Diaphragmatic motor cortex hyperexcitability in patients with chronic obstructive pulmonary disease


Autoři: Rehab Elnemr aff001;  Rania Ahmad Sweed aff002;  Hanaa Shafiek aff002
Působiště autorů: Physical Medicine, Rheumatology and Rehabilitation Department, Faculty of Medicine, Alexandria University, Alexandria, Egypt aff001;  Chest Diseases Department, Faculty of Medicine, Alexandria University, Alexandria, Egypt aff002
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0217886

Souhrn

Background and objectives

Respiratory muscles dysfunction has been reported in COPD. Transcranial magnetic stimulation (TMS) has been used for assessing the respiratory corticospinal pathways particularly of diaphragm. We aimed to study the cortico-diaphragmatic motor system changes in COPD using TMS and to correlate the findings with the pulmonary function.

Methods

A case control study recruited 30 stable COPD from the out-patient respiratory clinic of Main Alexandria University hospital- Egypt and 17 healthy control subjects who were subjected to spirometry. Cortical conduction of the diaphragm was performed by TMS to all participants followed by cervical magnetic stimulation of the phrenic nerve roots. Diaphragmatic resting motor threshold (DRMT), cortical motor evoked potential latency (CMEPL), CMEP amplitude (CMEPA), peripheral motor evoked potential latency (PMEPL), PMEP amplitude (PMEPA) and central motor conduction time (CMCT) were measured.

Results

66.7% of COPD patients had severe and very severe COPD with median age of 59 (55–63) years. There was statistically significant bilateral decrease in DRMT, CMEPA and PMEPA in COPD group versus healthy subjects and significant increase in CMEPL and PMEPL (p <0.01). Left CMCT was significantly prolonged in COPD group versus healthy subjects (p <0.0001) but not right CMCT. Further, there was significant increase in CMEPL and CMCT of left versus right diaphragm in COPD group (p = 0.003 and 0.001 respectively) that inversely correlated with FEV1% and FVC% predicted. Right and left DRMT were insignificantly different in COPD group (p >0.05) but positively correlated with FEV1/FVC, FEV1% and FVC% predicted.

Conclusion

Central cortico-diaphragmatic motor system is affected in COPD patients with heterogeneity of both sides that is correlated with pulmonary function.

Significance

Coticospinal pathway affection could be a factor for development of diaphragmatic dysfunction in COPD patients accordingly its evaluation could help in personalization of COPD management especially pulmonary rehabilitation programs.

Klíčová slova:

Functional electrical stimulation – Chronic obstructive pulmonary disease – Motor cortex – Motor neurons – Pulmonary function – Thoracic diaphragm – Transcranial magnetic stimulation – Motor evoked potentials


Zdroje

1. Vogelmeier CF, Criner GJ, Martinez FJ, Anzueto A, Barnes PJ, Bourbeau J, et al. (2017) Global Strategy for the Diagnosis, Management, and Prevention of Chronic Obstructive Lung Disease 2017 Report. GOLD Executive Summary. Am J Respir Crit Care Med 195: 557–582. doi: 10.1164/rccm.201701-0218PP 28128970

2. Dos Santos Yamaguti WP, Paulin E, Shibao S, Chammas MC, Salge JM, Ribeiro M, et al. (2008) Air trapping: The major factor limiting diaphragm mobility in chronic obstructive pulmonary disease patients. Respirology 13: 138–144. doi: 10.1111/j.1440-1843.2007.01194.x 18197925

3. Cassart M, Pettiaux N, Gevenois PA, Paiva M, Estenne M (1997) Effect of chronic hyperinflation on diaphragm length and surface area. Am J Respir Crit Care Med 156: 504–508. doi: 10.1164/ajrccm.156.2.9612089 9279231

4. Smith J, Bellemare F (1987) Effect of lung volume on in vivo contraction characteristics of human diaphragm. J Appl Physiol (1985) 62: 1893–1900.

5. Orozco-Levi M, Lloreta J, Minguella J, Serrano S, Broquetas JM, Gea J (2001) Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164: 1734–1739. doi: 10.1164/ajrccm.164.9.2011150 11719318

6. Reid WD, Huang J, Bryson S, Walker DC, Belcastro AN (1994) Diaphragm injury and myofibrillar structure induced by resistive loading. J Appl Physiol (1985) 76: 176–184.

