Neuromuscular efficiency in fibromyalgia is improved by hyperbaric oxygen therapy: looking inside muscles by means of surface electromyography - Core
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Neuromuscular efficiency in fibromyalgia is improved
by hyperbaric oxygen therapy: looking inside muscles
by means of surface electromyography
R. Casale1, G. Boccia2, Z. Symeonidou1,3, F. Atzeni4, A. Batticciotto5,
F. Salaffi6, P. Sarzi-Puttini5, P.R. Brustio2, A. Rainoldi2
1
Habilita Hospitals & Research ABSTRACT thus suggesting that muscle fatigue is
Rehabilitation Unit, Zingonia, Bergamo; Objective. Neuromuscular efficiency not primarily a muscular problem, as
2
NeuroMuscularFunction/Research (NME) is impaired in fibromyalgia (FM). also demonstrated by other authors
Group, School of Exercise & Sport Hyperbaric oxygen therapy (HBOT) is with different methods.
Sciences, Department of Medical
Sciences, University of Turin;
a medical treatment using 100% of oxy-
gen through an oxygen mask. HBOT in Introduction
3
Department of Physical and
Rehabilitation Medicine, General FM induces changes in cortical excita- Although its aetiology and efficacious
Hospital of Attica “KAT”, Athens, Greece; bility and a secondary reduction in pain treatment are still unclear, FM is a ma-
4
Rheumatology Unit, University of Messina; and muscle fatigue. However, there are jor problem for all National Health Ser-
5
Rheumatology Unit, University Hospital still no direct data indicating changes vices as many epidemiological studies
Luigi Sacco, Milan; in muscle fatigue. The aim of this study have shown that affects a large number
6
Polytechnic University of Marche, of people all over the world. A recent
C. Urbani Hospital, Jesi, Ancona, Italy.
was to assess whether the reduction in
muscle fatigue so far attributed to a cen- review of its prevalence in Europe has
Roberto Casale, MD, PhD found that it affects 2.3% of the popula-
Gennaro Boccia, PhD
tral effect of HBOT can be directly de-
Zaira Symeonidou, MD tected by means of non-invasive sEMG tion as a whole and up to 3.9% of fe-
Fabiola Atzeni, MD, PhD as a change in NME. males, and the trend is similar in North
Alberto Batticciotto, MD, PhD Methods. The study was an observa- America (1.9%, 2.9% of females),
Fausto Salaffi, MD, PhD tional longitudinal study on changes in South America (1.12%, 2.45% of fe-
Piercarlo Sarzi-Puttini, MD NME induced by 20 sessions of HBOT males), and Asia (1.64%, 3.24% of fe-
Paolo Riccardo Brustio, PhD at 2.4 atmosphere, in 22 patients with males) (1).
Alberto Rainoldi, MS, PhD The main somatic symptoms of fibro-
FM (3M; 19F) (age 49.8±9.5; height
Please address correspondence to: 164.7±7.5; weight 63.8±12.7). sEMG myalgia are diffuse musculoskeletal
Roberto Casale, MD, PhD, pain, stiffness and fatigue, all of which
Habilita Hospitals & Research
was recorded in single differential
Rehabilitation Hospitals, configuration from the biceps brachii are related to the muscle system and
Advanced Technology & Pain muscle during the 30-second fatigu- its functioning. Various attempts have
Rehabilitation Units, ing contractions using linear arrays of been made to find specific alterations in
Via Bologna 1, eight adhesive electrodes. muscle fibres using light microscopy,
24040 Zingonia (BG), Italy. Results. Evaluations made before histochemistry, electron microscopy,
E-mail: robertocasale@habilita.it and immediately after the first session and ultrastructural techniques, and the
Received on August 9, 2018; accepted in showed that maximal strength did not published results agree in suggesting
revised form on January 28, 2019. change (T0 49±20 N, T1 49±19 N, local muscle hypoxia as a possible
Clin Exp Rheumatol 2019; 37 (Suppl. 116): p=0.792), thus suggesting that HBOT cause of the development of both spe-
S75-S80. did not induce muscle fatigue or po- cific and non-specific biopsy findings
© Copyright Clinical and tentiation. After 20 sessions of HBOT, (for a short review see ref. 2).
