Central Autonomic Network Disturbance in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome: A Pilot Study
A Pilot Study
DOI:
https://doi.org/10.15540/nr.8.2.73Keywords:
chronic fatigue syndrome; myalgic encephalomyelitis; central autonomic network; handgrip; post-exertional malaise; eLORETA; central fatigueAbstract
Myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) is a debilitating disease of the central nervous system known to be associated with multiple behavioral symptoms (fatigue, low stamina, dizziness, etc.) combined with autonomic nervous system (ANS) dysfunction, thus implicating the central autonomic network (CAN). Post-exertional malaise (PEM) is a core feature of ME/CFS, characterized by a pathological reduction in stamina in response to performing minor physical or mental tasks, often lasting at least 24 hours. Exact low-resolution electromagnetic tomography (eLORETA) allows non-invasive investigation of cortical regions of interest that may contribute to better understanding of the role of the brain disturbances in behavioral manifestations of PEM. This pilot study therefore aimed to use eLORETA to characterize changes in current density in cortical structures related to the CAN following submaximal isometric handgrip exercise in 7 patients with ME/CFS and 6 neurotypical healthy controls (HCs). Resting EEG was recorded at pre-, post- handgrip, and 24 hours later. Findings showed that significant differences occurred immediately post-test, which were most pronounced after 24 hours, particularly in the low alpha (8-10 Hz) and low beta (13-18 Hz) frequency sub-bands. Together, the present findings offer support for EEG source localization techniques to investigate PEM. If confirmed, this study could provide a useful instrument for functional diagnosis and evaluation of treatment outcomes.
References
Allen, G. V., Saper, C. B., Hurley, K. M., & Cechetto, D. F. (1991). Organization of visceral and limbic connections in the insular cortex of the rat. The Journal of Comparative Neurology, 311(1), 1–16. https://doi.org/10.1002/cne.903110102
Amann, M., & Calbet, J. A. L. (2008). Convective oxygen transport and fatigue. Journal of Applied Physiology, 104(3), 861–870. https://doi.org/10.1152/japplphysiol.01008.2007
Aoki, Y., Kazui, H., Pascal-Marqui, R. D., Ishii, R., Yoshiyama, K., Kanemoto, H., Suzuki, Y., Sato, S., Hata, M., Canuet, L., Iwase, M., & Ikeda, M. (2019). EEG Resting-State Networks in Dementia with Lewy Bodies Associated with Clinical Symptoms. Neuropsychobiology, 77(4), 206–218. https://doi.org/10.1159/000495620
Babiloni, C., Visser, P. J., Frisoni, G., De Deyn, P. P., Bresciani, L., Jelic, V., Nagels, G., Rodriguez, G., Rossini, P. M., Vecchio, F., Colombo, D., Verhey, F., Wahlund, L. O., & Nobili, F. (2010). Cortical sources of resting EEG rhythms in mild cognitive impairment and subjective memory complaint. Neurobiological Aging, 31(10), 1787–1798. https://doi.org/10.1016/j.neurobiolaging.2008.09.020
Bansal, A. S., Bradley, A. S., Bishop, K. N., Kiani-Alikhan, S., & Ford, B. (2012). Chronic fatigue syndrome, the immune system and viral infection. Brain Behav Immun, 26(1), 24–31. https://doi.org/10.1016/j.bbi.2011.06.016
Barah, F., Whiteside, S., Batista, S., & Morris, J. (2014). Neurological aspects of human parvovirus B19 infection: A systematic review. Reviews in Medical Virology, 24(3), 154–168. https://doi.org/10.1002/rmv.1782
Barnden, L. R., Kwiatek, R., Crouch, B., Burnet, R., & Del Fante, P. (2016). Autonomic correlations with MRI are abnormal in the brainstem vasomotor centre in Chronic Fatigue Syndrome. Neuroimage Clin, 11, 530–537. https://doi.org/10.1016/j.nicl.2016.03.017
Beaumont, A., Burton, A. R., Lemon, J., Bennett, B. K., Lloyd, A., & Vollmer-Conna, U. (2012). Reduced cardiac vagal modulation impacts on cognitive performance in chronic fatigue syndrome. PLoS One, 7(11), e49518. https://doi.org/10.1371/journal.pone.0049518
Benarroch, E. (2019). Autonomic nervous system and neuroimmune interactions. Neurology. https://doi.org/10.1212/WNL.0000000000006942
Benarroch, E. E. (1993). The central autonomic network: Functional organization, dysfunction, and perspective. Mayo Clinic Proceedings, 68(10), 988–1001.
Benarroch, E. E. (2012). Central Autonomic Control. In D. Robertson, I. Biaggioni, G. Burnstock, P. A. Low, & J. F. R. Paton (Eds.), Primer on the autonomic nervous system (3rd ed., pp. 9–12). Elsevier.
Benwell, N. M., Mastaglia, F. L., & Thickbroom, G. W. (2006). Reduced functional activation after fatiguing exercise is not confined to primary motor areas. Experimental Brain Research, 175(4), 575–583. https://doi.org/10.1007/s00221-006-0573-9
Berelowitz, G. J., Burgess, A. P., Thanabalasingham, T., Murray-Lyon, I. M., & Wright, D. J. (1995). Post-hepatitis syndrome revisited. Journal of Viral Hepatitis, 2(3), 133–138.
