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Prognostic Prediction of Dysphagia by Analyzing the Corticobulbar Tract in the Early Stage of Intracerebral Hemorrhage

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Abstract

We investigated the predictive value of the corticobulbar tract (CBT) for dysphagia using diffusion tensor tractography in the early stage of intracerebral hemorrhage (ICH) for dysphagia. Forty-two patients with spontaneous ICH ± intraventricular hemorrhage (IVH) and 22 control subjects were recruited. The patients were classified into three groups: group A—could remove nasogastric tube (NGT) in the acute stage of ICH, group B—could remove NGT within 6 months after onset, and group C—could not remove NGT until 6 months after onset. The CBT were reconstructed, and fractional anisotropy (FA) and tract volume (TV) values were determined. The FA of the CBT in the affected hemisphere in group A was lower than in the control group (p < 0.05). The FA and TV of the CBT in the affected hemisphere in group B were lower than those in the control group (p < 0.05). In group C, the FA and TV in the affected hemisphere and unaffected hemispheres were lower than in the control group (p < 0.05). The TV of the CBT in the affected hemisphere in group B showed a moderate negative correlation with the length of time until NGT removal (r = 0.430, p < 0.05). We found that patients with CBT injuries in both hemispheres were not able to remove the NGT until 6 months after onset, whereas patients who were injured only in the affected hemisphere were able to remove NGT within 6 months of onset. The severity of injury to the CBT in the affected hemisphere appeared to be related to the length of time until NGT removal.

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Fig. 1

Abbreviations

CBT:

Corticobulbar tract

DTT:

Diffusion tensor tractography

DTI:

Diffusion tensor imaging

ROI:

Regions of interest

ICH:

Intracerebral hemorrhage

IVH:

Intraventricular hemorrhage

NGT:

Nasogastric tube

FA:

Fractional anisotropy

TV:

Tract volume

References

  1. 1.

    Martino R, Foley N, Bhogal S, Diamant N, Speechley M, Teasell R. Dysphagia after stroke: Incidence, diagnosis, and pulmonary complications. Stroke. 2005;36:2756–63.

  2. 2.

    O’Neill PA, Smithard DG, Morris J. Complications and outcome following acute stroke: revised table. Stroke. 1998;29:1480–1.

  3. 3.

    Mann G, Hankey GJ, Cameron D. Swallowing disorders following acute stroke: prevalence and diagnostic accuracy. Cerebrovasc Dis. 2000;10:380–6.

  4. 4.

    Guyomard V, Fulcher RA, Redmayne O, Metcalf AK, Potter JF, Myint PK. Effect of dysphasia and dysphagia on inpatient mortality and hospital length of stay: a database study. J Am Geriatr Soc. 2009;57:2101–6.

  5. 5.

    Wilson RD. Mortality and cost of pneumonia after stroke for different risk groups. J Stroke Cerebrovasc Dis. 2012;10:61–7.

  6. 6.

    Lin WC, Huang CY, Lee LF, Chen YW, Ho CH, Sun YT. Initial National Institute of Health Stroke Scale to early predict the improvement of swallowing in patients with acute ischemic stroke. J Stroke Cerebrovasc Dis. 2019;28:104297.

  7. 7.

    Schmidt J, Holas M, Halvorson K, Reding M. Videofluoroscopic evidence of aspiration predicts pneumonia and death but not dehydration following stroke. Dysphagia. 1994;9:7–11.

  8. 8.

    Kalra L, Smith DH, Crome P. Stroke in patients aged over 75 years: outcome and predictors. Postgrad Med J. 1993;69:33–6.

  9. 9.

    Eslick GD, Talley NJ. Dysphagia: epidemiology, risk factors and impact on quality of life—a population-based study. Aliment Pharmacol Ther. 2008;27:971–9.

  10. 10.

    Ickenstein GW, Stein J, Ambrosi D, Goldstein R, Horn M, Bogdahn U. Predictors of survival after severe dysphagic stroke. J Neurol. 2005;252:1510–6.

  11. 11.

    Ickenstein GW, Kelly PJ, Furie KL, Ambrosi D, Rallis N, Goldstein R, et al. Predictors of feeding gastrostomy tube removal in stroke patients with dysphagia. J Stroke Cerebrovasc Dis. 2003;12:169–74.

  12. 12.

    Broadley S, Croser D, Cottrell J, Creevy M, Teo E, Yiu D, et al. Predictors of prolonged dysphagia following acute stroke. J Clin Neurosci. 2003;10:300–5.

  13. 13.

    Kumar S, Doughty C, Doros G, Selim M, Lahoti S, Gokhale S, Schlaug G. Recovery of swallowing after dysphagic stroke: an analysis of prognostic factors. J Stroke Cerebrovasc Dis. 2014;23:56–62.

  14. 14.

    Maeshima S, Okazaki H, Okamoto S, Mizuno S, Asano N, Tsunoda T, et al. Dysphagia following putaminal hemorrhage at a rehabilitation hospital. J Stroke Cerebrovasc Dis. 2016;25:389–96.

  15. 15.

