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13.05.2022 | Original Article

Videofluoroscopic Swallowing Study Features and Resting-State Functional MRI Brain Activity for Assessing Swallowing Differences in Patients with Mild Cognitive Impairment and Risk of Dysphagia

verfasst von: Jie Wang, Cheng Yang, Xiaomei Wei, Mengqing Zhang, Meng Dai, Guohang Huang, Wenhao Huang, Hongmei Wen, Zulin Dou

Erschienen in: Dysphagia | Ausgabe 1/2023

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Abstract

To examine the swallowing characteristics in patients with mild cognitive impairment (MCI) and dysphagia risk and explore brain activity changes using regional homogeneity (ReHo) with resting-state functional magnetic resonance imaging (rs-fMRI). We included 28 patients with MCI and dysphagia risk and 17 age-matched older adults. All participants underwent neurological, cognitive examinations, and a videofluoroscopic swallowing study (VFSS). We quantitatively analyzed the VFSS temporal and kinetic parameters of the 5- and 10-mL swallows. The participants underwent rs-fMRI, and the ReHo values were calculated. Differences in the swallowing physiology and rs-fMRI findings between participants with MCI and controls were analyzed. Correlation analyses were also conducted. Compared to the control group, patients with MCI and dysphagia risk had lower global cognition scores, longer 10-mL oral transit times (OTTs), and lower executive function scores. ReHo in the bilateral inferior occipital lobes (IOLs) and left prefrontal lobe decreased in patients with MCI and dysphagia risk compared to participants in the control group. In patients with MCI, the 10-mL OTT was negatively correlated with the Montreal Cognitive Assessment (MoCA) score, and the ReHo values were positive correlated with quantitative temporal swallowing measurements using canonical correlation analysis. Mediation analysis revealed that the ReHo values of the left and right IOL acted as significant mediators between the MoCA score and the 10-mL OTT. We found that individuals with MCI and dysphagia risk, verified by reduced MoCA scores, demonstrated prolonged OTTs when swallowing larger boluses compared with age-matched controls. There was a negative correlation between the MoCA score and 10-mL OTT, which was partially mediated by the left and right IOL ReHo values, suggesting that functional changes in the IOLs and left prefrontal lobe associated with oral swallowing status and cognitive level in individuals with MCI and dysphagia risk.

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Trebbastoni A, Pichiorri F, D’Antonio F, Campanelli A, Onesti E, Ceccanti M, et al. Altered cortical synaptic plasticity in response to 5-Hz repetitive transcranial magnetic stimulation as a new electrophysiological finding in amnestic mild cognitive impairment converting to Alzheimer’s disease: results from a 4-year prospective cohort study. Front Aging Neurosci. 2015;7:253. https://doi.org/10.3389/fnagi.2015.00253.CrossRef

Gauthier S, Reisberg B, Zaudig M, Petersen RC, Ritchie K, Broich K, et al. Mild cognitive impairment. The Lancet. 2006;367(9518):1262–70. https://doi.org/10.1016/s0140-6736(06)68542-5.CrossRef

Rami L, Gómez-Anson B, Sanchez-Valle R, Bosch B, Monte GC, Lladó A, et al. Longitudinal study of amnesic patients at high risk for Alzheimer’s disease: clinical, neuropsychological and magnetic resonance spectroscopy features. Dement Geriatr Cogn Disord. 2007;24(5):402–10. https://doi.org/10.1159/000109750.CrossRef

Yang EJ, Kim KW, Lim JY, Paik NJ. Relationship between dysphagia and mild cognitive impairment in a community-based elderly cohort: the Korean longitudinal study on health and aging. J Am Geriatr Soc. 2014;62(1):40–6. https://doi.org/10.1111/jgs.12606.CrossRef

De Stefano A, Di Giovanni P, Kulamarva G, Gennachi S, Di Fonzo F, Sallustio V, et al. Oropharyngeal dysphagia in elderly population suffering from mild cognitive impairment and mild dementia: understanding the link. Am J Otolaryngol. 2020;41(4):102501. https://doi.org/10.1016/j.amjoto.2020.102501.CrossRef