7. Lissens MA (1994) Motor evoked potentials of the human diaphragm elicited through magnetic transcranial brain stimulation. J Neurol Sci 124: 204–207. doi: 10.1016/0022-510x(94)90327-1 7964872

8. Jalinous R (1991) Technical and practical aspects of magnetic nerve stimulation. J Clin Neurophysiol 8: 10–25. doi: 10.1097/00004691-199101000-00004 2019644

9. Mills KR, Boniface SJ, Schubert M (1992) Magnetic brain stimulation with a double coil: the importance of coil orientation. Electroencephalogr Clin Neurophysiol 85: 17–21. doi: 10.1016/0168-5597(92)90096-t 1371739

10. Groppa S, Oliviero A, Eisen A, Quartarone A, Cohen LG, Mall V, et al. (2012) A practical guide to diagnostic transcranial magnetic stimulation: report of an IFCN committee. Clin Neurophysiol 123: 858–882. doi: 10.1016/j.clinph.2012.01.010 22349304

11. Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1: 1106–1107. doi: 10.1016/s0140-6736(85)92413-4 2860322

12. Maskill D, Murphy K, Mier A, Owen M, Guz A (1991) Motor cortical representation of the diaphragm in man. J Physiol 443: 105–121. doi: 10.1113/jphysiol.1991.sp018825 1822523

13. Khedr EM, Trakhan MN (2001) Localization of diaphragm motor cortical representation and determination of corticodiaphragmatic latencies by using magnetic stimulation in normal adult human subjects. Eur J Appl Physiol 85: 560–566. doi: 10.1007/s004210100504 11718285

14. Hopkinson NS, Sharshar T, Ross ET, Nickol AH, Dayer MJ, Porcher R, et al. (2004) Corticospinal control of respiratory muscles in chronic obstructive pulmonary disease. Respir Physiol Neurobiol 141: 1–12. doi: 10.1016/j.resp.2004.04.003 15234671

15. Wang Y, Liu N, Zhang Z (2019) Respiratory electrophysiologic studies in chronic obstructive pulmonary disease. Medicine (Baltimore) 98: e13993.

16. Mohamed-Hussein AA, Hamed SA, Abdel-Hakim N (2007) Cerebral cortical dysfunction in chronic obstructive pulmonary disease: role of transcranial magnetic stimulation. Int J Tuberc Lung Dis 11: 515–521. 17439674

17. Series F, Wang W, Similowski T (2009) Corticomotor control of the genioglossus in awake OSAS patients: a transcranial magnetic stimulation study. Respir Res 10: 74. doi: 10.1186/1465-9921-10-74 19678922

18. Lanza G, Cantone M, Lanuzza B, Pennisi M, Bella R, Pennisi G, et al. (2015) Distinctive patterns of cortical excitability to transcranial magnetic stimulation in obstructive sleep apnea syndrome, restless legs syndrome, insomnia, and sleep deprivation. Sleep Med Rev 19: 39–50. doi: 10.1016/j.smrv.2014.04.001 24849846

19. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. (2005) Standardisation of spirometry. Eur Respir J 26: 319–338. doi: 10.1183/09031936.05.00034805 16055882

20. Demoule A, Verin E, Locher C, Derenne JP, Similowski T (2003) Validation of surface recordings of the diaphragm response to transcranial magnetic stimulation in humans. J Appl Physiol (1985) 94: 453–461.

21. Zifko U, Remtulla H, Power K, Harker L, Bolton CF (1996) Transcortical and cervical magnetic stimulation with recording of the diaphragm. Muscle Nerve 19: 614–620. doi: 10.1002/(SICI)1097-4598(199605)19:5<614::AID-MUS9>3.0.CO;2-E 8618559

22. Hallett M (2000) Transcranial magnetic stimulation and the human brain. Nature 406: 147–150. doi: 10.1038/35018000 10910346

23. Hamed SA, Youssef AH, Abd-Elaal RF, Hassan MM (2013) Evaluation of central diaphragmatic neural function in early stages of chronic obstructive pulmonary disease. J Neur Aand Neuroscience 4: 4.