Experimental Rheumatology 2019. NME increased from 1.6±1.1 to 2.1±0.8 Neuromuscular efficiency has been
(p=0.050), whereas maximal strength, studied in conditions such as chronic
Key words: fibromyalgia, surface heart failure (3) or hypoxia exposure
EMG amplitude and muscle fibre CV
electromyography, hyperbaric oxygen (4) using multi-channel surface EMG
did not change.
therapy, muscle fatigue (sEMG). Neuromuscular efficiency can
Conclusion. HBOT did not improve
muscle strength or change muscle fibre be defined as the ability of the nervous
content, but improved the ability of the system to recruit muscles and muscle
central motor command to generate fibres appropriately in order to produce
the same effort (MVC) with fewer re- a given effect, which is impaired in pa-
cruited fibres. Our sEMG findings un- tients with fibromyalgia (5), thus rais-
derlined a modified central mechanism ing the question as to whether fatigue is
Competing interests: none declared. related to fibre type recruitment order, more centrally mediated than a clinical
Clinical and Experimental Rheumatology 2019 S-75
Fibromyalgia and hyperbaric oxygen therapy / R. Casale et al.
epiphenomenon of local muscle hypoxia. Department of Rheumatology, Univer- 30 mg/daily), five patients were treated
The complexity of the syndrome is also sity Hospital Luigi Sacco, Milan, did with pregabalin (mean dose 75 mg/
reflected by the fact that pharmacologi- not consent to participate in the study daily), four patients were treated with
cal (6), non-pharmacological (7) and mainly because the length of the pro- amitriptyline (mean dose 50 mg/daily).
cognitive behavioural treatments (8) do tocol and logistical problems (distance The sEMG experimental protocol
not seem to be predictably efficacious. from the hospital). was carried out by two neurophysiol-
Hyperbaric oxygen therapy (HBOT) Patients with 1) inflammatory causes ogy technicians supervised by a trained
is a medical treatment that enhances of pain; or muscle pain caused by con- neurologist (RC) who was blinded to
the body’s natural healing process by ditions such as vitamin D deficiency the treatment. The data were analysed
means of the inhalation of 100% oxy- 2) alcohol/drug abuse or dependence; by AR,GB. All of the participants gave
gen through an oxygen mask in which 3) significant difficulty in maintaining their written informed consent before
atmospheric pressure is increased and attention or understanding clinimetric taking part in the study, and the protocol
controlled. It has been used for a wide evaluation instructions; 4) any clinical was approved by the Scientific Techni-
variety of conditions usually as part of condition that may interfere with the cal Committee of Habilita (no. 6/2016).
planned overall medical care, and has assessment; 5) pregnant women or po-
led to promising results in the treat- tentially childbearing women not using EMG protocol
ment of a number of painful orthopedic an adequate method of birth control; The subjects were familiarised with the
and rheumatological conditions (9), and 6) any of the following medical sEMG device by being asked to make
headache, complex regional pain syn- conditions that preclude safe HBOT ten sub-maximal isometric contractions
drome, and FM (10, 11). treatment: a) severe cognitive impair- at 90° of elbow flexion (0°=full exten-
HOBT was proposed for FM on the hy- ment; b) current mood episodes, claus- sion), and were then asked to make two
pothesis that it could act centrally by trophobia or seizure disorder; c) active maximal voluntary contraction (MVCs)
inducing changes in cortical excitability or severe pulmonary disease, previous separated by three minutes rest in or-
(12), on the basis of single-photon emis- thoracic surgery or pneumothorax; d) der to avoid any cumulative effects.