Layly J, Marmouset F, Chassagnon G, Bertrand P, Sirinelli D, Cottier JP, et al. Can we reduce frame rate to 15 images per second in pediatric videofluoroscopic swallow studies? Dysphagia. 2020;35(2):296–300. https://doi.org/10.1007/s00455-019-10027-8.CrossRef

Malandraki GA, Johnson S, Robbins J. Functional MRI of swallowing: from neurophysiology to neuroplasticity. Head Neck. 2011;33(Suppl 1):S14-20. https://doi.org/10.1002/hed.21903.CrossRef

Malandraki GA, Perlman AL, Karampinos DC, Sutton BP. Reduced somatosensory activations in swallowing with age. Hum Brain Mapp. 2011;32(5):730–43. https://doi.org/10.1002/hbm.21062.CrossRef

Martin R, Barr A, MacIntosh B, Smith R, Stevens T, Taves D, et al. Cerebral cortical processing of swallowing in older adults. Exp Brain Res. 2007;176(1):12–22. https://doi.org/10.1007/s00221-006-0592-6.CrossRef

10.

Mourão AM, Vicente LCC, Abreu MNS, Tatiana Simões C, Romeu Vale SA, De Souza LC, et al. Swallowing progression during the acute phase of cortical and subcortical ischemic stroke and its association with the extension of brain damage and cognitive impairment. Top Stroke Rehabil. 2019;26(7):523–7. https://doi.org/10.1080/10749357.2019.1628464.CrossRef

11.

Humbert IA, McLaren DG, Kosmatka K, Fitzgerald M, Johnson S, Porcaro E, et al. Early deficits in cortical control of swallowing in Alzheimer’s disease. J Alzheimer’s Disease. 2010;19(4):1185–97. https://doi.org/10.3233/JAD-2010-1316.Early.CrossRef

12.

Suh MK, Kim H, Na DL. Dysphagia in patients with dementia: Alzheimer versus vascular. Alzheimer Dis Assoc Disord. 2009;23(2):178–84. https://doi.org/10.1097/WAD.0b013e318192a539.CrossRef

13.

Damoiseaux JS, Rombouts SA, Barkhof F, Scheltens P, Stam CJ, Smith SM, et al. Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci U S A. 2006;103(37):13848–53. https://doi.org/10.1073/pnas.0601417103.CrossRef

14.

Smitha KA, Akhil Raja K, Arun KM, Rajesh PG, Thomas B, Kapilamoorthy TR, et al. Resting state fMRI: a review on methods in resting state connectivity analysis and resting state networks. Neuroradiol J. 2017;30(4):305–17. https://doi.org/10.1177/1971400917697342.CrossRef

15.

Lee MH, Smyser CD, Shimony JS. Resting-state fMRI: a review of methods and clinical applications. AJNR Am J Neuroradiol. 2013;34(10):1866–72. https://doi.org/10.3174/ajnr.A3263.CrossRef

16.

Baumgartner R, Somorjai R, Summers R, Richter W. Assessment of cluster homogeneity in fMRI data using Kendall’s coefficient of concordance. Magn Reson Imaging. 1999;17(10):1525–32. https://doi.org/10.1016/S0730-725x(99)00101-0.CrossRef

17.

Zang Y, Jiang T, Lu Y, He Y, Tian L. Regional homogeneity approach to fMRI data analysis. Neuroimage. 2004;22(1):394–400. https://doi.org/10.1016/j.neuroimage.2003.12.030.CrossRef

18.

Zhang Z, Liu Y, Jiang T, Zhou B, An N, Dai H, et al. Altered spontaneous activity in Alzheimer’s disease and mild cognitive impairment revealed by regional homogeneity. Neuroimage. 2012;59(2):1429–40. https://doi.org/10.1016/j.neuroimage.2011.08.049.CrossRef

19.

