nach oben

Erschienen in:

27.10.2023 | Sleep Breathing Physiology and Disorders • Original Article

Difference in functional connectivity between end-stage renal disease patients with and without restless legs syndrome: A prospective study

verfasst von: Bong Soo Park, Chang Min Heo, Yoo Jin Lee, Sihyung Park, Yang Wook Kim, SungHyun Son, Hyukyong Kwon, Youngchan Park, Yunmi Kim, Dong Ah Lee, Kang Min Park

Erschienen in: Sleep and Breathing | Ausgabe 2/2024

Einloggen, um Zugang zu erhalten

Abstract

Purpose

The purpose of this study was to examine differences in functional connectivity between patients with end-stage renal disease (ESRD) with and without restless legs syndrome (RLS). In addition, the study aimed to identify any potential associations between RLS severity and functional connectivity.

Methods

We enrolled patients with ESRD who had been undergoing hemodialysis. Patients with and without RLS were separated into two groups. Using functional near-infrared spectroscopy (fNIRS) and a graph theory approach, we determined the functional connectivity of patients with ESRD. The data were collected during a 300-s resting state evaluation performed in the dialysis room prior to dialysis.

Results

Eighteen of 48 patients with ESRD were diagnosed with RLS, whereas 30 patients did not exhibit RLS symptoms. Notably, functional connectivity metrics differed significantly between patients with and without RLS. Specifically, patients with ESRD and RLS displayed higher values for mean clustering coefficient (0.474 vs. 0.352, p = 0.001), global efficiency (0.520 vs. 0.414, p = 0.001), strength (6.538 vs. 4.783, p = 0.001), and transitivity (0.714 vs. 0.521, p = 0.001), while values for diameter (5.451 vs. 7.338, p = 0.002), eccentricity (4.598 vs. 5.985, p = 0.004), and characteristic path length (2.520 vs. 3.271, p = 0.002) were lower in patients with ESRD and RLS compared to those without RLS. In addition, there were correlations between the RLS severity score and the assortative coefficient (r = 0.479, p = 0.044), the small-worldness index (r = -0.475, p = 0.046), and transitivity (r = 0.500, p = 0.034).

Conclusions

We demonstrated differences in functional connectivity between patients with ESRD with and without RLS, which may shed light on the pathophysiology of RLS. Notably, a number of functional connectivity metrics demonstrated strong associations with RLS severity. Our study also confirmed the applicability of fNIRS as a tool for investigating functional connectivity in patients with RLS.

Krishnan AV, Kiernan MC (2009) Neurological complications of chronic kidney disease. Nat Rev Neurol 5(10):542–551. https://doi.org/10.1038/nrneurol.2009.138CrossRefPubMed

Lin Z, Zhao C, Luo Q, Xia X, Yu X, Huang F (2016) Prevalence of restless legs syndrome in chronic kidney disease: a systematic review and meta-analysis of observational studies. Ren Fail 38(9):1335–1346. https://doi.org/10.1080/0886022X.2016.1227564CrossRefPubMed

Murtagh FE, Addington-Hall J, Higginson IJ (2007) The prevalence of symptoms in end-stage renal disease: a systematic review. Adv Chronic Kidney Dis 14(1):82–99. https://doi.org/10.1053/j.ackd.2006.10.001CrossRefPubMed

Allen RP, Picchietti D, Hening WA, Trenkwalder C, Walters AS, Montplaisi J, Restless Legs Syndrome D, Epidemiology workshop at the National Institutes of H, International Restless Legs Syndrome Study G (2003) Restless legs syndrome: diagnostic criteria, special considerations, and epidemiology. A report from the restless legs syndrome diagnosis and epidemiology workshop at the National Institutes of Health. Sleep Med 4(2):101–119. https://doi.org/10.1016/s1389-9457(03)00010-8CrossRefPubMed

Allen RP, Picchietti DL, Garcia-Borreguero D, Ondo WG, Walters AS, Winkelman JW, Zucconi M, Ferri R, Trenkwalder C, Lee HB, International Restless Legs Syndrome Study G (2014) Restless legs syndrome/Willis-Ekbom disease diagnostic criteria: updated International Restless Legs Syndrome Study Group (IRLSSG) consensus criteria–history, rationale, description, and significance. Sleep Med 15(8):860–873. https://doi.org/10.1016/j.sleep.2014.03.025CrossRefPubMed

Park BS, Kim SE, Lee HJ, Kim YW, Kim IH, Park JH, Park SH, Lee YJ, Seo SA, Park KM (2020) Alterations in Structural and Functional Connectivities in Patients with End-Stage Renal Disease. J Clin Neurol 16(3):390–400. https://doi.org/10.3988/jcn.2020.16.3.390CrossRefPubMedPubMedCentral

Park BS, Seong M, Ko J, Park SH, Kim YW, Hwan Kim I, Park JH, Lee YJ, Park S, Park KM (2020) Differences of connectivity between ESRD patients with PD and HD. Brain Behav 10(8):e01708. https://doi.org/10.1002/brb3.1708CrossRefPubMedPubMedCentral

Zhou H, Si Y, Sun J, Deng J, Yang L, Tang Y, Qin W (2023) Effectiveness of functional magnetic resonance imaging for early identification of chronic kidney disease: A systematic review and network meta-analysis. Eur J Radiol 160:110694. https://doi.org/10.1016/j.ejrad.2023.110694CrossRefPubMed

Chen HJ, Wang YF, Wen J, Xu Q, Lu GM, Zhang LJ (2020) Functional-structural relationship in large-scale brain networks of patients with end stage renal disease after kidney transplantation: A longitudinal study. Hum Brain Mapp 41(2):328–341. https://doi.org/10.1002/hbm.24804CrossRefPubMed

10.

