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BioPsychoSocial Medicine
Published in: BioPsychoSocial Medicine 1/2019

Open Access 01-12-2019 | Cytokines | Research

The longitudinal effects of seated isometric yoga on blood biomarkers, autonomic functions, and psychological parameters of patients with chronic fatigue syndrome: a pilot study

Authors: Takakazu Oka, Tokusei Tanahashi, Battuvshin Lkhagvasuren, Yu Yamada

Published in: BioPsychoSocial Medicine | Issue 1/2019

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Abstract

Background

In a previous randomized controlled trial, we found that practicing seated isometric yoga regularly for 2 months improved the fatigue of patients with chronic fatigue syndrome (CFS) who are resistant to conventional therapy. The aim of this pilot study was to investigate the possible mechanisms behind this finding by comparing blood biomarkers, autonomic nervous function, and psychological indices before versus after an intervention period of seated isometric yoga practice.

Methods

Fifteen patients with CFS who did not show satisfactory improvements after at least 6 months of conventional therapy practiced seated isometric yoga (biweekly 20-min sessions with a yoga instructor and daily practice at home) for 2 months. The longitudinal effects of seated isometric yoga on fatigue, blood biomarkers, autonomic function, and psychological state were investigated by comparing the following parameters before and after the intervention period: Fatigue severity was assessed by the Chalder fatigue scale (FS) score. Levels of the blood biomarkers cortisol, DHEA-S, TNF-α, IL-6, prolactin, carnitine, TGF-β1, BDNF, MHPG, HVA, and α-MSH were measured. The autonomic nervous functions assessed were heart rate (HR) and HR variability. Psychological indices included the 20-item Toronto Alexithymia Scale (TAS-20) and the Hospital Anxiety and Depression Scale (HADS).

Results

Practicing seated isometric yoga for 2 months resulted in significant reductions in the Chalder FS (P = 0.002) and HADS-depression (P = 0.02) scores. No significant changes were observed in any other parameter evaluated. The change in Chalder FS score was not correlated with the change in HADS-depression score. However, this change was positively correlated with changes in the serum TNF-α levels (P = 0.048), the high frequency component of HR variability (P = 0.042), and TAS-20 scores (P = 0.001).

Conclusions

Regular practice of seated isometric yoga for 2 months reduced the fatigue and depressive symptom scores of patients with CFS without affecting any other parameters we investigated. This study failed to identify the markers responsible for the longitudinal fatigue-relieving effect of seated isometric yoga. However, considering that the reduced fatigue was associated with decreased serum TNF-α level and TAS-20 scores, fatigue improvement might be related to reduced inflammation and improved alexithymia in these patients.