Verwoerd JH, Mattace-Raso FUS. Mild cognitive impairment. Huisarts en Wetenschap. 2012;55(10):464–7. https://doi.org/10.1007/s12445-012-0228-y.CrossRef

20.

Gale SA, Acar D, Daffner KR. Dementia. Am J Med. 2018;131(10):1161–9. https://doi.org/10.1016/j.amjmed.2018.01.022.CrossRef

21.

Igarashi K, Kikutani T, Tamura F. Survey of suspected dysphagia prevalence in home-dwelling older people using the 10-Item eating assessment tool (EAT-10). PLoS ONE. 2019;14(1):e0211040. https://doi.org/10.1371/journal.pone.0211040.CrossRef

22.

Marik PE, Kaplan D. Aspiration pneumonia and dysphagia in the elderly. Chest. 2003;124(1):328–36. https://doi.org/10.1378/chest.124.1.328.CrossRef

23.

Stephen JR, Taves DH, Smith RC, Martin RE. Bolus location at the initiation of the pharyngeal stage of swallowing in healthy older adults. Dysphagia. 2005;20(4):266–72. https://doi.org/10.1007/s00455-005-0023-z.CrossRef

24.

Kim Y, McCullough GH, Asp CW. Temporal measurements of pharyngeal swallowing in normal populations. Dysphagia. 2005;20(4):290–6. https://doi.org/10.1007/s00455-005-0029-6.CrossRef

25.

Leonard R. Predicting aspiration risk in patients with dysphagia: evidence from fluoroscopy. Laryngoscope Investig Otolaryngol. 2019;4(1):83–8. https://doi.org/10.1002/lio2.226.CrossRef

26.

Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9(1):97–113. https://doi.org/10.1016/0028-3932(71)90067-4.CrossRef

27.

Maruyama M, Morita K, Kimura H, Nishio F, Yoshida M, Tsuga K. Association between masticatory ability and oral functions. J Clin Exp Dent. 2020;12(11):e1011–4. https://doi.org/10.4317/jced.56747.CrossRef

28.

Kim Y, McCullough GH. Maximum hyoid displacement in normal swallowing. Dysphagia. 2008;23(3):274–9. https://doi.org/10.1007/s00455-007-9135-y.CrossRef

29.

O’Driscoll C, Shaikh M. Cross-cultural applicability of the montreal cognitive assessment (MoCA): a systematic review. J Alzheimers Dis. 2017;58(3):789–801. https://doi.org/10.3233/JAD-161042.CrossRef

30.

Reitan RM, Wolfson D. The trail making test as an initial screening procedure for neuropsychological impairment in older children. Arch Clin Neuropsychol: Off J Natl Acad Neuropsychologists. 2004;19(2):281–8. https://doi.org/10.1016/s0887-6177(03)00042-8.CrossRef

31.

Corrigan JD, Hinkeldey NS. Relationships between parts A and B of the trail making test. J Clin Psychol. 1987;43(4):402–9. https://doi.org/10.1002/1097-4679(198707)43:4%3c402::Aid-jclp2270430411%3e3.0.Co;2-e.CrossRef

32.

Hayes A. Introduction to mediation, moderation, and conditional process analysis: a regression-based approach. 2nd ed. New York, NY: The Guilford Press; 2017.

33.

Enderlein G FJ. The design and analysis of clinical experiments 1986.

34.

Dantas RO, Kern MK, Massey BT, Dodds WJ, Kahrilas PJ, Brasseur JG, et al. Effect of swallowed bolus variables on oral and pharyngeal phases of swallowing. Am J Physiol. 1990;258(5 Pt 1):G675–81. https://doi.org/10.1152/ajpgi.1990.258.5.G675.CrossRef

35.

Dodds WJ, Man KM, Cook IJ, Kahrilas PJ, Stewart ET, Kern MK. Influence of bolus volume on swallow-induced hyoid movement in normal subjects. AJR Am J Roentgenol. 1988;150(6):1307–9. https://doi.org/10.2214/ajr.150.6.1307.CrossRef

36.