Bozzini, S., Albergati, A., Capelli, E., Lorusso, L., Gazzaruso, C., Pelissero, G., & Falcone, C. (2018). Cardiovascular characteristics of chronic fatigue syndrome. Biomedical Reports, 8(1), 26–30. https://doi.org/10.3892/br.2017.1024
Brett, M., Johnsrude, I. S., & Owen, A. M. (2002). The problem of functional localization in the human brain. Nature Reviews. Neuroscience, 3(3), 243–249. https://doi.org/10.1038/nrn756
Busch, N. A., Dubois, J., & VanRullen, R. (2009). The phase of ongoing EEG oscillations predicts visual perception. J Neurosci, 29(24), 7869–7876. https://doi.org/10.1523/jneurosci.0113-09.2009
Buzsaki, G., & Watson, B. O. (2012). Brain rhythms and neural syntax: Implications for efficient coding of cognitive content and neuropsychiatric disease. Dialogues Clin Neurosci, 14(4), 345–367.
Cambras, T., Castro-Marrero, J., Zaragoza, M. C., Díez-Noguera, A., & Alegre, J. (2018). Circadian rhythm abnormalities and autonomic dysfunction in patients with Chronic Fatigue Syndrome/Myalgic Encephalomyelitis. PloS One, 13(6), e0198106. https://doi.org/10.1371/journal.pone.0198106
Canuet, L., Tellado, I., Couceiro, V., Fraile, C., Fernandez-Novoa, L., Ishii, R., Takeda, M., & Cacabelos, R. (2012). Resting-state network disruption and APOE genotype in Alzheimer’s disease: A lagged functional connectivity study. PLoS One, 7(9), e46289. https://doi.org/10.1371/journal.pone.0046289
Cao, C., & Slobounov, S. (2010). Alteration of cortical functional connectivity as a result of traumatic brain injury revealed by graph theory, ICA, and sLORETA analyses of EEG signals. IEEE Trans Neural Syst Rehabil Eng, 18(1), 11–19. https://doi.org/10.1109/tnsre.2009.2027704
Carruthers, B.M., van de Sande, M. I., De Meirleir, K. L., Klimas, N. G., Broderick, G., Mitchell, T., Staines, D., Powles, P., Speight, N., Vallings, R., Bateman, L., Baumgarten- Austrheim, B., Bell, D. S., Carlo- Stella, N., Chia, J., Darragh, A., Jo, D., Lewis, D., Light, A. R., … Stevens, S. (2011). Myalgic Encephalomyelitis: International Consensus Criteria. Journal of Internal Medicine. https://doi.org/10.1111/j.1365-2796.2011.02428.x
Carruthers, Bruce M., Jain, A. K., Meirleir, K. L. D., Peterson, D. L., Klimas, N. G., Lerner, A. M., Bested, A. C., Flor-Henry, P., Joshi, P., Powles, A. C. P., Sherkey, J. A., & Sande, M. I. van de. (2003). Myalgic Encephalomyelitis/Chronic Fatigue Syndrome. Journal of Chronic Fatigue Syndrome, 11(1), 7–115. https://doi.org/10.1300/J092v11n01_02
Caso, F., Cursi, M., Magnani, G., Fanelli, G., Falautano, M., Comi, G., Leocani, L., & Minicucci, F. (2012). Quantitative EEG and LORETA: valuable tools in discerning FTD from AD? Neurobiol Aging, 33(10), 2343–2356. https://doi.org/10.1016/j.neurobiolaging.2011.12.011
Chaudhuri, A., & Behan, P. O. (2004). Fatigue in neurological disorders. The Lancet, 363(9413), 978–988. https://doi.org/10.1016/S0140-6736(04)15794-2
Chen, R., Liang, F. X., Moriya, J., Yamakawa, J., Sumino, H., Kanda, T., & Takahashi, T. (2008). Chronic fatigue syndrome and the central nervous system. J Int Med Res, 36(5), 867–874.