Trial registration

University Hospital Medical Information Network (UMIN CTR) UMIN000009646. Registered Dec 27, 2012.
Literature
1.
Fukuda K, Straus SE, Hickie I, Sharpe MC, Dobbins JG, Komaroff A. The chronic fatigue syndrome: a comprehensive approach to its definition and study. International chronic fatigue syndrome study group. Ann Intern Med. 1994;121(12):953–9.PubMedCrossRef
2.
Carruthers BM, van de Sande MI. Myalgic encephalomyelitis/chronic fatigue syndrome: a clinical case definition and guidelines for medical practitioners an overview of the Canadian consensus document; 2005.
3.
Oka T. Influence of psychological stress on chronic fatigue syndrome. Adv Neuroimmune Biol. 2013;4:301–9.
4.
Powell DJ, Liossi C, Moss-Morris R, Schlotz W. Unstimulated cortisol secretory activity in everyday life and its relationship with fatigue and chronic fatigue syndrome: a systematic review and subset meta-analysis. Psychoneuroendocrinology. 2013;38(11):2405–22.PubMedCrossRef
5.
Papadopoulos AS, Cleare AJ. Hypothalamic-pituitary-adrenal axis dysfunction in chronic fatigue syndrome. Nat Rev Endocrinol. 2011;8(1):22–32.PubMedCrossRef
6.
Kuratsune H, Yamaguti K, Sawada M, Kodate S, Machii T, Kanakura Y, Kitani T. Dehydroepiandrosterone sulfate deficiency in chronic fatigue syndrome. Int J Mol Med. 1998;1(1):143–6.PubMed
7.
Scott LV, Salahuddin F, Cooney J, Svec F, Dinan TG. Differences in adrenal steroid profile in chronic fatigue syndrome, in depression and in health. J Affect Disord. 1999;54(1–2):129–37.PubMedCrossRef
8.
Moss RB, Mercandetti A, Vojdani A. TNF-alpha and chronic fatigue syndrome. J Clin Immunol. 1999;19(5):314–6.PubMedCrossRef
9.
Maes M, Twisk FN, Kubera M, Ringel K. Evidence for inflammation and activation of cell-mediated immunity in Myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS): increased interleukin-1, tumor necrosis factor-alpha, PMN-elastase, lysozyme and neopterin. J Affect Disord. 2012;136(3):933–9.PubMedCrossRef
10.
Garcia MN, Hause AM, Walker CM, Orange JS, Hasbun R, Murray KO. Evaluation of prolonged fatigue post-West Nile virus infection and association of fatigue with elevated antiviral and proinflammatory cytokines. Viral Immunol. 2014;27(7):327–33.PubMedPubMedCentralCrossRef
11.
Khaiboullina SF, DeMeirleir KL, Rawat S, Berk GS, Gaynor-Berk RS, Mijatovic T, Blatt N, Rizvanov AA, Young SG, Lombardi VC. Cytokine expression provides clues to the pathophysiology of gulf war illness and myalgic encephalomyelitis. Cytokine. 2015;72(1):1–8.PubMedCrossRef
12.
Miller AH, Jones JF, Drake DF, Tian H, Unger ER, Pagnoni G. Decreased basal ganglia activation in subjects with chronic fatigue syndrome: association with symptoms of fatigue. PLoS One. 2014;9(5):e98156.PubMedPubMedCentralCrossRef
13.
Mizuno K, Kawatani J, Tajima K, Sasaki AT, Yoneda T, Komi M, Hirai T, Tomoda A, Joudoi T, Watanabe Y. Low putamen activity associated with poor reward sensitivity in childhood chronic fatigue syndrome. Neuroimage Clin. 2016;12:600–6.PubMedPubMedCentralCrossRef
14.
Kopin IJ. Catecholamine metabolism: basic aspects and clinical significance. Pharmacol Rev. 1985;37(4):333–64.PubMed
15.
Nagaoka S, Iwamoto N, Arai H. First-episode neuroleptic-free schizophrenics: concentrations of monoamines and their metabolites in plasma and their correlations with clinical responses to haloperidol treatment. Biol Psychiatry. 1997;41(8):857–64.PubMedCrossRef