Park KM, Kim KT, Kang KW, Park JA, Seo JG, Kim J, Chang H, Kim EY, Cho YW, Society RLSSotKSR (2022) Alterations of Functional Connectivity in Patients With Restless Legs Syndrome. J Clin Neurol 18(3):290–297. https://doi.org/10.3988/jcn.2022.18.3.290CrossRefPubMedPubMedCentral

11.

Park KM, Kim KT, Lee DA, Cho YW (2022) Structural brain connectivity in patients with restless legs syndrome: a diffusion tensor imaging study. Sleep 45(7):zsac099. https://doi.org/10.1093/sleep/zsac099CrossRefPubMed

12.

Abdalmalak A, Milej D, Norton L, Debicki DB, Owen AM, Lawrence KS (2021) The Potential Role of fNIRS in Evaluating Levels of Consciousness. Front Hum Neurosci 15:703405. https://doi.org/10.3389/fnhum.2021.703405CrossRefPubMedPubMedCentral

13.

Baik JS, Ko MH, Ko SH, Min JH, Choi JK, Baek JY, Kim TH, Jung NY, Jo Y, Lee TY, Shin YI (2022) Assessment of Functional Near-infrared Spectroscopy by Comparing Prefrontal Cortex Activity: A Cognitive Impairment Screening Tool. Alzheimer Dis Assoc Disord 36(3):266–268. https://doi.org/10.1097/WAD.0000000000000475CrossRefPubMed

14.

Levey AS, Eckardt KU, Dorman NM, Christiansen SL, Hoorn EJ, Ingelfinger JR, Inker LA, Levin A, Mehrotra R, Palevsky PM, Perazella MA, Tong A, Allison SJ, Bockenhauer D, Briggs JP, Bromberg JS, Davenport A, Feldman HI, Fouque D, Gansevoort RT, Gill JS, Greene EL, Hemmelgarn BR, Kretzler M, Lambie M, Lane PH, Laycock J, Leventhal SE, Mittelman M, Morrissey P, Ostermann M, Rees L, Ronco P, Schaefer F, St Clair Russell J, Vinck C, Walsh SB, Weiner DE, Cheung M, Jadoul M, Winkelmayer WC (2020) Nomenclature for kidney function and disease: report of a Kidney Disease: Improving Global Outcomes (KDIGO) Consensus Conference. Kidney Int 97(6):1117–1129. https://doi.org/10.1016/j.kint.2020.02.010CrossRefPubMed

15.

Chapter 1: Definition and classification of CKD (2013) Kidney Int Suppl 3(1):19–62. https://doi.org/10.1038/kisup.2012.64

16.

Walters AS, LeBrocq C, Dhar A, Hening W, Rosen R, Allen RP, Trenkwalder C, International Restless Legs Syndrome Study G (2003) Validation of the International Restless Legs Syndrome Study Group rating scale for restless legs syndrome. Sleep Med 4(2):121–132. https://doi.org/10.1016/s1389-9457(02)00258-7CrossRefPubMed

17.

Choi JK, Choi MG, Kim JM, Bae HM (2013) Efficient data extraction method for near-infrared spectroscopy (NIRS) systems with high spatial and temporal resolution. IEEE Trans Biomed Circuits Syst 7(2):169–177. https://doi.org/10.1109/TBCAS.2013.2255052CrossRefPubMed

18.

Kim TJ, Kim JM, Lee JS, Park SH, Jeong HB, Choi JK, Kim K, Bae HM, Ko SB (2020) Prognostication of neurological outcome after cardiac arrest using wavelet phase coherence analysis of cerebral oxygen. Resuscitation 150:41–49. https://doi.org/10.1016/j.resuscitation.2020.02.031CrossRefPubMed

19.

Mijalkov M, Kakaei E, Pereira JB, Westman E, Volpe G, Alzheimer’s Disease Neuroimaging I (2017) BRAPH: A graph theory software for the analysis of brain connectivity. PLoS ONE 12(8):e0178798. https://doi.org/10.1371/journal.pone.0178798CrossRefPubMedPubMedCentral

20.

Falsaperla R, Vitaliti G, Marino SD, Pratico AD, Mailo J, Spatuzza M, Cilio MR, Foti R, Ruggieri M (2021) Graph theory in paediatric epilepsy: A systematic review. Dialogues Clin Neurosci 23(1):3–13. https://doi.org/10.1080/19585969.2022.2043128CrossRefPubMed

21.