Cho, H. J., Skowera, A., Cleare, A., & Wessely, S. (2006). Chronic fatigue syndrome: An update focusing on phenomenology and pathophysiology. Curr Opin Psychiatry, 19(1), 67–73. https://doi.org/10.1097/01.yco.0000194370.40062.b0
Cleare, A. J. (2004). The HPA axis and the genesis of chronic fatigue syndrome. Trends Endocrinol Metab, 15(2), 55–59. https://doi.org/10.1016/j.tem.2003.12.002
Clemens, B., Bank, J., Piros, P., Bessenyei, M., Veto, S., Toth, M., & Kondakor, I. (2008). Three-dimensional localization of abnormal EEG activity in migraine: A low resolution electromagnetic tomography (LORETA) study of migraine patients in the pain-free interval. Brain Topogr, 21(1), 36–42. https://doi.org/10.1007/s10548-008-0061-6
Clemens, B., Bessenyei, M., Fekete, I., Puskás, S., Kondákor, I., Tóth, M., & Hollódy, K. (2010). Theta EEG source localization using LORETA in partial epilepsy patients with and without medication. Clinical Neurophysiology, 121(6), 848–858. https://doi.org/10.1016/j.clinph.2010.01.020
Cockshell, S. J., & Mathias, J. L. (2014). Cognitive functioning in people with chronic fatigue syndrome: A comparison between subjective and objective measures. Neuropsychology, 28(3), 394–405. https://doi.org/10.1037/neu0000025
Cook, D. B., Stegner, A. J., Nagelkirk, P. R., Meyer, J. D., Togo, F., & Natelson, B. H. (2012). Responses to Exercise Differ For Chronic Fatigue Syndrome Patients with Fibromyalgia. Medicine and Science in Sports and Exercise, 44(6), 1186–1193. https://doi.org/10.1249/MSS.0b013e3182417b9a
Cutsforth-Gregory, J. K., & Benarroch, E. E. (2017). Nucleus of the solitary tract, medullary reflexes, and clinical implications. Neurology, 88(12), 1187. https://doi.org/10.1212/WNL.0000000000003751
Cvejic, E., Sandler, C. X., Keech, A., Barry, B. K., Lloyd, A. R., & Vollmer-Conna, U. (2017). Autonomic nervous system function, activity patterns, and sleep after physical or cognitive challenge in people with chronic fatigue syndrome. Journal of Psychosomatic Research, 103, 91–94. https://doi.org/10.1016/j.jpsychores.2017.10.010
Demitrack, M. A., Dale, J. K., Straus, S. E., Laue, L., Listwak, S. J., Kruesi, M. J., Chrousos, G. P., & Gold, P. W. (1991). Evidence for impaired activation of the hypothalamic-pituitary-adrenal axis in patients with chronic fatigue syndrome. The Journal of Clinical Endocrinology and Metabolism, 73(6), 1224–1234. https://doi.org/10.1210/jcem-73-6-1224
Dierks, T., Jelic, V., Pascual-Marqui, R. D., Wahlund, L., Julin, P., Linden, D. E., Maurer, K., Winblad, B., & Nordberg, A. (2000). Spatial pattern of cerebral glucose metabolism (PET) correlates with localization of intracerebral EEG-generators in Alzheimer’s disease. Clin Neurophysiol, 111(10), 1817–1824.
Fuchs, M., Kastner, J., Wagner, M., Hawes, S., & Ebersole, J. S. (2002). A standardized boundary element method volume conductor model. Clin Neurophysiol, 113(5), 702–712.
Fukuda, K., Straus, S. E., Hickie, I., Sharpe, M. C., Dobbins, J. G., & Komaroff, A. (1994). The chronic fatigue syndrome: A comprehensive approach to its definition and study. Ann Intern Med, 121(12), 953–959.
Gianotti, L. R., Kunig, G., Lehmann, D., Faber, P. L., Pascual-Marqui, R. D., Kochi, K., & Schreiter-Gasser, U. (2007). Correlation between disease severity and brain electric LORETA tomography in Alzheimer’s disease. Clin Neurophysiol, 118(1), 186–196. https://doi.org/10.1016/j.clinph.2006.09.007
Grech, R., Cassar, T., Muscat, J., Camilleri, K. P., Fabri, S. G., Zervakis, M., Xanthopoulos, P., Sakkalis, V., & Vanrumste, B. (2008). Review on solving the inverse problem in EEG source analysis. J Neuroeng Rehabil, 5, 25. https://doi.org/10.1186/1743-0003-5-25
Guntekin, B., Emek-Savas, D. D., Kurt, P., Yener, G. G., & Basar, E. (2013). Beta oscillatory responses in healthy subjects and subjects with mild cognitive impairment. Neuroimage Clin, 3, 39–46. https://doi.org/10.1016/j.nicl.2013.07.003
Gunzelmann, G., M James, S., & Caldwell, J. L. (2019). Basic and applied science interactions in fatigue understanding and risk mitigation. Progress in Brain Research, 246, 177–204. https://doi.org/10.1016/bs.pbr.2019.03.022
Harris, P. A., Taylor, R., Thielke, R., Payne, J., Gonzalez, N., & Conde, J. G. (2009). Research electronic data capture (REDCap)—A metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform, 42(2), 377–381. https://doi.org/10.1016/j.jbi.2008.08.010
Hata, M., Kazui, H., Tanaka, T., Ishii, R., Canuet, L., Pascual-Marqui, R. D., Aoki, Y., Ikeda, S., Kanemoto, H., Yoshiyama, K., Iwase, M., & Takeda, M. (2016). Functional connectivity assessed by resting state EEG correlates with cognitive decline of Alzheimer’s disease: An eLORETA study. Clin Neurophysiol, 127(2), 1269–1278. https://doi.org/10.1016/j.clinph.2015.10.030
Heister, D., Diwakar, M., Nichols, S., Robb, A., Angeles, A. M., Tal, O., Harrington, D. L., Song, T., Lee, R. R., & Huang, M. (2013). Resting-state neuronal oscillatory correlates of working memory performance. PLoS One, 8(6), e66820. https://doi.org/10.1371/journal.pone.0066820
Hilty, L., Jancke, L., Luechinger, R., Boutellier, U., & Lutz, K. (2011). Limitation of physical performance in a muscle fatiguing handgrip exercise is mediated by thalamo-insular activity. Hum Brain Mapp, 32(12), 2151–2160. https://doi.org/10.1002/hbm.21177
Hilty, Lea, Langer, N., Pascual-Marqui, R., Boutellier, U., & Lutz, K. (2011). Fatigue-induced increase in intracortical communication between mid/anterior insular and motor cortex during cycling exercise. European Journal of Neuroscience, 34(12), 2035–2042. a2h. https://doi.org/10.1111/j.1460-9568.2011.07909.x
Holgate, S. T., Komaroff, A. L., Mangan, D., & Wessely, S. (2011). Chronic fatigue syndrome: Understanding a complex illness. Nat Rev Neurosci, 12(9), 539–544. https://doi.org/10.1038/nrn3087
Ickmans, K., Meeus, M., De Kooning, M., Lambrecht, L., Pattyn, N., & Nijs, J. (2014). Can recovery of peripheral muscle function predict cognitive task performance in chronic fatigue syndrome with and without fibromyalgia? Phys Ther, 94(4), 511–522. https://doi.org/10.2522/ptj.20130367
Institute of Medicine. (2015). Beyond Myalgic Encephalomyelitis/Chronic Fatigue Syndrome: Redefining an Illness (25695122). National Academies Press. https://doi.org/10.17226/19012
Jammes, Y., Stavris, C., Charpin, C., Rebaudet, S., Lagrange, G., Stavris, C., & Retornaz, F. (2020). Maximal handgrip strength can predict maximal physical performance in patients with chronic fatigue. Clinical Biomechanics. https://doi.org/10.1016/j.clinbiomech.2020.01.003
Jason, L. A., Evans, M., Porter, N., Brown, A., Brown, M., Hunnell, J., Anderson, V., Lerch, A., DeMeirleir, K., & Friedberg, F. (2010). The development of a revised Canadian myalgic encephalomyelitis-chronic fatigue syndrome case definition. Am J Biochem Biotechnol, 6(2), 120-135.