16.
Demitrack MA, Gold PW, Dale JK, Krahn DD, Kling MA, Straus SE. Plasma and cerebrospinal fluid monoamine metabolism in patients with chronic fatigue syndrome: preliminary findings. Biol Psychiatry. 1992;32(12):1065–77.PubMedCrossRef
17.
Shishioh-Ikejima N, Ogawa T, Yamaguti K, Watanabe Y, Kuratsune H, Kiyama H. The increase of alpha-melanocyte-stimulating hormone in the plasma of chronic fatigue syndrome patients. BMC Neurol. 2010;10:73.PubMedPubMedCentralCrossRef
18.
De Becker P, Roeykens J, Reynders M, McGregor N, De Meirleir K. Exercise capacity in chronic fatigue syndrome. Arch Intern Med. 2000;160(21):3270–7.PubMedCrossRef
19.
Boneva RS, Decker MJ, Maloney EM, Lin JM, Jones JF, Helgason HG, Heim CM, Rye DB, Reeves WC. Higher heart rate and reduced heart rate variability persist during sleep in chronic fatigue syndrome: a population-based study. Auton Neurosci. 2007;137(1–2):94–101.PubMedCrossRef
20.
Beaumont A, Burton AR, Lemon J, Bennett BK, Lloyd A, Vollmer-Conna U. Reduced cardiac vagal modulation impacts on cognitive performance in chronic fatigue syndrome. PLoS One. 2012;7(11):e49518.PubMedPubMedCentralCrossRef
21.
Kuratsune H, Yamaguti K, Takahashi M, Misaki H, Tagawa S, Kitani T. Acylcarnitine deficiency in chronic fatigue syndrome. Clin Infect Dis. 1994;18(Suppl 1):S62–7.PubMedCrossRef
22.
Kuratsune H, Yamaguti K, Lindh G, Evengard B, Takahashi M, Machii T, Matsumura K, Takaishi J, Kawata S, Langstrom B, et al. Low levels of serum acylcarnitine in chronic fatigue syndrome and chronic hepatitis type C, but not seen in other diseases. Int J Mol Med. 1998;2(1):51–6.PubMed
23.
Carruthers BM, van de Sande MI, De Meirleir KL, Klimas NG, Broderick G, Mitchell T, Staines D, Powles AC, Speight N, Vallings R, et al. Myalgic encephalomyelitis: international consensus criteria. J Intern Med. 2011;270(4):327–38.PubMedPubMedCentralCrossRef
24.
Maroti D, Molander P, Bileviciute-Ljungar I. Differences in alexithymia and emotional awareness in exhaustion syndrome and chronic fatigue syndrome. Scand J Psychol. 2017;58(1):52–61.PubMedCrossRef
25.
Oka T, Tanahashi T, Chijiwa T, Lkhagvasuren B, Sudo N, Oka K. Isometric yoga improves the fatigue and pain of patients with chronic fatigue syndrome who are resistant to conventional therapy: a randomized, controlled trial. Biopsychosoc Med. 2014;8:27.PubMedPubMedCentralCrossRef
26.
Oka T, Tanahashi T, Sudo N, Lkhagvasuren B, Yamada Y. Changes in fatigue, autonomic functions, and blood biomarkers due to sitting isometric yoga in patients with chronic fatigue syndrome. Biopsychosoc Med. 2018;12:3.PubMedPubMedCentralCrossRef
27.
Chandwani KD, Perkins G, Nagendra HR, Raghuram NV, Spelman A, Nagarathna R, Johnson K, Fortier A, Arun B, Wei Q, et al. Randomized, controlled trial of yoga in women with breast cancer undergoing radiotherapy. J Clin Oncol. 2014;32(10):1058–65.PubMedPubMedCentralCrossRef
28.
Rao RM, Nagendra HR, Raghuram N, Vinay C, Chandrashekara S, Gopinath KS, Srinath BS. Influence of yoga on postoperative outcomes and wound healing in early operable breast cancer patients undergoing surgery. Int J Yoga. 2008;1(1):33–41.PubMedPubMedCentralCrossRef
29.