    Maeshima S, Osawa A, Yamane F, Ishihara S, Tanahashi N. Dysphagia following acute thalamic haemorrhage: clinical correlates and outcomes. Eur Neurol. 2014;71:165–72.

  16. 16.

    Flowers HL, AlHarbi MA, Mikulis D, Silver FL, Rochon E, Streiner D, Martino R. MRI-based neuroanatomical predictors of dysphagia, dysarthria, and aphasia in patients with first acute ischemic stroke. Cerebrovasc Dis Extra. 2017;7:21–34.

  17. 17.

    Mann G, Hankey GJ, Cameron D. Swallowing function after stroke: prognosis and prognostic factors at 6 months. Stroke. 1999;30:744–8.

  18. 18.

    Ween JE, Alexander MP, D’Esposito M, Roberts M. Incontinence after stroke in a rehabilitation setting: outcome associations and predictive factors. Neurology. 1996;47:659–63.

  19. 19.

    Daniels SK, McAdam CP, Brailey K, Foundas AL. Clinical assessment of swallowing and prediction of dysphagia severity. Am J Speech Lang Pathol. 1997;6:17–24.

  20. 20.

    Horner J, Massey EW, Riski JE, Lathrop DL, Chase KN. Aspiration following stroke: clinical correlates and outcome. Neurology. 1988;38:1359–62.

  21. 21.

    Broadley S, Croser D, Cottrell J, Creevy M, Teo E, Yiu D, Pathi R, Taylor J, Thompson PD. Predictors of prolonged dysphagia following acute stroke. J Clin Neurosci. 2003;10:300–5.

  22. 22.

    Okubo PC, Fabio SR, Domenis DR, Takayanagui OM. Using the national institute of health stroke scale to predict dysphagia in acute ischemic stroke. Cerebrovasc Dis. 2012;33:501–7.

  23. 23.

    Joundi RA, Martino R, Saposnik G, Giannakeas V, Fang J, Kapral MK. Predictors and outcomes of dysphagia screening after acute ischemic stroke. Stroke. 2017;48:900–6.

  24. 24.

    Kwon HG, Lee J, Jang SH. Injury of the corticobulbar tract in patients with dysarthria following cerebral infarct: diffusion tensor tractography study. Int J Neurosci. 2016;126:361–5.

  25. 25.

    Jenabi M, Peck KK, Young RJ, Brennan N, Holodny AI. Identification of the corticobulbar tracts of the tongue and face using deterministic and probabilistic DTI fiber tracking in patients with brain tumor. Am J Neuroradiol. 2015;36:2036–41.

  26. 26.

    Jang SH, Seo JP. The anatomical location of the corticobulbar tract at the corona radiata in the human brain: diffusion tensor tractography study. Neurosci Lett. 2015;590:80–3.

  27. 27.

    Jang SH, Kim SH, Kwon YH. Extensive traumatic axonal injury of brain due to violence: a case report. Medicine (Baltim). 2018;97:e13315.

  28. 28.

    Jang SH, Lee HD. Weak phonation due to unknown injury of the corticobulbar tract in a patient with mild traumatic brain injury: a diffusion tensor tractography study. Neural Regen Res. 2018;13:936.

  29. 29.

    Jang SH, Seo YS. Dysarthria due to injury of the corticobulbar tract in a patient with mild traumatic brain injury. Am J Phys Med Rehabil. 2016;95:e187–8.

  30. 30.

    Pan C, Peck KK, Young RJ, Holodny AI. Somatotopic organization of motor pathways in the internal capsule: a probabilistic diffusion tractography study. Am J Neuroradiol. 2012;33:1274–80.

  31. 31.

    Yim SH, Kim JH, Han ZA, Jeon S, Cho JH, Kim GS, Choi SA, Lee JH. Distribution of the corticobulbar tract in the internal capsule. J Neurol Sci. 2013;334:63–8.

  32. 32.

    Jang SH, Lee J, Kwon HG. Reorganization of the corticobulbar tract in a patient with bilateral middle cerebral artery territory infarct. Am J Phys Med Rehabil. 2016;95:e58–9.

  33. 33.

    Kim HK, Han M, Lee HJ. Corticobulbar tract involvement in neuropsychiatric systemic lupus erythematosus: a case report. Iran J Radiol. 2016;13:e32927.

  34. 34.

    Liégeois F, Tournier J-D, Pigdon L, Connelly A, Morgan AT. Corticobulbar tract changes as predictors of dysarthria in childhood brain injury. Neurology. 2013. https://doi.org/10.1212/WNL.1210b1013e3182840c3182846d.

  35. 35.

    Jang SH, Kim SH, Seo JP. Image of the month: dysphasia due to injury of the corticobulbar tract following traumatic brain injury. Clin Med (Lond). 2017;17:584–5.

  36. 36.

    Moon HI, Kim GS, Lee E. Is the location of white matter lesions important in the swallowing function of older patients with mild stroke? Dysphagia. 2018;34(3):407–14.

  37. 37.

    Trapl M, Enderle P, Nowotny M, Teuschl Y, Matz K, Dachenhausen A, Brainin M. Dysphagia bedside screening for acute-stroke patients: the Gugging Swallowing Screen. Stroke. 2007;38:2948–52.