Jason, Leonard A., So, S., Brown, A. A., Sunnquist, M., & Evans, M. (2015). Test–retest reliability of the DePaul Symptom Questionnaire. In Fatigue: Biomedicine, Health & Behavior (Vol. 3, pp. 16–32). Taylor & Francis. https://doi.org/10.1080/21641846.2014.978110
Jeppesen, T. D., Quistorff, B., Wibrand, F., & Vissing, J. (2007). 31P-MRS of skeletal muscle is not a sensitive diagnostic test for mitochondrial myopathy. Journal of Neurology, 254(1), 29–37. https://doi.org/10.1007/s00415-006-0229-5
LaManca, J. J., Sisto, S. A., DeLuca, J., Johnson, S. K., Lange, G., Pareja, J., Cook, S., & Natelson, B. H. (1998). Influence of exhaustive treadmill exercise on cognitive functioning in chronic fatigue syndrome. Am J Med, 105(3a), 59s–65s.
Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., Kochunov, P. V., Nickerson, D., Mikiten, S. A., & Fox, P. T. (2000). Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp, 10(3), 120–131.
Lantz, G., Michel, C. M., Pascual-Marqui, R. D., Spinelli, L., Seeck, M., Seri, S., Landis, T., & Rosen, I. (1997). Extracranial localization of intracranial interictal epileptiform activity using LORETA (low resolution electromagnetic tomography). Electroencephalogr Clin Neurophysiol, 102(5), 414–422.
Light, A. R., Bateman, L., Jo, D., Hughen, R. W., Vanhaitsma, T. A., White, A. T., & Light, K. C. (2012). Gene expression alterations at baseline and following moderate exercise in patients with Chronic Fatigue Syndrome and Fibromyalgia Syndrome. J Intern Med, 271(1), 64–81. https://doi.org/10.1111/j.1365-2796.2011.02405.x
Light, A. R., White, A. T., Hughen, R. W., & Light, K. C. (2009). Moderate exercise increases expression for sensory adrenergic and immune genes in chronic fatigue syndrome patients but not in normal subjects. The Journal of Pain, 10(10), 1099–1112. https://doi.org/10.1016/j.pain.2009.06.003
Loebel, M., Strohschein, K., Giannini, C., Koelsch, U., Bauer, S., Doebis, C., Thomas, S., Unterwalder, N., von Baehr, V., Reinke, P., Knops, M., Hanitsch, L. G., Meisel, C., Volk, H. D., & Scheibenbogen, C. (2014). Deficient EBV-specific B- and T-cell response in patients with chronic fatigue syndrome. PLoS One, 9(1), e85387. https://doi.org/10.1371/journal.pone.0085387
Lubar, J. F., Congedo, M., & Askew, J. H. (2003). Low-resolution electromagnetic tomography (LORETA) of cerebral activity in chronic depressive disorder. Int J Psychophysiol, 49(3), 175–185.
Maes, M., Twisk, F. N., Kubera, M., & Ringel, K. (2012). 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, 136(3), 933–939. https://doi.org/10.1016/j.jad.2011.09.004
Mathias, C. J., & Bannister, R. (Eds.). (2013). Autonomic Failure: A Textbook of Clinical Disorders of the Autonomic Nervous System (5th ed.). Oxford Univeristy Press.
Mazziotta, J., Toga, A., Evans, A., Fox, P., Lancaster, J., Zilles, K., Woods, R., Paus, T., Simpson, G., Pike, B., Holmes, C., Collins, L., Thompson, P., MacDonald, D., Iacoboni, M., Schormann, T., Amunts, K., Palomero-Gallagher, N., Geyer, S., … Mazoyer, B. (2001). A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci, 356(1412), 1293–1322. https://doi.org/10.1098/rstb.2001.0915
McEwen, B. S., Bowles, N. P., Gray, J. D., Hill, M. N., Hunter, R. G., Karatsoreos, I. N., & Nasca, C. (2015). Mechanisms of stress in the brain. Nat Neurosci, 18(10), 1353–1363. https://doi.org/10.1038/nn.4086
Meeus, M., Nijs, J., & Meirleir, K. D. (2007). Chronic musculoskeletal pain in patients with the chronic fatigue syndrome: A systematic review. Eur J Pain, 11(4), 377–386. https://doi.org/10.1016/j.ejpain.2006.06.005
Meulemans, A., Gerlo, E., Seneca, S., Lissens, W., Smet, J., Van Coster, R., & De Meirleir, L. (2007). The aerobic forearm exercise test, a non-invasive tool to screen for mitochondrial disorders. Acta Neurologica Belgica, 107(3), 78–83.