Bower JE, Greendale G, Crosswell AD, Garet D, Sternlieb B, Ganz PA, Irwin MR, Olmstead R, Arevalo J, Cole SW. Yoga reduces inflammatory signaling in fatigued breast cancer survivors: a randomized controlled trial. Psychoneuroendocrinology. 2014;43:20–9.PubMedPubMedCentralCrossRef
30.
Bower JE, Garet D, Sternlieb B, Ganz PA, Irwin MR, Olmstead R, Greendale G. Yoga for persistent fatigue in breast cancer survivors: a randomized controlled trial. Cancer. 2012;118(15):3766–75.PubMedCrossRef
31.
Greenlee H, DuPont-Reyes MJ, Balneaves LG, Carlson LE, Cohen MR, Deng G, Johnson JA, Mumber M, Seely D, Zick SM, et al. Clinical practice guidelines on the evidence-based use of integrative therapies during and after breast cancer treatment. CA Cancer J Clin. 2017;67(3):194–232.PubMedPubMedCentralCrossRef
32.
33.
Oka T, Kanemitsu Y, Sudo N, Hayashi H, Oka K. Psychological stress contributed to the development of low-grade fever in a patient with chronic fatigue syndrome: a case report. Biopsychosoc Med. 2013;7(1):7.PubMedPubMedCentralCrossRef
34.
Oka T, Okumi H, Nishida S, Ito T, Morikiyo S, Kimura Y, Murakami M. Effects of Kampo on functional gastrointestinal disorders. Biopsychosoc Med. 2014;8(1):5.PubMedPubMedCentralCrossRef
35.
Oka T. Efficacy and limitations of autogenic training as a treatment of chronic fatigue syndrome. Jpn J Autogenic Ther. 2015;35(1):12–9.
36.
37.
Oka T: You Tube “Seated isometric yoga program for ME CFS”. https://​wwwyoutubecom/​watch?​v=​ithZVKBRyok&​t=​572s 2018.
38.
Chalder T, Berelowitz G, Pawlikowska T, Watts L, Wessely S, Wright D, Wallace EP. Development of a fatigue scale. J Psychosom Res. 1993;37(2):147–53.PubMedCrossRef
39.
Tanaka M, Fukuda S, Mizuno K, Imai-Matsumura K, Jodoi T, Kawatani J, Takano M, Miike T, Tomoda A, Watanabe Y. Reliability and validity of the Japanese version of the Chalder fatigue scale among youth in Japan. Psychol Rep. 2008;103(3):682–90.PubMedCrossRef
40.
Kobayashi Y, Fujikawa T, Kobayashi H, Sumida K, Suzuki S, Kagimoto M, Okuyama Y, Ehara Y, Katsumata M, Fujita M, et al. Relationship between arterial stiffness and blood pressure drop during the sit-to-stand test in patients with diabetes mellitus. J Atheroscler Thromb. 2017;24(2):147–56.PubMedPubMedCentralCrossRef
41.
Sawada Y, Ohtomo N, Tanaka Y, Tanaka G, Yamakoshi K, Terachi S, Shimamoto K, Nakagawa M, Satoh S, Kuroda S, et al. New technique for time series analysis combining the maximum entropy method and non-linear least squares method: its value in heart rate variability analysis. Med Biol Eng Comput. 1997;35(4):318–22.PubMedCrossRef
42.
Jia T, Ogawa Y, Miura M, Ito O, Kohzuki M. Music attenuated a decrease in parasympathetic nervous system activity after exercise. PLoS One. 2016;11(2):e0148648.PubMedPubMedCentralCrossRef
43.
Shaffer F, McCraty R, Zerr CL. A healthy heart is not a metronome: an integrative review of the heart's anatomy and heart rate variability. Front Psychol. 2014;5:1040.PubMedPubMedCentralCrossRef
44.
Zigmond AS, Snaith RP. The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67(6):361–70.PubMedCrossRef
45.
Zigmond AS, Snaith RP, Kitamura T. The hospital anxiety and depression scale (in Japanese). Seisinka-Sindangaku. 1993;4:371–2.
46.