  38. 38.

    Rosenbek JC, Robbins JA, Roecker EB, Coyle JL, Wood JL. A penetration-aspiration scale. Dysphagia. 1996;11:93–8.

  39. 39.

    Han TR, Paik NJ, Park JW. Quantifying swallowing function after stroke: a functional dysphagia scale based on videofluoroscopic studies. Arch Phys Med Rehabil. 2001;82:677–82.

  40. 40.

    Kothari RU, Brott T, Broderick JP, Barsan WG, Sauerbeck LR, Zuccarello M, Khoury J. The ABCs of measuring intracerebral hemorrhage volumes. Stroke. 1996;27:1304–5.

  41. 41.

    Staykov D, Wagner I, Volbers B, Hauer EM, Doerfler A, Schwab S, Bardutzky J. Natural course of perihemorrhagic edema after intracerebral hemorrhage. Stroke. 2011;42:2625–9.

  42. 42.

    Lee SH, Park HK, Ryu WS, Lee JS, Bae HJ, Han MK, Lee YS, Kwon HM, Kim CK, Park ES, Chung JW, Jung KH, Roh JK. Effects of celecoxib on hematoma and edema volumes in primary intracerebral hemorrhage: a multicenter randomized controlled trial. Eur J Neurol. 2013;20:1161–9.

  43. 43.

    Morgan TC, Dawson J, Spengler D, Lees KR, Aldrich C, Mishra NK, et al. The Modified Graeb Score: an enhanced tool for intraventricular hemorrhage measurement and prediction of functional outcome. Stroke. 2013;44:635–41.

  44. 44.

    Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23(Suppl 1):S208–19.

  45. 45.

    Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW. Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage. 2007;34:144–55.

  46. 46.

    Behrens TE, Johansen-Berg H, Woolrich M, Smith S, Wheeler-Kingshott C, Boulby P, Barker G, Sillery E, Sheehan K, Ciccarelli O. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 2003;6:750.

  47. 47.

    Wuensch KL. Straightforward statistic for the behavioral sciences. J Am Stat Assoc. 1996;91:1750.

  48. 48.

    Lim KO, Hedehus M, Moseley M, de Crespigny A, Sullivan EV, Pfefferbaum A. Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging. Arch Gen Psychiatry. 1999;56:367–74.

  49. 49.

    Filippi M, Cercignani M, Inglese M, Horsfield M, Comi G. Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology. 2001;56:304–11.

  50. 50.

    Mori S, Frederiksen K, Van Zijl PC, Stieltjes B, Kraut MA, Solaiyappan M, Pomper MG. Brain white matter anatomy of tumor patients evaluated with diffusion tensor imaging. Ann Neurol. 2002;51:377–80.

  51. 51.

    Jang SH, Park JS, Shin DG, Kim SH, Kim MS. Relationship between consciousness and injury of ascending reticular activating system in patients with hypoxic ischaemic brain injury. J Neurol Neurosurg Psychiatry. 2018. https://doi.org/10.1136/jnnp-2018-318366.

  52. 52.

    Mori S, van Zijl PC. Fiber tracking: principles and strategies—a technical review. NMR Biomed. 2002;15:468–80.

  53. 53.

    Seo JP, Jang SH. Different characteristics of the corticospinal tract according to the cerebral origin: DTI study. Am J Neuroradiol. 2013;34:1359–63.

  54. 54.

    Kwon HG, Choi BY, Kim SH, Chang CH, Jung YJ, Lee HD, Jang SH. Injury of the cingulum in patients with putaminal hemorrhage: a diffusion tensor tractography study. Front Hum Neurosci. 2014;8:366.

  55. 55.

    Yeo SS, Choi BY, Chang CH, Jung YJ, Ahn SH, Son SM, Byun WM, Jang SH. Periventricular white matter injury by primary intraventricular hemorrhage: a diffusion tensor imaging study. Eur Neurol. 2011;66:235–41.

  56. 56.

    Barritt AW, Smithard DG. Role of cerebral cortex plasticity in the recovery of swallowing function following dysphagic stroke. Dysphagia. 2009;24:83.

  57. 57.

    Jang SH, Shin SM. The usefulness of diffusion tensor tractography for estimating the state of corticobulbar tract in stroke patients. Clin Neurophysiol. 2016;127:2708–9.

  58. 58.

    Yamada K, Sakai K, Akazawa K, Yuen S, Nishimura T. MR tractography: a review of its clinical applications. Magn Reson Med Sci. 2009;8:165–74.

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Acknowledgements

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean Government (MSIP) (No. 2018R1A2B6000996).

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Correspondence to Jun Young Kim.

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Jang, S.H., Kwak, S.Y., Chang, C.H. et al. Prognostic Prediction of Dysphagia by Analyzing the Corticobulbar Tract in the Early Stage of Intracerebral Hemorrhage. Dysphagia (2020). https://doi.org/10.1007/s00455-020-10093-3

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Keywords

  • Dysphagia
  • Intracerebral hemorrhage
  • Diffusion tensor tractography
  • Corticobulbar tract
  • Deglutition
  • Deglutition disorders