke J. Spinal reflex excitability changes
trial. Ann Fam Med 2013;11:122e9. after cervical and lumbar spinal manipulation: a compara-
4. Airaksinen O, Brox JI, Cedraschi C, Hildebrandt J, Klaber- tive study. Spine J 2003;3:204e12.
Moffett J, Kovacs F, et al. European guidelines for the 20. Dishman JD, Dougherty PE, Burke JR. Evaluation of the
management of chronic nonspecific low back pain. Eur effect of postural perturbation on motoneuronal activity
Spine J 2006;15:192e300. following various methods of lumbar spinal manipulation.
5. Van Tulder M, Becker A, Bekkering T, Breen A, Del Real MT, Spine J 2005;5:650e9.
Hutchinson A. European guidelines for the management of 21. Orakifar N, Kamali F, Pirouzi S, Jamshidi F. Sacroiliac joint
acute nonspecific low back pain in primary care. Eur Spine J manipulation attenuates alpha-motoneuron activity in
2006;15:169e91. healthy women: a quasi-experimental study. Arch Phys Med
6. Evans DW. Mechanisms and effects of spinal high-velocity, Rehabil 2012;93:56e61.
low-amplitude thrust manipulation: previous theories. J 22. Hugon M. Methodology of the Hoffmann reflex in man. In:
Manipulative Physiol Ther 2002;25:251e62. Desmedt JE, editor. New developments in electromyog-
7. Indahl A, Kaigle AM, Reikeras O, Holm SH. Interaction be- raphy and clinical neurophysiology. New York, NY: Karger;
tween the porcine lumbar intervertebral disc, zyg- 1973. pp. 277e93.
apophysial joints, and paraspinal muscles. Spine 1997;22: 23. Cram JR, Kasman GS. Introduction to surface electromy-
2834e40. ography. 2nd ed. Jones & Bartlett Learning; 2010.
8. Korr IM. Proprioceptors and somatic dysfunction. J Am 24. Palmieri RM, Ingersoll CD, Hoffman MA. The Hoffmann re-
Osteopath Assoc 1975;74:638e50. flex: methodologic considerations and applications for use
9. Howell JN, Cabell KS, Chila AG, Eland DC. Stretch reflex and in sports medicine and athetic training research. J Athl
Hoffmann reflex responses to osteopathic manipulative Train 2004;39:268e77.
treatment in participants with achilles tendinitis. J Am 25. Gibbons P, Tehan P. Manipulation of the spine. Thorax and
Osteopath Assoc 2006;106:537e45. pelvis an osteopathic perspective. 3rd ed. Churchill Liv-
10. King HH, Janig W, Patterson MM. The science and applica- ingstone Elsevier; 2009.
tion of manual therapy. 1st ed. Elsevier; 2011. 26. Cramer GD, Gregerson DM, Knudsen JT, Hubbard BB,
11. Wynne MM, Burns JM, Eland DC, Conaster RR, Howell JN. Ustas LM, Cantu JA. The effects of side-posture positioning
Effect of counterstrain on stretch reflex, Hoffmann re- and spinal adjusting on the lumbar Z joints. A randomized
flexes, and clinical outcomes in subjecs with plantar fas- controlled trial with sixty-four participants. Spine J 2002;
ciitis. J Am Osteopath Assoc 2006;106:547e56. 27:2459e66.
12. Fryer G, Pearce AJ. The effect of lumbosacral manipulation 27. Dishman JD, Cunningham BM, Burke J. Comparison of tibial
on corticospinal and spinal reflex excitability on asymp- nerve H-reflex excitability after cervical and lumbar spine
tomatic participants. J Manipulative Physiol Ther 2011;35: manipulation. J Manipulative Physiol Ther 2002;25:
86e93. 318e25.
13. Cramer GD, Humphreys CR, Hondras MA, McGregor M, 28. Chila GA. Foundations of osteopathic medicine. 3rd ed.
Triano JJ. The Hmax/Mmax ratio as an outcome measure Lippincott Williams & Wilkins; 2010.
for acute low back pain. J Manipulative Physiol Ther 1993; 29. Greenman EP. Principles of manual medicine. 4th ed. Lip-
16:7e13. pincott Williams & Wilkins; 2010.
14. Schindler-Ivens SM, Shields RK. Low frequency depression 30. Gregory JE, Morgan DL, Proske U. Aftereffects in the re-
of H-reflex in humans with acute and chronic spinal cord sponses of cat muscle spindles. J Neurophysiol 1986;56:
injury. Exp Brain Res 2000;133:233e41. 451e61.
15. Humphreys CR, Triano JJ, Brandl MJ. Sensitivity studies of 31. Pickar JG. Neurophysiological effects of spinal manipula-
H-reflex alterations in idiopathic low back pain patients vs. tion. Spine J 2002;2:357e71.
a healthy population. J Manipulative Physiol Ther 1989;12: 33. Bereznick DE, Pecora CG, Ross JK, McGill SM. The refractory
71e8. period of the audible crack after lumbar manipulation: a
16. Floman Y, Liram N, Gilai AN. Spinal manipulation results in preliminary study. J Manipulative Physiol Ther 2008;31:
immediate H-reflex changes in patients with unilateral disc 199e203.
herniation. Eur Spine J 1997;6:398e401.
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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