24. El-Tantawi GA, Imam MH, Morsi TS (2015) Phrenic Nerve Conduction Abnormalities Correlate with Diaphragmatic Descent in Chronic Obstructive Pulmonary Disease. COPD 12: 516–524. doi: 10.3109/15412555.2014.993465 25774441

25. Hopkinson NS, Sharshar T, Dayer MJ, Lofaso F, Moxham J, Polkey MI (2012) The effect of acute non-invasive ventilation on corticospinal pathways to the respiratory muscles in chronic obstructive pulmonary disease. Respir Physiol Neurobiol 183: 41–47. doi: 10.1016/j.resp.2012.05.018 22652437

26. Wedzicha JA (2000) The heterogeneity of chronic obstructive pulmonary disease. Thorax 55: 631–632. doi: 10.1136/thorax.55.8.631 10899236

27. Isaev G, Murphy K, Guz A, Adams L (2002) Areas of the brain concerned with ventilatory load compensation in awake man. J Physiol 539: 935–945. doi: 10.1113/jphysiol.2001.012957 11897862

28. Dodd JW, Chung AW, van den Broek MD, Barrick TR, Charlton RA, Jones PW (2012) Brain structure and function in chronic obstructive pulmonary disease: a multimodal cranial magnetic resonance imaging study. Am J Respir Crit Care Med 186: 240–245. doi: 10.1164/rccm.201202-0355OC 22652026

29. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19: 126–130. doi: 10.1016/s0166-2236(96)80018-x 8658594

30. Scheibe N, Sosnowski N, Pinkhasik A, Vonderbank S, Bastian A (2015) Sonographic evaluation of diaphragmatic dysfunction in COPD patients. Int J Chron Obstruct Pulmon Dis 10: 1925–1930. doi: 10.2147/COPD.S85659 26392767

31. Rocha FR, Bruggemann AK, Francisco DS, Medeiros CS, Rosal D, Paulin E (2017) Diaphragmatic mobility: relationship with lung function, respiratory muscle strength, dyspnea, and physical activity in daily life in patients with COPD. J Bras Pneumol 43: 32–37. doi: 10.1590/S1806-37562016000000097 28380186

32. Chun EM, Han SJ, Modi HN (2015) Analysis of diaphragmatic movement before and after pulmonary rehabilitation using fluoroscopy imaging in patients with COPD. Int J Chron Obstruct Pulmon Dis 10: 193–199. doi: 10.2147/COPD.S74438 25670895

33. Diaz O, Begin P, Torrealba B, Jover E, Lisboa C (2002) Effects of noninvasive ventilation on lung hyperinflation in stable hypercapnic COPD. Eur Respir J 20: 1490–1498. doi: 10.1183/09031936.02.00034402 12503709

34. Sharshar T, Ross ET, Hopkinson NS, Porcher R, Nickol AH, Jonville S, et al. (2004) Depression of diaphragm motor cortex excitability during mechanical ventilation. J Appl Physiol (1985) 97: 3–10.

35. Sharshar T, Hopkinson NS, Ross ET, Jonville S, Dayer MJ, Nickol AH, et al. (2005) Motor control of the costal and crural diaphragm—insights from transcranial magnetic stimulation in man. Respir Physiol Neurobiol 146: 5–19. doi: 10.1016/j.resp.2004.10.010 15733775

36. Ntritsos G, Franek J, Belbasis L, Christou MA, Markozannes G, Altman P, et al. (2018) Gender-specific estimates of COPD prevalence: a systematic review and meta-analysis. Int J Chron Obstruct Pulmon Dis 13: 1507–1514. doi: 10.2147/COPD.S146390 29785100

37. Adeloye D, Chua S, Lee C, Basquill C, Papana A, Theodoratou E, et al. (2015) Global and regional estimates of COPD prevalence: Systematic review and meta-analysis. J Glob Health 5: 020415. doi: 10.7189/jogh.05-020415 26755942

38. Gea J, Pascual S, Casadevall C, Orozco-Levi M, Barreiro E (2015) Muscle dysfunction in chronic obstructive pulmonary disease: update on causes and biological findings. J Thorac Dis 7: E418–438. doi: 10.3978/j.issn.2072-1439.2015.08.04 26623119


Článek vyšel v časopise

PLOS One


2019 Číslo 12