Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-17T20:12:46.383Z Has data issue: false hasContentIssue false
  • English
  • Français

Elevated tau and β-amyloid in the serum of fibromyalgia patients

Published online by Cambridge University Press:  07 December 2020

Bich-Hanh Thi Nguy ,
Wen-Te Liu ,
Yu-Tai Chang ,
Chih-Peng Lin  and
Jiunn-Horng Kang Open the ORCID record for Jiunn-Horng Kang [Opens in a new window]
Bich-Hanh Thi Nguy
Affiliation:
Department of Physical Medicine and Rehabilitation, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan The International Master Program in Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan
Wen-Te Liu
Affiliation:
Taipei Neuroscience Institute, Taipei Medical University, Taipei, Taiwan Sleep Center, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan Division of Pulmonary Medicine, Department of Internal Medicine, Shuang Ho Hospital, Taipei Medical University, New Taipei City, Taiwan School of Respiratory Therapy, College of Medicine, Taipei Medical University, Taipei, Taiwan
Yu-Tai Chang
Affiliation:
Department of Physical Medicine and Rehabilitation, Taipei Medical University Hospital, Taipei, Taiwan
Chih-Peng Lin
Affiliation:
Department of Anesthesiology, National Taiwan University Hospital, Taipei, Taiwan Department of Anesthesiology, National Taiwan University College of Medicine, Taipei, Taiwan
Jiunn-Horng Kang*
Affiliation:
Department of Physical Medicine and Rehabilitation, School of Medicine, College of Medicine, Taipei Medical University, Taipei, Taiwan Taipei Neuroscience Institute, Taipei Medical University, Taipei, Taiwan Department of Physical Medicine and Rehabilitation, Taipei Medical University Hospital, Taipei, Taiwan
*
Author for correspondence: Jiunn-Horng Kang, Email: jhk@tmu.edu.tw
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective

Fibromyalgia (FM) is a chronic widespread pain syndrome. Although its mechanism remains relatively unknown, accelerated neurodegeneration in the brain has been reported in patients with FM. Sleep disturbance can increase the risk of neurocognitive disorders, which are associated with tau and beta-amyloid (Aβ) protein accumulation. We hypothesize neurodegeneration in patients with FM may be associated with sleep disturbance.

Methods

In this case-control study, we analyzed serum tau and Aβ levels and their association with symptom profiles for patients with FM, by recruiting 22 patients with FM and 22 age-matched healthy participants. The visual analog scale, Fibromyalgia Impact Questionnaire, pressure pain threshold test, Pittsburgh Sleep Quality Index (PSQI), Beck Depression Inventory-II, Beck Anxiety Inventory, and serum tau and beta-amyloid-42 (Aβ-42) levels were recorded. The Mann–Whitney test was conducted to compare questionnaire and protein level results between the groups. Pearson correlation test was conducted to investigate the correlation of questionnaire scores with tau and Aβ-42 levels in patients with FM. The significance level was set at P < .05.

Results

Serum tau and Aβ-42 levels were significantly higher in patients with FM than in controls. A positive correlation between serum tau levels and PSQI scores was observed in patients with FM (r = 0.476, P = .025). We found that only sleep disturbance in patients with FM was significantly associated with higher serum tau levels among all symptom scores.

Conclusions

We suggest sleep disturbance may play a vital role in the pathomechanism of accelerated neurodegeneration in FM.