sion computed tomography (SPECT) a history of severe heart disease; e) If the MVCs differed from each other
findings that FM patients show abnor- chronic or acute sinusitis/otitis media by more than 5%, a third MVC was
mally high levels of activity in the so- or major eardrum trauma; and f) a his- required. Each attempted MVC lasted
matosensory cortex, but reduced ac- tory of bleomycin-including chemo- 3–5 seconds, during which the sub-
tivity in the frontal, cingulate, medial therapy or current chemotherapy were jects were given strong verbal encour-
temporal, and cerebellar cortices (13). excluded from the study. agement to maximise their effort, and
Eftari et al. showed that HBOT normal- The remaining 28 were sent to the Hy- received visual feedback generated by
ised cortical excitability in a group of perbaric Unit, Habilita Hospitals & Re- signal acquisition software. The great-
FM patients, and inferred a secondary search, Zingonia (Bergamo) to be as- est MVC was used to calculate sub-
reduction in pain and muscle fatigue on sessed by an expert for their eligibility maximal loads.
the grounds that the change temporally for HBOT, and three were considered Three minutes after the last MVC, the
correlated with a clinical improvement ineligible because of the presence of subjects were involved in two isometric
on symptoms (12). However, there are a clinical contraindication to the treat- contractions at respectively 30% and
still no direct data indicating changes in ment (14). 60% of the torque exerted during the
muscle fatigue. Finally, of the 25 patients enrolled in MVC separated by a 5-minute interval.
The primary aim of this study was to the study, two dropped out because They received visual feedback about
assess whether the reduction in muscle of the side effects of HBOT (15, 16), the actual torque exerted, and were
fatigue so far attributed to a central ef- and one who was unwilling to continue instructed to maintain constant the tar-
fect of HOBT can be directly detected the study because of unforeseen fam- get elbow flexion torque at 90° for 30
by means of non-invasive sEMG of the ily problems. The study was therefore seconds. They were also provided with
biceps brachii muscle as a change in completed by 22 patients (3 males and standardised encouragement to keep
neuromuscular efficiency before and 19 females) (mean age 50.6, min 28 the exerted torque as stable as possible.
after treatments repeated over time in max 64 years; mean height 164.7, min
a group of patients with fibromyalgia. 164 max 175 cm; mean weight 66.9, EMG measurements
mean 45 max 95 kg). All the patients The myoelectrical signals were re-
Methods received analgesic treatment (paraceta- corded in single differential configura-
Patients mol, tramadol) at stable doses before tion from the long head of the biceps
Twelve of an initially unselected group the enrollment in the study protocol. brachii muscle during the 30-second
of 40 female patients with a confirmed All the patients were in controlled re- fatiguing contractions using linear ar-
diagnosis of fibromyalgia made by habilitation therapy, but no one was rays of eight adhesive electrodes sepa-
two experts (SP, FA) on the basis of practicing heavy physical activity at rated by an inter-electrode distance of
the 1990 and 2010 American College the moment of enrollment. Ten patients 5 mm (OT Bioelettronica, Turin, Italy).
of Rheumatology (ACR) criteria at the were receiving duloxetine (mean dose Before the arrays were positioned, the
S-76 Clinical and Experimental Rheumatology 2019Fibromyalgia and hyperbaric oxygen therapy / R. Casale et al.
skin was slightly abraded with paste parameters are not exceeded (< 22%). computed using non-overlapping signal
and cleaned with water in accordance Delivery times: therapies are normally epochs of 0.5 seconds and were aver-
with the skin preparation recommenda- divided into 3 periods of oxygen breath- aged among all of the accepted channels.
tions of the Surface Electromyography ing of 20–25 minutes. Taking into ac- The data were analysed using custom-
for the Non-invasive Assessment of count the times necessary for compres- written software in MATLAB R2014a
Muscles (SENIAM) project (17). sion, decompression, oxygen respiration (Mathworks, Natick, MA, USA).