Cosentino G, Tassorelli C, Prunetti P, Bertino G, De Icco R, Todisco M, et al. Anodal transcranial direct current stimulation and intermittent theta-burst stimulation improve deglutition and swallowing reproducibility in elderly patients with dysphagia. Neurogastroenterol Motil. 2020;32(5):e13791. https://doi.org/10.1111/nmo.13791.CrossRef

37.

Kalia M. Dysphagia and aspiration pneumonia in patients with Alzheimer’s disease. Metabolism: Clin Exp. 2003;52(10):36–8. https://doi.org/10.1016/s0026-0495(03)00300-7.CrossRef

38.

Ozsurekci C, Arslan SS, Demir N, Caliskan H, Sengul Aycicek G, Kilinc HE, et al. Timing of dysphagia screening in Alzheimer’s dementia. JPEN J Parenter Enteral Nutr. 2020;44(3):516–24. https://doi.org/10.1002/jpen.1664.CrossRef

39.

Hu S, Xu D, Peterson BS, Wang Q, He X, Hu J, et al. Association of cerebral networks in resting state with sexual preference of homosexual men: a study of regional homogeneity and functional connectivity. PLoS ONE. 2013;8(3):e59426. https://doi.org/10.1371/journal.pone.0059426.CrossRef

40.

Wu T, Zang Y, Wang L, Long X, Li K, Chan P. Normal aging decreases regional homogeneity of the motor areas in the resting state. Neurosci Lett. 2007;423(3):189–93. https://doi.org/10.1016/j.neulet.2007.06.057.CrossRef

41.

Zang YF, He Y, Zhu CZ, Cao QJ, Sui MQ, Liang M, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Develop. 2007;29(2):83–91. https://doi.org/10.1016/j.braindev.2006.07.002.CrossRef

42.

Liu H, Liu Z, Liang M, Hao Y, Tan L, Kuang F, et al. Decreased regional homogeneity in schizophrenia: a resting state functional magnetic resonance imaging study. NeuroReport. 2006;17(1):19–22. https://doi.org/10.1097/01.wnr.0000195666.22714.35.CrossRef

43.

Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412(6843):150–7. https://doi.org/10.1038/35084005.CrossRef

44.

Robertson J, Chadwick D, Baines S, Emerson E, Hatton C. People with intellectual disabilities and dysphagia. Disabil Rehabil. 2018;40(11):1345–60. https://doi.org/10.1080/09638288.2017.1297497.CrossRef

45.

Cristofori I, Cohen-Zimerman S, Grafman J. Executive functions. 1st ed. Amsterdam: Elsevier; 2019. p. 197–219.

46.

Suzuki M, Asada Y, Ito J, Hayashi K, Inoue H, Kitano H. Activation of cerebellum and basal ganglia on volitional swallowing detected by functional magnetic resonance imaging. Dysphagia. 2003;18(2):71–7. https://doi.org/10.1007/s00455-002-0088-x.CrossRef

47.

Ruth E, Martin BJM, Smith RC, Barr AM, Stevens TK, Gati JS, Menon RS. cerebral areas processing swallowing and tongue movement are overlapping but distinct a fMRI study. J Neurophysiol. 2004;92:2428–43. https://doi.org/10.1152/jn.01144.2003.CrossRef

48.

Ogura E, Matsuyama M, Goto TK, Nakamura Y, Koyano K. Brain activation during oral exercises used for dysphagia rehabilitation in healthy human subjects: a functional magnetic resonance imaging study. Dysphagia. 2012;27(3):353–60. https://doi.org/10.1007/s00455-011-9374-9.CrossRef

49.

Hamdy S, Rothwell JC, Brooks DJ, Bailey D, Aziz Q, Thompson DG. Identification of the cerebral loci processing human swallowing with H215O PET activation. J Neurophysiol. 1999;81(4):1917–26. https://doi.org/10.1152/jn.1999.81.4.1917.CrossRef

50.