Keywords

Fibromyalgiatau proteinbeta-amyloidsleep disturbanceneurodegeneration
Type
Original Research
Information
CNS Spectrums , Volume 27 , Issue 3 , June 2022 , pp. 339 - 346
Copyright
© The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Clauw, DJ. Fibromyalgia: an overview. Am J Med. 2009;122(12 Suppl):S3–S13. doi:10.1016/j.amjmed.2009.09.006.CrossRefGoogle ScholarPubMed
Petzke, F, Clauw, DJ, Ambrose, K, Khine, A, Gracely, RH. Increased pain sensitivity in fibromyalgia: effects of stimulus type and mode of presentation. Pain. 2003;105(3):403–413. doi:10.1016/s0304-3959(03)00204-5.CrossRefGoogle ScholarPubMed
Shi, H, Yuan, C, Dai, Z, Ma, H, Sheng, L. Gray matter abnormalities associated with fibromyalgia: a meta-analysis of voxel-based morphometric studies. Semin Arthritis Rheum. 2016;46(3):330–337. doi:10.1016/j.semarthrit.2016.06.002.CrossRefGoogle ScholarPubMed
Kuchinad, A, Schweinhardt, P, Seminowicz, DA, Wood, PB, Chizh, BA, Bushnell, MC. Accelerated brain gray matter loss in fibromyalgia patients: premature aging of the brain? J Neurosci. 2007;27(15):4004–4007. doi:10.1523/jneurosci.0098-07.2007.CrossRefGoogle ScholarPubMed
Wu, YL, Huang, CJ, Fang, SC, Ko, LH, Tsai, PS. Cognitive impairment in fibromyalgia: a meta-analysis of case-control studies. Psychosom Med. 2018;80(5):432–438. doi:10.1097/PSY.0000000000000575.CrossRefGoogle ScholarPubMed
Tzeng, NS, Chung, CH, Liu, FC, et al. Fibromyalgia and risk of dementia—a nationwide, population-based, cohort study. Am J Med Sci. 2018;355(2):153–161. doi:10.1016/j.amjms.2017.09.002.CrossRefGoogle ScholarPubMed
Diaz-Piedra, C, Guzman, MA, Buela-Casal, G, Catena, A. The impact of fibromyalgia symptoms on brain morphometry. Brain Imaging Behav. 2016;10(4):1184–1197. doi:10.1007/s11682-015-9485-2.CrossRefGoogle ScholarPubMed
Bigatti, SM, Hernandez, AM, Cronan, TA, Rand, KL. Sleep disturbances in fibromyalgia syndrome: relationship to pain and depression. Arthritis Rheum. 2008;59(7):961–967. doi:10.1002/art.23828.CrossRefGoogle ScholarPubMed
Fang, SC, Wu, YL, Chen, SC, Teng, HW, Tsai, PS. Subjective sleep quality as a mediator in the relationship between pain severity and sustained attention performance in patients with fibromyalgia. J Sleep Res. 2019;28(6):e12843. doi:10.1111/jsr.12843.CrossRefGoogle ScholarPubMed
Altena, E, Vrenken, H, Van Der Werf, YD, van den Heuvel, OA, Van Someren, EJ. Reduced orbitofrontal and parietal gray matter in chronic insomnia: a voxel-based morphometric study. Biol Psychiatry. 2010;67(2):182–185. doi:10.1016/j.biopsych.2009.08.003.CrossRefGoogle ScholarPubMed
Andreasen, N, Hesse, C, Davidsson, P, et al. Cerebrospinal fluid beta-amyloid(1-42) in Alzheimer disease: differences between early- and late-onset Alzheimer disease and stability during the course of disease. Arch Neurol. 1999;56(6):673–680. doi:10.1001/archneur.56.6.673.CrossRefGoogle ScholarPubMed
Shokri-Kojori, E, Wang, GJ, Wiers, CE, et al. Beta-amyloid accumulation in the human brain after one night of sleep deprivation. Proc Natl Acad Sci USA. 2018;115(17):4483–4488. doi:10.1073/pnas.1721694115.CrossRefGoogle ScholarPubMed
Motamedi, V, Kanefsky, R, Matsangas, P, et al. Elevated tau and interleukin-6 concentrations in adults with obstructive sleep apnea. Sleep Med. 2018;43:71–76. doi:10.1016/j.sleep.2017.11.1121.CrossRefGoogle ScholarPubMed
Wolfe, F, Clauw, DJ, Fitzcharles, MA, et al. The American College of Rheumatology preliminary diagnostic criteria for fibromyalgia and measurement of symptom severity. Arthritis Care Res (Hoboken). 2010;62(5):600–610. doi:10.1002/acr.20140.CrossRefGoogle ScholarPubMed
Burckhardt, CS, Clark, SR, Bennett, RM. The Fibromyalgia Impact Questionnaire: development and validation. J Rheumatol. 1991;18(5):728–733.Google ScholarPubMed
Buysse, DJ, Reynolds, CF III, Monk, TH, Berman, SR, Kupfer, DJ. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193–213. doi:10.1016/0165-1781(89)90047-4.CrossRefGoogle ScholarPubMed