The optimal position and orientation and pauses between the aforementioned The maximum torque of each MVC
of the array was sought on the basis of periods, the indicative duration of an or- was determined, and the instant at
visual inspection of the sEMG signals. dinary therapy was 91 minutes. which it occurred was used to calculate
The sites showing the clear propagation O2 dispensation control: the mask is the EMG variables. In the case of fa-
of muscle fibre action potentials and the provided of a specific analysis system tiguing contractions, it has been dem-
main innervation zones were identified able to measure the percentage of oxy- onstrated that linear regression is the
using a dry linear array of 16 electrodes gen present in the mask and available best model for fitting EMG data during
separated by an inter-electrode distance for the patient. sub-maximal isometric contractions
of 5 mm (OT Bioelettronica). The adhe- Although oxygen is delivered to the (21), and so linear regressions were
sive electrode arrays were then placed patient in pure 100% form, there are used to calculate the rate of change in
parallel to the muscle fibres proximal to always minimum leakages in the con- the EMG variables (calculated as the
the innervation zone in which the unidi- tact between the mask and the face of percentage ratio between the change in
rectional propagation of the motor units the patient (the oxygen comes out and the EMG estimate in one second and
(MU) action potentials was detected. In the ambient air enters) with a real per- the initial value, and expressed as %/s).
order to ensure correct electrode-skin centage of oxygen in the mask reduced Neuromuscolar efficency (NME) was
contact, the electrode cavities were to an average of 95%. Below this per- calculated as the ratio between force
filled with 20-30 μl of conductive paste centage signals are activated, alerting and muscle fibre CV (22).
(Spes-Medica, Battipaglia, Italy), and the personnel within the chamber to
the arrays were fixed using an extensible check the current situation (mask not Statistical analysis
dressing (Fixomull®, Beiersdorf, D). positioned, uncooperative patient, etc.) The Kolmogorov-Smirnov test was
The sEMG signals were amplified, sam- This monitoring takes place in real used to assess the normality of data
pled at 2048 Hz, bandpass filtered (3 time and with each patient’s control distribution and, if the data were not
dB bandwidth, 20-450 Hz, 12 dB/oct step every 3–4 minutes. normally distributed, they were log-
slope on each side), and converted to transformed before statistical analysis
digital data using a 16-bit A/D converter Data analysis and back-transformed to obtain de-
(EMG-USB2+, OT Bioelettronica). The sEMG signals were visually in- scriptive statistics. Student’s t-tests
Samples were visualised during acquisi- spected in order to select the best chan- for independent samples were used to
tion, and then stored on a personal com- nels to use for variable estimates. The compare maximal force and the EMG
puter using OT BioLab software (v. 1.8, muscle fibre conduction velocity (CV) values at T0 vs. T1 (acute effects) and
OT Bioelettronica) for further analysis. of the sEMG signals were computed pre- vs. post HBOT treatment (cumu-
off-line among all the selected chan- lative effects). The statistical analyses
HBOT nels using numerical algorithms (18) were made using SPSS statistics soft-
Treatments were done using a hyperbaric and non-overlapping signal epochs of ware (version 20.0, IBM Corporation,
chamber GAMMA, GALEAZZI S.p.A. 0.5 seconds. CV was computed as e/d, Somers, NY, USA), and a p-value of
n° 510/88, ISPESL n° SP 78-88. capac- where e is the inter-electrode distanceFibromyalgia and hyperbaric oxygen therapy / R. Casale et al.
Fig. 1. Mean mechanical and electromyographical (EMG) values recorded during MVC (Maximum Voluntary Contractor); average rectified EMG ampli-
tude; NME (i.e. the ratio between force and ARV); and muscle fibre CV. *p=0.050.
tabolism, reduces apoptosis, alleviates
oxidative stress, and increases neurotro-
phin and nitric oxide levels by enhanc-
ing mitochondrial function in neurons
and glial cells, and it may even promote
the neurogenesis of endogenous neural
stem cells (27, 28).