Miraglia, F., Tomino, C., Vecchio, F., Alù, F., Orticoni, A., Judica, E., Cotelli, M., & Rossini, P. M. (2020). Assessing the dependence of the number of EEG channels in the brain networks’ modulations. Brain Research Bulletin. https://doi.org/10.1016/j.brainresbull.2020.11.014
Mo, J., Huang, L., Peng, J., Ocak, U., Zhang, J., & Zhang, J. H. (2019). Autonomic Disturbances in Acute Cerebrovascular Disease. Neuroscience Bulletin, 35(1), 133–144. https://doi.org/10.1007/s12264-018-0299-2
Morrison, S. F., & Nakamura, K. (2019). Central Mechanisms for Thermoregulation. Annual Review of Physiology, 81(1), null. https://doi.org/10.1146/annurev-physiol-020518-114546
Mulert, C., Jager, L., Schmitt, R., Bussfeld, P., Pogarell, O., Moller, H. J., Juckel, G., & Hegerl, U. (2004). Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage, 22(1), 83–94. https://doi.org/10.1016/j.neuroimage.2003.10.051
Nacul, L. C., Mudie, K., Kingdon, C. C., Clark, T. G., & Lacerda, E. M. (2018). Hand Grip Strength as a Clinical Biomarker for ME/CFS and Disease Severity. Frontiers in Neurology, 9. https://doi.org/10.3389/fneur.2018.00992
Nakatomi, Y., Mizuno, K., Ishii, A., Wada, Y., Tanaka, M., Tazawa, S., Onoe, K., Fukuda, S., Kawabe, J., Takahashi, K., Kataoka, Y., Shiomi, S., Yamaguti, K., Inaba, M., Kuratsune, H., & Watanabe, Y. (2014). Neuroinflammation in Patients with Chronic Fatigue Syndrome/Myalgic Encephalomyelitis: An 11C-(R)-PK11195 PET Study. Journal of Nuclear Medicine: Official Publication, Society of Nuclear Medicine, 55(6), 945–950. https://doi.org/10.2967/jnumed.113.131045
Naviaux, R. K., Naviaux, J. C., Li, K., Bright, A. T., Alaynick, W. A., Wang, L., Baxter, A., Nathan, N., Anderson, W., & Gordon, E. (2016). Metabolic features of chronic fatigue syndrome. Proceedings of the National Academy of Sciences of the United States of America, 113(37), E5472–E5480. https://doi.org/10.1073/pnas.1607571113
Neu, D., Mairesse, O., Montana, X., Gilson, M., Corazza, F., Lefevre, N., Linkowski, P., Le Bon, O., & Verbanck, P. (2014). Dimensions of pure chronic fatigue: Psychophysical, cognitive and biological correlates in the chronic fatigue syndrome. European Journal of Applied Physiology, 114(9), 1841–1851. https://doi.org/10.1007/s00421-014-2910-1
Nielsen, S. E., & Mather, M. (2015). Comparison of two isometric handgrip protocols on sympathetic arousal in women. Physiology & Behavior, 142, 5–13. https://doi.org/10.1016/j.physbeh.2015.01.031
Nijs, J., Van Oosterwijck, J., Meeus, M., Lambrecht, L., Metzger, K., Fremont, M., & Paul, L. (2010). Unravelling the nature of postexertional malaise in myalgic encephalomyelitis/chronic fatigue syndrome: The role of elastase, complement C4a and interleukin-1beta. J Intern Med, 267(4), 418–435. https://doi.org/10.1111/j.1365-2796.2009.02178.x
Nishida, K., Yoshimura, M., Isotani, T., Yoshida, T., Kitaura, Y., Saito, A., Mii, H., Kato, M., Takekita, Y., Suwa, A., Morita, S., & Kinoshita, T. (2011). Differences in quantitative EEG between frontotemporal dementia and Alzheimer’s disease as revealed by LORETA. Clin Neurophysiol, 122(9), 1718–1725. https://doi.org/10.1016/j.clinph.2011.02.011
Norman, K., Stobäus, N., Smoliner, C., Zocher, D., Scheufele, R., Valentini, L., Lochs, H., & Pirlich, M. (2010). Determinants of hand grip strength, knee extension strength and functional status in cancer patients. Clinical Nutrition (Edinburgh, Scotland), 29(5), 586–591. https://doi.org/10.1016/j.clnu.2010.02.007
Ohashi, K., Yamamoto, Y., & Natelson, B. H. (2002). Activity rhythm degrades after strenuous exercise in chronic fatigue syndrome. Physiol Behav, 77(1), 39–44.