Abdel-Rahman, EM, Balogun, SA, Kepple, A, et al. Beck Depression Inventory and survival in elderly hemodialysis patients. Nephrol Dial Transplant. 2011;26(6):2064–2065. doi:10.1093/ndt/gfr086.CrossRefGoogle ScholarPubMed
Osman, A, Barrios, FX, Gutierrez, PM, Williams, JE, Bailey, J. Psychometric properties of the Beck Depression Inventory-II in nonclinical adolescent samples. J Clin Psychol. 2008;64(1):83–102. doi:10.1002/jclp.20433.CrossRefGoogle ScholarPubMed
Beck, AT, Epstein, N, Brown, G, Steer, RA. An inventory for measuring clinical anxiety: psychometric properties. J Consult Clin Psychol. 1988;56(6):893–897. doi:10.1037//0022-006x.56.6.893.CrossRefGoogle ScholarPubMed
Julian, LJ. Measures of anxiety: State-Trait Anxiety Inventory (STAI), Beck Anxiety Inventory (BAI), and Hospital Anxiety and Depression Scale-Anxiety (HADS-A). Arthritis Care Res (Hoboken). 2011;63(Suppl 11):S467–S472. doi:10.1002/acr.20561.CrossRefGoogle Scholar
Chieh, JJ, Yang, SY, Jian, ZF, et al. Hyper-high-sensitivity wash-free magnetoreduction assay on biomolecules using high-T-c superconducting quantum interference devices. J Appl Phys. 2008;103(1):014703. doi:10.1063/1.2827359. Artn 014703.CrossRefGoogle Scholar
Yang, CC, Yang, SY, Chieh, JJ, et al. Biofunctionalized magnetic nanoparticles for specifically detecting biomarkers of Alzheimer’s disease in vitro. Acs Chem Neurosci. 2011;2(9):500–505. doi:10.1021/cn200028j.CrossRefGoogle ScholarPubMed
Chiu, MJ, Yang, SY, Horng, HE, et al. Combined plasma biomarkers for diagnosing mild cognition impairment and Alzheimer’s disease . Acs Chem Neurosci. 2013;4(12):1530–1536. doi:10.1021/cn400129p.CrossRefGoogle ScholarPubMed
Trojanowski, JQ, Schuck, T, Schmidt, ML, Lee, VM. Distribution of tau proteins in the normal human central and peripheral nervous system. J Histochem Cytochem. 1989;37(2):209–215. doi:10.1177/37.2.2492045.CrossRefGoogle ScholarPubMed
Lv, HY, Wang, QL, Chen, HY, You, YJ, Ren, PS, Li, LX. Study on serum tau protein level and neurodevelopmental outcome of placental abruption with neonatal hypoxic-ischemic encephalopathy. J Matern Fetal Neonatal Med. 2019;28:1–7. doi:10.1080/14767058.2019.1588878.Google Scholar
Alonso, A, Zaidi, T, Novak, M, Grundke-Iqbal, I, Iqbal, K. Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc Natl Acad Sci USA. 2001;98(12):6923–6928. doi:10.1073/pnas.121119298.CrossRefGoogle ScholarPubMed
Lue, LF, Sabbagh, MN, Chiu, MJ, et al. Plasma levels of Aβ42 and tau identified probable Alzheimer’s dementia: findings in two cohorts. Front Aging Neurosci. 2017;9:226. doi:10.3389/fnagi.2017.00226.CrossRefGoogle ScholarPubMed
O’Brien, RJ, Wong, PC. Amyloid precursor protein processing and Alzheimer’s disease. Annu Rev Neurosci. 2011;34:185–204. doi:10.1146/annurev-neuro-061010-113613.CrossRefGoogle ScholarPubMed
Turner, PR, O’Connor, K, Tate, WP, Abraham, WC. Roles of amyloid precursor protein and its fragments in regulating neural activity, plasticity and memory. Prog Neurobiol. 2003;70(1):1–32. doi:10.1016/s0301-0082(03)00089-3.CrossRefGoogle ScholarPubMed
Fleming, SM, Espay, AJ. Cinnamon in a mouse model of PD: Khasnavis S, Pahan K. Cinnamon protects dopaminergic neurons in a mouse model of Parkinson’s disease. J Neuroimmune Pharmacol. 2014;9:569–581. Mov Disord. 2014;29(12):1466. doi:10.1002/mds.26034.CrossRefGoogle Scholar
Park, JC, Han, SH, Yi, D, et al. Plasma tau/amyloid-β1-42 ratio predicts brain tau deposition and neurodegeneration in Alzheimer’s disease. Brain. 2019;142(3):771–786. doi:10.1093/brain/awy347.CrossRefGoogle ScholarPubMed
Roberts, KF, Elbert, DL, Kasten, TP, et al. Amyloid-beta efflux from the central nervous system into the plasma. Ann Neurol. 2014;76(6):837–844. doi:10.1002/ana.24270.CrossRefGoogle ScholarPubMed