Fig. 2. Mean (SD) rate of change in EMG variables during the fatiguing contraction (30 seconds at 60% of On the basis of these premises and MNF
maximal force): muscle fibre CV; mean power spectra frequency of the EMG signal (MNF); fractal dimen- findings of altered cortical activity in
sion of the EMG signal (FD). There were not statistically significant differences between PRE vs. POST. FM patients, two Israeli groups (10-12)
have evaluated the efficacy of HBOT
p=0.695), but average rectified value of memory loss. All of these symptoms in improving fibromyalgia symptoms
(ARV) decreased from 77±48 μV to and signs are related to region-specific by rectifying the typically altered brain
72±51 μV (p=0.024). anatomical changes in grey matter functions. Both groups suggest that the
volume, central sensitisation with de- clinical improvement is due to a pri-
EMG results pre- vs. post-MCV creased functional connectivity in the mary improvement in central functions
(cumulative effects: T1-T20) descending pain-modulating system, that is only secondarily reflected on
The mechanical and EMG variables and increased activity in the so-called muscle fatigue and pain.
recorded during the MVC are shown pain matrix (24). It is therefore a com- The aim of this study was to look direct-
in Figure 1. There was no difference plex and heterogeneous clinical condi- ly at muscle in order to assess whether
in maximal strength, EMG amplitude tion that always reduced the patients’ the rearranged cortical activity induced
or muscle fibre CV before and after quality of life and leads to increasing by HBOT can really improve neuromus-
the intervention (p>0.3), but NME physical, functional and emotional dis- cular efficiency and therefore muscle
(i.e. the ratio between EMG amplitude ability. function. To this end, sEMG was used
and force) increased from 1.6±1.1 to Its complexity is also reflected in the as a widely accepted and reproducible
2.1±0.8 (p=0.050). substantial lack of efficacious phar- means of evaluating muscle fatigue be-
The rate of change in the EMG varia- macological and non-pharmacological cause its variables correlate with acute
bles (used as indices of the myoelectric treatments, whether they are used alone alterations in motor unit recruitment
manifestation of fatigue) are shown in or in combination (6, 23). A wide range strategies and/or chronic changes in the
Figure 2. None of these variables were of non-pharmacological treatments number or size of muscle fibre types that
affected by the intervention (p>0.3). have been tried, including various reflect muscle biopsy findings and can
types of exercise, cognitive-behav- be used to foresee the mechanical and
Discussion ioural therapy, physiotherapy, physical functional impairments observed in bio-
FM is a major cause of chronic wide- therapy including transcutaneous elec- mechanical and clinical studies, includ-
spread pain, and its general population trical nerve stimulation, LASER treat- ing neuromuscular efficiency and the
prevalence of 2.3% makes it a consid- ment of trigger points, heat and cold, early development of fatigue (18, 22).
erable burden on National Health Ser- balneotherapy and acupuncture (7, 25). We have previously used sEMG to ob-
vices because of the delays in making HBOT has also been suggested because, serve altered neuromuscular efficiency
a correct diagnosis (23) and very late under normal circumstances, oxygen is in FM patients (5), whose muscles
referrals for rehabilitation. The most transported throughout the body only by simply work inefficiently rather than
disabling aspects of the syndrome are red blood cells, whereas HBOT allows showing any specific alteration capable
pain and fatigue, but there may also be oxygen to be carried into all body fluids, of explaining pain and muscle fatigue,
various combinations of other symp- plasma, lymph, bone and central nerv- and these seems to be related to a fail-
toms, the most frequent of which are ous system fluids, and areas where blood ure in central control due to an altera-
non-refreshing sleep, mood disturbanc- circulation is diminished or blocked tion in suprasegmental control. These
es, cognitive impairment, and a sense (26). In vitro, HBOT increases cell me- conclusions are supported by the find-
S-78 Clinical and Experimental Rheumatology 2019Fibromyalgia and hyperbaric oxygen therapy / R. Casale et al.
ings of the present study showing the among the authors that a treatment du- tigue during exposure to hypobaric hypoxia
for 12 days. Muscle Nerve 2004; 30: 618-25.