Oosterwijck, J. V., Marusic, U., De Wandele, I., Paul, L., Meeus, M., Moorkens, G., Lambrecht, L., Danneels, L., & Nijs, J. (2017). The Role of Autonomic Function in Exercise-induced Endogenous Analgesia: A Case-control Study in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome and Healthy People. Pain Physician, 20(3), E389–E399.
Orjatsalo, M., Alakuijala, A., & Partinen, M. (2018). Autonomic Nervous System Functioning Related to Nocturnal Sleep in Patients With Chronic Fatigue Syndrome Compared to Tired Controls. Journal of Clinical Sleep Medicine: JCSM: Official Publication of the American Academy of Sleep Medicine, 14(2), 163–171. https://doi.org/10.5664/jcsm.6924
Pajediene, E., Bileviciute-Ljungar, I., & Friberg, D. (2018). Sleep patterns among patients with chronic fatigue: A polysomnography-based study. The Clinical Respiratory Journal, 12(4), 1389–1397. https://doi.org/10.1111/crj.12667
Palva, J. M., Palva, S., & Kaila, K. (2005). Phase synchrony among neuronal oscillations in the human cortex. J Neurosci, 25(15), 3962–3972. https://doi.org/10.1523/jneurosci.4250-04.2005
Papadopoulos, A. S., & Cleare, A. J. (2012). Hypothalamic-pituitary-adrenal axis dysfunction in chronic fatigue syndrome. Nat Rev Endocrinol, 8(1), 22–32. https://doi.org/10.1038/nrendo.2011.153
Parker, A. J., Wessely, S., & Cleare, A. J. (2001). The neuroendocrinology of chronic fatigue syndrome and fibromyalgia. Psychol Med, 31(8), 1331–1345.
Pascual-Marqui, R. D. (2002). Standardized low-resolution brain electromagnetic tomography (sLORETA): Technical details. Methods Find Exp Clin Pharmacol, 24 Suppl D, 5–12.
Pascual-Marqui, R. D., Lehmann, D., Koukkou, M., Kochi, K., Anderer, P., Saletu, B., Tanaka, H., Hirata, K., John, E. R., Prichep, L., Biscay-Lirio, R., & Kinoshita, T. (2011). Assessing interactions in the brain with exact low-resolution electromagnetic tomography. Philos Trans A Math Phys Eng Sci, 369(1952), 3768–3784. https://doi.org/10.1098/rsta.2011.0081
Pascual-Marqui, R. D., Michel, C. M., & Lehmann, D. (1994). Low resolution electromagnetic tomography: A new method for localizing electrical activity in the brain. Int J Psychophysiol, 18(1), 49–65.
Pendergrast, T., Brown, A., Sunnquist, M., Jantke, R., Newton, J. L., Strand, E. B., & Jason, L. A. (2016). Housebound versus nonhousebound patients with myalgic encephalomyelitis and chronic fatigue syndrome. Chronic Illness, 12(4), 292–307. https://doi.org/10.1177/1742395316644770
Pfaff, D. W., Kieffer, B. L., & Swanson, L. W. (2008). Mechanisms for the Regulation of State Changes in the Central Nervous System. Annals of the New York Academy of Sciences, 1129(1), 1–7. https://doi.org/10.1196/annals.1417.031
Pizzagalli, D. A., Oakes, T. R., Fox, A. S., Chung, M. K., Larson, C. L., Abercrombie, H. C., Schaefer, S. M., Benca, R. M., & Davidson, R. J. (2004). Functional but not structural subgenual prefrontal cortex abnormalities in melancholia. Mol Psychiatry, 9(4), 325, 393–405. https://doi.org/10.1038/sj.mp.4001469
Porges, S. W. (1992). Vagal tone: A physiologic marker of stress vulnerability. Pediatrics, 90(3 Pt 2), 498–504.
Porges, S. W. (2009). The polyvagal theory: New insights into adaptive reactions of the autonomic nervous system. Cleveland Clinic Journal of Medicine, 76(Suppl 2), S86–S90. https://doi.org/10.3949/ccjm.76.s2.17
Rasa, S., Nora-Krukle, Z., Henning, N., Eliassen, E., Shikova, E., Harrer, T., Scheibenbogen, C., Murovska, M., Prusty, B. K., & European Network on ME/CFS (EUROMENE). (2018). Chronic viral infections in myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS). Journal of Translational Medicine, 16(1), 268. https://doi.org/10.1186/s12967-018-1644-y
Roerink, M. E., Roerink, S. H. P. P., Skoluda, N., van der Schaaf, M. E., Hermus, A. R. M. M., van der Meer, J. W. M., Knoop, H., & Nater, U. M. (2018). Hair and salivary cortisol in a cohort of women with chronic fatigue syndrome. Hormones and Behavior, 103, 1–6. https://doi.org/10.1016/j.yhbeh.2018.05.016
Roos, K. L., & Miravalle, A. (2014). Postinfectious encephalomyelitis. In W. M. Scheld, R. J. Whitley, & C. M. Marra (Eds.), Infections of the Central Nervous System (4th ed., pp. 331–339). Wolters Kluwer Health.
Ropper, A., & Samuels, M. (2009). Principles of Neurology (9th ed.). McGrall Hill.
Sandroni, P. (2012). Clinical Evaluation of Autonomic Disorders. In I. Biaggioni, G. Burnstock, P. A. Low, & J. F. R. Paton (Eds.), Primer on the Autonomic Nervous System (3rd ed., pp. 377–382). Academic Press.