Steriade, M. Slow-wave sleep: serotonin, neuronal plasticity, and seizures. Arch Ital Biol. 2004;142(4):359–367.Google ScholarPubMed
Perlis, ML, Giles, DE, Bootzin, RR, et al. Alpha sleep and information processing, perception of sleep, pain, and arousability in fibromyalgia. Int J Neurosci. 1997;89(3–4):265–280. doi:10.3109/00207459708988479.CrossRefGoogle ScholarPubMed
Yaffe, K, Falvey, CM, Hoang, T. Connections between sleep and cognition in older adults. Lancet Neurol. 2014;13(10):1017–1028. doi:10.1016/S1474-4422(14)70172-3.CrossRefGoogle ScholarPubMed
Holth, JK, Fritschi, SK, Wang, C, et al. The sleep-wake cycle regulates brain interstitial fluid tau in mice and CSF tau in humans. Science. 2019;363(6429):880–884. doi:10.1126/science.aav2546.CrossRefGoogle ScholarPubMed
Jensen, KB, Srinivasan, P, Spaeth, R, et al. Overlapping structural and functional brain changes in patients with long-term exposure to fibromyalgia pain. Arthritis Rheum. 2013;65(12):3293–3303. doi:10.1002/art.38170.CrossRefGoogle ScholarPubMed
Gelonch, O, Garolera, M, Valls, J, et al. The effect of depressive symptoms on cognition in patients with fibromyalgia. PLoS One. 2018;13(7):e0200057. doi:10.1371/journal.pone.0200057.CrossRefGoogle ScholarPubMed
Gatchel, JR, Donovan, NJ, Locascio, JJ, et al. Depressive symptoms and tau accumulation in the inferior temporal lobe and entorhinal cortex in cognitively normal older adults: a pilot study. J Alzheimers Dis. 2017;59(3):975–985. doi:10.3233/JAD-170001.CrossRefGoogle ScholarPubMed
Wei, M, Zhao, B, Huo, K, et al. Sleep deprivation induced plasma amyloid-beta transport disturbance in healthy young adults. J Alzheimers Dis. 2017;57(3):899–906. doi:10.3233/JAD-161213.CrossRefGoogle ScholarPubMed
Salminen, A, Kauppinen, A, Kaarniranta, K. Hypoxia/ischemia activate processing of amyloid precursor protein: impact of vascular dysfunction in the pathogenesis of Alzheimer’s disease. J Neurochem. 2017;140(4):536–549. doi:10.1111/jnc.13932.CrossRefGoogle ScholarPubMed
Alvarez Lario, B, Alonso Valdivielso, JL, Alegre Lopez, J, Martel Soteres, C, Viejo Banuelos, JL, Maranon Cabello, A. Fibromyalgia syndrome: overnight falls in arterial oxygen saturation. Am J Med. 1996;101(1):54–60. doi:10.1016/s0002-9343(96)00067-8.CrossRefGoogle ScholarPubMed
Albrecht, DS, Forsberg, A, Sandstrom, A, et al. Brain glial activation in fibromyalgia—a multi-site positron emission tomography investigation. Brain Behav Immun. 2019;75:72–83. doi:10.1016/j.bbi.2018.09.018.CrossRefGoogle Scholar
Bellesi, M, de Vivo, L, Chini, M, Gilli, F, Tononi, G, Cirelli, C. Sleep loss promotes astrocytic phagocytosis and microglial activation in mouse cerebral cortex. J Neurosci. 2017;37(21):5263–5273. doi:10.1523/JNEUROSCI.3981-16.2017.CrossRefGoogle ScholarPubMed
McCrae, CS, Mundt, JM, Curtis, AF, et al. Gray matter changes following cognitive behavioral therapy for patients with comorbid fibromyalgia and insomnia: a pilot study. J Clin Sleep Med. 2018;14(9):1595–1603. doi:10.5664/jcsm.7344.CrossRefGoogle ScholarPubMed
Gratuze, M, Julien, J, Morin, F, Marette, A, Planel, E. Differential effects of voluntary treadmill exercise and caloric restriction on tau pathogenesis in a mouse model of Alzheimer’s disease-like tau pathology fed with Western diet. Prog Neuropsychopharmacol Biol Psychiatry. 2017;79(Pt B):452–461. doi:10.1016/j.pnpbp.2017.08.001.CrossRefGoogle Scholar
Viola-Saltzman, M, Watson, NF, Bogart, A, Goldberg, J, Buchwald, D. High prevalence of restless legs syndrome among patients with fibromyalgia: a controlled cross-sectional study. J Clin Sleep Med. 2010;6(5):423–427.CrossRefGoogle ScholarPubMed
Meresh, ES, Artin, H, Joyce, C, et al. Obstructive sleep apnea co-morbidity in patients with fibromyalgia: a single-center retrospective analysis and literature review. Open Access Rheumatol. 2019;11:103–109. doi:10.2147/OARRR.S196576.CrossRefGoogle ScholarPubMed