Komaki G, Maeda M, Arimura T, Nakata A, Shinoda H, Ogata I, Shimura M, Kawamura N, Kubo C. The reliability and factorial validity of the Japanese version of the 20-item Toronto alexithymia scale (TAS-20). Jpn J Psychosom Med. 2003;43:839–46.
47.
Cohen J. Statistical power analysis for the behavioral sciences. 2nd ed. New York: Lawrence Erlbaum Associtates; 1988.
48.
Benjamini Y, Krieger AM, Yekutieli D. Adaptive linear step-up procedures that control the false discovery rate. Biometrika. 2006;93:491–507.CrossRef
49.
Faul F, Erdfelder E, Lang AG, Buchner A. G*power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.PubMedCrossRef
50.
Van Houdenhove B, Van Den Eede F, Luyten P. Does hypothalamic-pituitary-adrenal axis hypofunction in chronic fatigue syndrome reflect a 'crash' in the stress system? Med Hypotheses. 2009;72(6):701–5.PubMedCrossRef
51.
Morgan CA 3rd, Southwick S, Hazlett G, Rasmusson A, Hoyt G, Zimolo Z, Charney D. Relationships among plasma dehydroepiandrosterone sulfate and cortisol levels, symptoms of dissociation, and objective performance in humans exposed to acute stress. Arch Gen Psychiatry. 2004;61(8):819–25.PubMedCrossRef
52.
Cahn BR, Goodman MS, Peterson CT, Maturi R, Mills PJ. Yoga, meditation and mind-body health: increased BDNF, cortisol awakening response, and altered inflammatory marker expression after a 3-month yoga and meditation retreat. Front Hum Neurosci. 2017;11:315.PubMedPubMedCentralCrossRef
53.
Oka T, Aou S, Hori T. Intracerebroventricular injection of interleukin-1 beta induces hyperalgesia in rats. Brain Res. 1993;624(1–2):61–8.PubMedCrossRef
54.
Oka T, Oka K, Hosoi M, Hori T. Intracerebroventricular injection of interleukin-6 induces thermal hyperalgesia in rats. Brain Res. 1995;692(1–2):123–8.PubMedCrossRef
55.
Oka T, Wakugawa Y, Hosoi M, Oka K, Hori T. Intracerebroventricular injection of tumor necrosis factor-alpha induces thermal hyperalgesia in rats. Neuroimmunomodulation. 1996;3(2–3):135–40.PubMedCrossRef
56.
Oka T, Oka K, Hori T. Mechanisms and mediators of psychological stress-induced rise in core temperature. Psychosom Med. 2001;63(3):476–86.PubMedCrossRef
57.
Montoya JG, Holmes TH, Anderson JN, Maecker HT, Rosenberg-Hasson Y, Valencia IJ, Chu L, Younger JW, Tato CM, Davis MM. Cytokine signature associated with disease severity in chronic fatigue syndrome patients. Proc Natl Acad Sci U S A. 2017;114(34):E7150-8.CrossRef
58.
59.
Blundell S, Ray KK, Buckland M, White PD. Chronic fatigue syndrome and circulating cytokines: a systematic review. Brain Behav Immun. 2015;50:186–95.PubMedCrossRef
60.
Pal R, Singh SN, Chatterjee A, Saha M. Age-related changes in cardiovascular system, autonomic functions, and levels of BDNF of healthy active males: role of yogic practice. Age (Dordr). 2014;36(4):9683.CrossRef
61.
Lee M, Moon W, Kim J. Effect of yoga on pain, brain-derived neurotrophic factor, and serotonin in premenopausal women with chronic low back pain. Evid Based Complement Alternat Med. 2014;2014:203173.PubMedPubMedCentral
62.
Yoshimura R, Nakamura J, Shinkai K, Ueda N. Clinical response to antidepressant treatment and 3-methoxy-4-hydroxyphenylglycol levels: mini review. Prog Neuro-Psychopharmacol Biol Psychiatry. 2004;28(4):611–6.CrossRef
63.
Ben-Jonathan N, Hnasko R. Dopamine as a prolactin (PRL) inhibitor. Endocr Rev. 2001;22(6):724–63.PubMedCrossRef