Saper, C. B. (2002). The central autonomic nervous system: Conscious visceral perception and autonomic pattern generation. Annual Review of Neuroscience, 25, 433–469. https://doi.org/10.1146/annurev.neuro.25.032502.111311
Scheld, W. M., Whitley, R. J., & Marra, C. M. (2014). Infections of the Central Nervous System (4th ed.). Lippincott Williams and Wilkins.
Schillings, M. L., Stegeman, D. F., & Zwarts, M. J. (2005). Determining central activation failure and peripheral fatigue in the course of sustained maximal voluntary contractions: A model-based approach. J Appl Physiol (1985), 98(6), 2292–2297. https://doi.org/10.1152/japplphysiol.01342.2004
Sclocco, R., Kim, J., Garcia, R. G., Sheehan, J. D., Beissner, F., Bianchi, A. M., Cerutti, S., Kuo, B., Barbieri, R., & Napadow, V. (2016). Brain Circuitry Supporting Multi-Organ Autonomic Outflow in Response to Nausea. Cerebral Cortex (New York, NY), 26(2), 485–497. https://doi.org/10.1093/cercor/bhu172
Shan, Z. Y., Kwiatek, R., Burnet, R., Del Fante, P., Staines, D. R., Marshall‐Gradisnik, S. M., & Barnden, L. R. (2016). Progressive brain changes in patients with chronic fatigue syndrome: A longitudinal MRI study. Journal of Magnetic Resonance Imaging, 44(5), 1301–1311. https://doi.org/10.1002/jmri.25283
Sharma, Y., Xu, T., Graf, W. M., Fobbs, A., Sherwood, C. C., Hof, P. R., Allman, J. M., & Manaye, K. F. (2010). Comparative anatomy of the locus coeruleus in humans and nonhuman primates. The Journal of Comparative Neurology, 518(7), 963–971. https://doi.org/10.1002/cne.22249
Shungu, D. C., Weiduschat, N., Murrough, J. W., Mao, X., Pillemer, S., Dyke, J. P., Medow, M. S., Natelson, B. H., Stewart, J. M., & Mathew, S. J. (2012). Increased ventricular lactate in chronic fatigue syndrome. III. Relationships to cortical glutathione and clinical symptoms implicate oxidative stress in disorder pathophysiology. NMR Biomed, 25(9), 1073–1087. https://doi.org/10.1002/nbm.2772
Siemionow, V., Fang, Y., Calabrese, L., Sahgal, V., & Yue, G. H. (2004). Altered central nervous system signal during motor performance in chronic fatigue syndrome. Clin Neurophysiol, 115(10), 2372–2381. https://doi.org/10.1016/j.clinph.2004.05.012
Snell, C. R., Stevens, S. R., E., D. T., & VanNess, J. M. (2013). Discriminative Validity of metabolic and workload measurements to identify individuals with chronic fatigue syndrome. Physical Therapy, 93(11), 1484–1492. https://doi.org/10.2522/ptj.20110368
Staud, R., Mokthech, M., Price, D. D., & Robinson, M. E. (2015). Evidence for Sensitized Fatigue Pathways in Patients with Chronic Fatigue Syndrome. Pain, 156(4), 750–759. https://doi.org/10.1097/j.pain.0000000000000110
Sterman, M. B., & Kaiser, D. A. (2000). Automatic artifact detection, overlapping windows, and state transitions. Journal of Neurotherapy, 4(3), 85–92.
Stevens, S., Snell, C., Stevens, J., Keller, B., & VanNess, J. M. (2018). Cardiopulmonary Exercise Test Methodology for Assessing Exertion Intolerance in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome. Frontiers in Pediatrics, 6. https://doi.org/10.3389/fped.2018.00242
Tanaka, M., Tajima, S., Mizuno, K., Ishii, A., Konishi, Y., Miike, T., & Watanabe, Y. (2015). Frontier studies on fatigue, autonomic nerve dysfunction, and sleep-rhythm disorder. The Journal of Physiological Sciences, 65(6), 483–498. https://doi.org/10.1007/s12576-015-0399-y
Tatsuoka, M. M., & Lohnes, P. R. (1988). Multivariate analysis: Techniques for educational and psychological research, 2nd ed. Macmillan Publishing Co, Inc.
Teresa Pascarelli, M., Del Percio, C., Francesca De Pandis, M., Ferri, R., Lizio, R., Noce, G., Lopez, S., Rizzo, M., Soricelli, A., Nobili, F., Arnaldi, D., Famà, F., Orzi, F., Buttinelli, C., Giubilei, F., Salvetti, M., Cipollini, V., Franciotti, R., Onofri, M., … Babiloni, C. (2020). Abnormalities of resting-state EEG in patients with prodromal and overt dementia with Lewy bodies: Relation to clinical symptoms. Clinical Neurophysiology. https://doi.org/10.1016/j.clinph.2020.09.004
Togo, F., & Natelson, B. H. (2013). Heart rate variability during sleep and subsequent sleepiness in patients with chronic fatigue syndrome. Auton Neurosci, 176(1–2), 85–90. https://doi.org/10.1016/j.autneu.2013.02.015
Topolovec, J. C., Gati, J. S., Menon, R. S., Shoemaker, J. K., & Cechetto, D. F. (2004). Human cardiovascular and gustatory brainstem sites observed by functional magnetic resonance imaging. Journal of Comparative Neurology, 471(4), 446–461. https://doi.org/10.1002/cne.20033
Toth, M., Faludi, B., Wackermann, J., Czopf, J., & Kondakor, I. (2009). Characteristic changes in brain electrical activity due to chronic hypoxia in patients with obstructive sleep apnea syndrome (OSAS): A combined EEG study using LORETA and omega complexity. Brain Topogr, 22(3), 185–190. https://doi.org/10.1007/s10548-009-0110-9
Turkeltaub, P. E., Eden, G. F., Jones, K. M., & Zeffiro, T. A. (2002). Meta-analysis of the functional neuroanatomy of single-word reading: Method and validation. NeuroImage, 16(3 Pt 1), 765–780.