same sEMG picture in the pre- HBOT ration of 40 sessions was not realistic in
5. CASALE R, SARZI-PUTTINI P, ATZENI F, GAZ-
tests: i.e. patients with FM are affect- our local situation because the patients ZONI M, BUSKILA D, RAINOLDI A: Central
ed by neuromuscular inefficiency that attending the recruiting centre came motor control failure in fibromyalgia: a sur-
is mainly due to altered central motor from all over Italy. We therefore de- face electromyography study. BMC Muscu-
loskelet Disord 2009; 10:78
drive. As there were no changes in mus- cided to reduce the number of sessions 6. SARZI-PUTTINI P, TORTA R, MARINANGELI
cle fibres, these findings suggest that from 40 to 20, and to increase chamber F et al.: Fibromyalgia syndrome: the phar-
HBOT acted at central level by induc- pressure to 2.4 atm instead of using the macological treatment options. Reumatismo
ing a change in adopted strategies, op- 2 atm used in the other experiments. 2008; 60 (Suppl. 1): 50-8.
7. CASALE R, CAZZOLA M, ARIOLI G et al.:
timising mechanical output, and reduc- We are aware that the statistical signifi- Non-pharmacological treatments in fibromy-
ing the myoelectrical manifestations of cance of the improvement in NME ob- algia. Reumatismo 2008; 60 (Suppl. 1): 59-
fatigue. This possibility has previously served in our study may have been due 69.
been demonstrated in healthy subjects to the reduction in the number of ses- 8. BERNARDY K, KLOSE P, WELSCH P, HÄUSER
W: Efficacy, acceptability and safety of cog-
using a different conditioning treatment sions, which raises the question of the nitive behavioural therapies in fibromyalgia
(29-31). right HBOT dose for FM. This is funda- syndrome - A systematic review and meta-
In terms of the acute effects of HBOT mentally important not only because the analysis of randomized controlled trials. Eur
on sEMG parameters, evaluations were length of the treatment may be difficult J Pain 2018; 22: 242-60.
9. BARILARO G, MASALA FI, PARRACCHINI R
made before and immediately after for the patients to cope with, but also et al.: The role of hyperbaric oxygen therapy
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strength had not changed (T0 49±20 N, is a recognised pharmacological treat- Isr Med Assoc J 2017; 19: 429-34.
10. YILDIZ S, UZUN G, KIRALP MZ: Hyperbaric
T1 49±19 N, p=0.792), thus suggest- ment (30) and the appropriate dose has
oxygen therapy in chronic pain management.
ing that HBOT did not induce muscle to be carefully assessed. There is there- Curr Pain Headache Rep 2006; 10: 95-100.
fatigue or potentiation. However, after fore a need to develop HBOT protocols 11. YILDIZ S, KIRALP MZ, AKIN A et al.: A new
20 sessions of HBOT, neuromuscular and establish the intensity (O2 atm) and treatment modality for fibromyalgia syn-
drome: hyperbaric oxygen therapy. J Int Med
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amplitude and force) increased from sions for patients with this specific pa- 12. EFRATI S, GOLAN H, BECHOR Y et al.:
1.6±1.1 to 2.1±0.8 (p=0.050), whereas thology, all of which will require more Hyperbaric oxygen therapy can diminish fi-
maximal strength, EMG amplitude and research and a shared consensus con- bromyalgia syndrome – prospective clinical
trial. PLoS One 2015; 10: e0127012.
muscle fibre CV did not change. cerning the best treatment/dose. 13. GUEDJ E, CAMMILLERI S, NIBOYET J et al.:
In other words, HBOT did not improve Clinical correlate of brain SPECT perfusion
muscle strength or change muscle fibre Acknowledgements abnormalities in fibromyalgia. J Nucl Med
content, but improved the ability of the We are very grateful to all the staff of 2008; 49: 1798-803.
14. MATHIEU D, MARRONI A, KOT J: Tenth Eu-
central motor command to generate the HBOT Service of Habilita, Hospi- ropean Consensus Conference on Hyperbaric
the same effort (MVC) with fewer re- tals & Research, Zingonia: they are so Medicine: recommendations for accepted
cruited fibres. Our sEMG findings un- many that it is not possible to mention and non-accepted clinical indications and
them all. Our special thanks to Ugo Pani practice of hyperbaric oxygen treatment.
derlined a modified central mechanism
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