Thiebaut de Schotten M, Urbanski M, Valabregue R, Bayle DJ, Volle E. Subdivision of the occipital lobes: an anatomical and functional MRI connectivity study. Cortex. 2014;56:121–37. https://doi.org/10.1016/j.cortex.2012.12.007.CrossRef

51.

Garcia-Garcia D, Clavero P, Gasca Salas C, Lamet I, Arbizu J, Gonzalez-Redondo R, et al. Posterior parietooccipital hypometabolism may differentiate mild cognitive impairment from dementia in Parkinson’s disease. Eur J Nucl Med Mol Imaging. 2012;39(11):1767–77. https://doi.org/10.1007/s00259-012-2198-5.CrossRef

52.

Kern MK, Jaradeh S, Arndorfer RC, Shaker R. Cerebral cortical representation of reflexive and volitional swallowing in humans. Am J Physiol Gastrointest Liver Physiol. 2001;280(3):G354–60. https://doi.org/10.1152/ajpgi.2001.280.3.G354.CrossRef

53.

Mihai PG, Otto M, Domin M, Platz T, Hamdy S, Lotze M. Brain imaging correlates of recovered swallowing after dysphagic stroke: a fMRI and DWI study. NeuroImage: Clin. 2015;12:1013–21. https://doi.org/10.1016/j.nicl.2016.05.006.CrossRef

54.

Lowell SY, Poletto CJ, Knorr-Chung BR, Reynolds RC, Simonyan K, Ludlow CL. Sensory stimulation activates both motor and sensory components of the swallowing system. Neuroimage. 2008;42(1):285–95. https://doi.org/10.1016/j.neuroimage.2008.04.234.CrossRef

55.

Muhle P, Labeit B, Wollbrink A, Claus I, Warnecke T, Wolters CH, et al. Targeting the sensory feedback within the swallowing network-reversing artificially induced pharyngolaryngeal hypesthesia by central and peripheral stimulation strategies. Hum Brain Mapp. 2021;42(2):427–38. https://doi.org/10.1002/hbm.25233.CrossRef

56.

Michou E, Williams S, Vidyasagar R, Downey D, Mistry S, Edden RAE, et al. FMRI and MRS measures of neuroplasticity in the pharyngeal motor cortex. Neuroimage. 2015;117:1–10. https://doi.org/10.1016/j.neuroimage.2015.05.007.CrossRef

57.

Miller AJ. The neurobiology of swallowing and dysphagia. Dev Disabil Res Rev. 2008;14(2):77–86. https://doi.org/10.1002/ddrr.12.CrossRef

58.

Gardini S, Venneri A, McGeown WJ, Toraci C, Nocetti L, Porro CA, et al. Brain activation patterns characterizing different phases of motor action: execution. Choice Ideation Brain Topography. 2016;29(5):679–92. https://doi.org/10.1007/s10548-016-0491-5.CrossRef

59.

Lowe MJ, Mock BJ, Sorenson JA. Functional connectivity in single and multislice echoplanar imaging using resting-state fluctuations. Neuroimage. 1998;7(2):119–32. https://doi.org/10.1006/nimg.1997.0315.CrossRef

Titel: Videofluoroscopic Swallowing Study Features and Resting-State Functional MRI Brain Activity for Assessing Swallowing Differences in Patients with Mild Cognitive Impairment and Risk of Dysphagia
verfasst von: Jie Wang
Cheng Yang
Xiaomei Wei
Mengqing Zhang
Meng Dai
Guohang Huang
Wenhao Huang
Hongmei Wen
Zulin Dou
Publikationsdatum: 13.05.2022
Verlag: Springer US
Erschienen in: Dysphagia / Ausgabe 1/2023
Print ISSN: 0179-051X
Elektronische ISSN: 1432-0460
DOI: https://doi.org/10.1007/s00455-022-10460-2

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