64.
Ogawa T, Shishioh-Ikejima N, Konishi H, Makino T, Sei H, Kiryu-Seo S, Tanaka M, Watanabe Y, Kiyama H. Chronic stress elicits prolonged activation of alpha-MSH secretion and subsequent degeneration of melanotroph. J Neurochem. 2009;109(5):1389–99.PubMedCrossRef
65.
Sisto SA, Tapp W, Drastal S, Bergen M, DeMasi I, Cordero D, Natelson B. Vagal tone is reduced during paced breathing in patients with the chronic fatigue syndrome. Clin Auton Res. 1995;5(3):139–43.PubMedCrossRef
66.
Yamaguti K, Tajima S, Kuratsune H. Autonomic dysfunction in chronic fatigue syndrome. Adv Neuroimmune Biol. 2013;4:281–9.
67.
Cvejic E, Sandler CX, Keech A, Barry BK, Lloyd AR, Vollmer-Conna U. Autonomic nervous system function, activity patterns, and sleep after physical or cognitive challenge in people with chronic fatigue syndrome. J Psychosom Res. 2017;103:91–4.PubMedCrossRef
68.
Orjatsalo M, Alakuijala A, Partinen M. Autonomic nervous system functioning related to nocturnal sleep in patients with chronic fatigue syndrome compared to tired controls. J Clin Sleep Med. 2018;14(2):163–71.PubMedPubMedCentralCrossRef
69.
70.
Rebouche CJ, Engel AG. Carnitine metabolism and deficiency syndromes. Mayo Clin Proc. 1983;58(8):533–40.PubMed
71.
Groven N, Fors EA, Iversen VC, White LR, Reitan SK. Association between cytokines and psychiatric symptoms in chronic fatigue syndrome and healthy controls. Nord J Psychiatry. 2018:1–5.
72.
Caseras X, Mataix-Cols D, Rimes KA, Giampietro V, Brammer M, Zelaya F, Chalder T, Godfrey E. The neural correlates of fatigue: an exploratory imaginal fatigue provocation study in chronic fatigue syndrome. Psychol Med. 2008;38(7):941–51.PubMedCrossRef
73.
Sepede G, Racciatti D, Gorgoretti V, Nacci M, Pizzigallo E, Onofrj M, Di Giannantonio M, Niolu C, Salerno RM, Gambi F. Psychophysical distress and alexithymic traits in chronic fatigue syndrome with and without comorbid depression. Int J Immunopathol Pharmacol. 2011;24(4):1017–25.PubMedCrossRef
74.
Moriguchi Y, Maeda M, Igarashi T, Ishikawa T, Shoji M, Kubo C, Komaki G. Age and gender effect on alexithymia in large, Japanese community and clinical samples: a cross-validation study of the Toronto alexithymia scale (TAS-20). Biopsychosoc Med. 2007;1:7.PubMedPubMedCentralCrossRef
75.
Oka T, Wakita H, Kimura K. Development of a recumbent isometric yoga program for patients with severe chronic fatigue syndrome/myalgic encephalomyelitis: a pilot study to assess feasibility and efficacy. Biopsychosoc Med. 2017;11:5.PubMedPubMedCentralCrossRef
76.
Nakatomi Y, Mizuno K, Ishii A, Wada Y, Tanaka M, Tazawa S, Onoe K, Fukuda S, Kawabe J, Takahashi K, et al. Neuroinflammation in patients with chronic fatigue syndrome/myalgic encephalomyelitis: an (1)(1)C-(R)-PK11195 PET study. J Nucl Med. 2014;55(6):945–50.PubMedCrossRef
Metadata
Title
The longitudinal effects of seated isometric yoga on blood biomarkers, autonomic functions, and psychological parameters of patients with chronic fatigue syndrome: a pilot study
Authors
Takakazu Oka
Tokusei Tanahashi
Battuvshin Lkhagvasuren
Yu Yamada
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BioPsychoSocial Medicine / Issue 1/2019
Electronic ISSN: 1751-0759
DOI
https://doi.org/10.1186/s13030-019-0168-x

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