Farahani FV, Karwowski W, Lighthall NR (2019) Application of Graph Theory for Identifying Connectivity Patterns in Human Brain Networks: A Systematic Review. Front Neurosci 13:585. https://doi.org/10.3389/fnins.2019.00585CrossRefPubMedPubMedCentral

22.

Lenoir D, Cagnie B, Verhelst H, De Pauw R (2021) Graph Measure Based Connectivity in Chronic Pain Patients: A Systematic Review. Pain Physician 24(7):E1037–E1058PubMed

23.

Bahrami M, Laurienti PJ, Shappell HM, Simpson SL (2022) Brain Network Analysis: A Review on Multivariate Analytical Methods. Brain Connect. https://doi.org/10.1089/brain.2022.0007CrossRefPubMed

24.

Park KM, Kim KT, Lee DA, Cho YW (2023) Alterations of the thalamic nuclei volumes and intrinsic thalamic network in patients with restless legs syndrome. Sci Rep 13(1):4415. https://doi.org/10.1038/s41598-023-31606-8CrossRefPubMedPubMedCentral

25.

Lin XW, Zhang JF, Qiu MY, Ni LY, Yu HL, Kuo SH, Ondo WG, Yu Q, Wu YC (2019) Restless legs syndrome in end stage renal disease patients undergoing hemodialysis. BMC Neurol 19(1):47. https://doi.org/10.1186/s12883-019-1265-yCrossRefPubMedPubMedCentral

26.

Pearson VE, Allen RP, Dean T, Gamaldo CE, Lesage SR, Earley CJ (2006) Cognitive deficits associated with restless legs syndrome (RLS). Sleep Med 7(1):25–30. https://doi.org/10.1016/j.sleep.2005.05.006CrossRefPubMed

27.

Cha KS, Choi JW, Jung KY, Kim KH (2017) Frontal dysfunction in patients with restless legs syndrome performing a visual oddball task: an event-related potential source imaging study. Sleep Med 36:48–54. https://doi.org/10.1016/j.sleep.2017.04.017CrossRefPubMed

28.

Fulda S, Beitinger ME, Reppermund S, Winkelmann J, Wetter TC (2010) Short-term attention and verbal fluency is decreased in restless legs syndrome patients. Mov Disord 25(15):2641–2648. https://doi.org/10.1002/mds.23353CrossRefPubMed

29.

Magalhaes SC, Kaelin-Lang A, Sterr A, do Prado GF, Eckeli AL, Conforto AB (2015) Transcranial magnetic stimulation for evaluation of motor cortical excitability in restless legs syndrome/Willis-Ekbom disease. Sleep Med 16(10):1265–1273. https://doi.org/10.1016/j.sleep.2015.03.018CrossRefPubMed

30.

Newman ME (2002) Assortative mixing in networks. Phys Rev Lett 89(20):208701. https://doi.org/10.1103/PhysRevLett.89.208701CrossRefPubMed

31.

Babaeeghazvini P, Rueda-Delgado LM, Gooijers J, Swinnen SP, Daffertshofer A (2021) Brain Structural and Functional Connectivity: A Review of Combined Works of Diffusion Magnetic Resonance Imaging and Electro-Encephalography. Front Hum Neurosci 15:721206. https://doi.org/10.3389/fnhum.2021.721206CrossRefPubMedPubMedCentral

32.

Shim HK, Lee HJ, Kim SE, Lee BI, Park S, Park KM (2020) Alterations in the metabolic networks of temporal lobe epilepsy patients: A graph theoretical analysis using FDG-PET. Neuroimage Clin 27:102349. https://doi.org/10.1016/j.nicl.2020.102349CrossRefPubMedPubMedCentral

33.

Novi SL, Rodrigues RB, Mesquita RC (2016) Resting state connectivity patterns with near-infrared spectroscopy data of the whole head. Biomed Opt Express 7(7):2524–2537. https://doi.org/10.1364/BOE.7.002524CrossRefPubMedPubMedCentral

34.

Dravida S, Noah JA, Zhang X, Hirsch J (2018) Comparison of oxyhemoglobin and deoxyhemoglobin signal reliability with and without global mean removal for digit manipulation motor tasks. Neurophotonics 5(1):011006. https://doi.org/10.1117/1.NPh.5.1.011006CrossRefPubMed

Titel: Difference in functional connectivity between end-stage renal disease patients with and without restless legs syndrome: A prospective study
verfasst von: Bong Soo Park
Chang Min Heo
Yoo Jin Lee
Sihyung Park
Yang Wook Kim
SungHyun Son
Hyukyong Kwon
Youngchan Park
Yunmi Kim
Dong Ah Lee
Kang Min Park
Publikationsdatum: 27.10.2023
Verlag: Springer International Publishing
Erschienen in: Sleep and Breathing / Ausgabe 2/2024
Print ISSN: 1520-9512
Elektronische ISSN: 1522-1709
DOI: https://doi.org/10.1007/s11325-023-02943-9

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Difference in functional connectivity between end-stage renal disease patients with and without restless legs syndrome: A prospective study