Underhill, R. A. (2015). Myalgic encephalomyelitis, chronic fatigue syndrome: An infectious disease. Medical Hypotheses, 85(6), 765–773. https://doi.org/10.1016/j.mehy.2015.10.011
Van Cauwenbergh, D., Nijs, J., Kos, D., Van Weijnen, L., Struyf, F., & Meeus, M. (2014). Malfunctioning of the autonomic nervous system in patients with chronic fatigue syndrome: A systematic literature review. Eur J Clin Invest, 44(5), 516–526. https://doi.org/10.1111/eci.12256
Van Den Eede, F., Moorkens, G., Van Houdenhove, B., Cosyns, P., & Claes, S. J. (2007). Hypothalamic-pituitary-adrenal axis function in chronic fatigue syndrome. Neuropsychobiology, 55(2), 112–120. https://doi.org/10.1159/000104468
VanElzakker, M. B., Brumfield, S. A., & Lara Mejia, P. S. (2018). Neuroinflammation and Cytokines in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS): A Critical Review of Research Methods. Frontiers in Neurology, 9, 1033. https://doi.org/10.3389/fneur.2018.01033
VanNess, M., Snell, C. R., & Stevens, S. R. (2007). Diminished cardiopulmonary capacity during post-exertional malaise. Journal of Chronic Fatigue Syndrome, 14(2), 77–85.
Vanneste, S., & Ridder, D. D. (2013). Brain Areas Controlling Heart Rate Variability in Tinnitus and Tinnitus-Related Distress. PLOS ONE, 8(3), e59728. https://doi.org/10.1371/journal.pone.0059728
Vermeulen, R. C., & Vermeulen van Eck, I. W. (2014). Decreased oxygen extraction during cardiopulmonary exercise test in patients with chronic fatigue syndrome. Journal of Translational Medicine, 12, 20. https://doi.org/10.1186/1479-5876-12-20
Vitacco, D., Brandeis, D., Pascual-Marqui, R., & Martin, E. (2002). Correspondence of event-related potential tomography and functional magnetic resonance imaging during language processing. Hum Brain Mapp, 17(1), 4–12. https://doi.org/10.1002/hbm.10038
Ware, J. E., Jr., & Sherbourne, C. D. (1992). The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med Care, 30(6), 473–483.
Ware, J. E., Kosinski, M., Bayliss, M. S., McHorney, C. A., Rogers, W. H., & Raczek, A. (1995). Comparison of methods for the scoring and statistical analysis of SF-36 health profile and summary measures: Summary of results from the Medical Outcomes Study. Medical Care, 33(4 Suppl), AS264-279.
Ware, J. E., Snow, K. K., Kosinski, M., & Gandek, B. (1993). SF-36 health survey: Manual and interpretation guide. New England Medical Center, Health Institute.
Wyller, V. B., Eriksen, H. R., & Malterud, K. (2009). Can sustained arousal explain the Chronic Fatigue Syndrome? Behav Brain Funct, 5, 10. https://doi.org/10.1186/1744-9081-5-10
Yoshiuchi, K., Cook, D. B., Ohashi, K., Kumano, H., Kuboki, T., Yamamoto, Y., & Natelson, B. H. (2007). A real-time assessment of the effect of exercise in chronic fatigue syndrome. Physiol Behav, 92(5), 963–968. https://doi.org/10.1016/j.physbeh.2007.07.001
[Blinded for Review]
Zumsteg, D., Lozano, A. M., & Wennberg, R. A. (2006). Depth electrode recorded cerebral responses with deep brain stimulation of the anterior thalamus for epilepsy. Clinical Neurophysiology, 117(7), 1602–1609. https://doi.org/10.1016/j.clinph.2006.04.008
Zumsteg, D., Lozano, A. M., Wieser, H. G., & Wennberg, R. A. (2006). Cortical activation with deep brain stimulation of the anterior thalamus for epilepsy. Clin Neurophysiol, 117(1), 192–207. https://doi.org/10.1016/j.clinph.2005.09.015
Zumsteg, D., Wennberg, R. A., Treyer, V., Buck, A., & Wieser, H. G. (2005). H2(15)O or 13NH3 PET and electromagnetic tomography (LORETA) during partial status epilepticus. Neurology, 65(10), 1657–1660. https://doi.org/10.1212/01.wnl.0000184516.32369.1a
Zwarts, M. J., Bleijenberg, G., & van Engelen, B. G. M. (2007). Clinical neurophysiology of fatigue. Clinical Neurophysiology, 119(1), 2–10. https://doi.org/10.1016/j.clinph.2007.09.126
Downloads
Published
Issue
Section
License
Authors who publish with this journal agree to the following terms:- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC-BY) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).