Diaphragmatic neuromechanical coupling and mechanisms of hypercapnia during inspiratory loading

Respiratory Physiology and Neurobiology

Volumn 198, Issue 1, 2014, Pages 32-41

  Laghi, Franco ^a,b   Shaikh, Hameeda S ^a,b   Morales, Daniel ^a   Sinderby, Christer ^c,d   Jubran, Amal ^a,b   Tobin, Martin J ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c ST MICHAEL'S HOSPITAL   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Breathing pattern; Dyspnea; Hypercapnia; Muscle fatigue; Phrenic nerve; Respiratory muscles

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; DIAPHRAGM MUSCLE; DIAPHRAGMATIC ELECTRICAL ACTIVITY; DIAPHRAGMATIC NEUROMECHANICAL COUPLING; ELECTRIC ACTIVITY; END EXPIRATORY LUNG VOLUME; FATIGUE; FEMALE; HUMAN; HYPERCAPNIA; INSPIRATORY LOADING; LUNG ALVEOLUS HYPOVENTILATION; LUNG VOLUME; MALE; NEUROPHYSIOLOGICAL RECRUITMENT; PERSONAL EXPERIENCE; PRESSURE; PRIORITY JOURNAL; RESPIRATORY TRACT PARAMETERS; TIDAL TRANSDIAPHRAGMATIC PRESSURE; ABDOMINAL WALL; AIR; BIOLOGICAL MODEL; BRAIN; BREATHING MUSCLE; DIAPHRAGM; DYSPNEA; ELECTROMYOGRAPHY; EXHALATION; INHALATION; METABOLISM; MUSCLE FATIGUE; PATHOPHYSIOLOGY; PHYSIOLOGY; STIMULATION;

CARBON DIOXIDE;

ABDOMINAL WALL; ADULT; AIR; BRAIN; CARBON DIOXIDE; DIAPHRAGM; DYSPNEA; ELECTROMYOGRAPHY; EXHALATION; FEMALE; HUMANS; HYPERCAPNIA; INHALATION; LUNG VOLUME MEASUREMENTS; MALE; MODELS, NEUROLOGICAL; MUSCLE FATIGUE; PHYSICAL STIMULATION; PRESSURE; RESPIRATORY MUSCLES;

EID: 84899829769     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2014.03.004     Document Type: Article

References (56)

1. Abe T., Yamada T., Tomita T., Easton P.A. Posture effects on timing of abdominal muscle activity during stimulated ventilation. J. Appl. Physiol. 1999, 86:1994-2000.
2. Axen K., Haas F., Gaudino D., Haas S.S. Effect of mechanical loading on breathing patterns in women. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 1984, 56:175-181.
3. Axen K., Haas S.S., Haas F., Gaudino D., Haas A. Ventilatory adjustments during sustained mechanical loading in conscious humans. J. Appl. Physiol. Respir. Environ. Exerc. Physiol. 1983, 55:1211-1218.
4. 2-induced air hunger in normal subjects. Respir. Physiol. 1996, 103:19-31.
5. Beck J., Reilly M., Grasselli G., Mirabella L., Slutsky A.S., Dunn M.S., Sinderby C. Patient-ventilator interaction during neurally adjusted ventilatory assist in low birth weight infants. Pediatr. Res. 2009, 65:663-668.
6. Beck J., Sinderby C., Lindstrom L., Grassino A. Effects of lung volume on diaphragm EMG signal strength during voluntary contractions. J. Appl. Physiol. 1998, 85:1123-1134.
7. Bellemare F., Bigland-Ritchie B. Central components of diaphragmatic fatigue assessed by phrenic nerve stimulation. J. Appl. Physiol. 1987, 62:1307-1316.
8. Brannan S., Liotti M., Egan G., Shade R., Madden L., Robillard R., Abplanalp B., Stofer K., Denton D., Fox P.T. Neuroimaging of cerebral activations and deactivations associated with hypercapnia and hunger for air. Proc. Natl. Acad. Sci. 2001, 98:2029-2034.
9. Chiti L., Biondi G., Morelot-Panzini C., Raux M., Similowski T., Hug F. Scalene muscle activity during progressive inspiratory loading under pressure support ventilation in normal humans. Respir. Physiol. Neurobiol. 2008, 164:441-448.
10. De Troyer A. Interaction between the canine diaphragm and intercostal muscles in lung expansion. J. Appl. Physiol. 2005, 98:795-803.
11. De Troyer A., Wilson T.A. Effect of acute inflation on the mechanics of the inspiratory muscles. J. Appl. Physiol. 2009, 107:315-323.
12. Druz W.S., Sharp J.T. Activity of respiratory muscles in upright and recumbent humans. J. Appl. Physiol. 1981, 51:1552-1561.
13. Eastwood P.R., Hillman D.R., Finucane K.E. Ventilatory responses to inspiratory threshold loading and role of muscle fatigue in task failure. J. Appl. Physiol. 1994, 76:185-195.
14. Flume P.A., Eldridge F.L., Edwards L.J., Houser L.M. The Fowler breathholding study revisited: continuous rating of respiratory sensation. Respir. Physiol. 1994, 95:53-66.
15. Gandevia S.C. Spinal and supraspinal factors in human muscle fatigue. Physiol. Rev. 2001, 81:1725-1789.
16. Gandevia S., McKenzie D.K., Plassman B.L. Activation of human respiratory muscles during different voluntary manoeuvres. J. Physiol. 1990, 428:387-403.
17. 2 accumulation without fatigue during inspiratory resistive loading in humans. Respir. Physiol. 1999, 115:273-286.
18. Grassino A., Goldman M.D., Mead J., Sears T.A. Mechanics of the human diaphragm during voluntary contraction: statics. J. Appl. Physiol. 1978, 44:829-839.
19. Gravier G., Delliaux S., Delpierre S., Guieu R., Jammes Y. Inter-individual differences in breathing pattern at high levels of incremental cycling exercise in healthy subjects. Respir. Physiol. Neurobiol. 2013, 189:59-66.
20. Hill J.M. Discharge of group IV phrenic afferent fibers increases during diaphragmatic fatigue. Brain Res. 2000, 856:240-244.
21. Hussain O., Collins E.G., Adiguzel N., Langbein W.E., Tobin M.J., Laghi F. Contrasting pressure-support ventilation and helium-oxygen during exercise in severe COPD. Respir. Med. 2011, 105:494-505.
22. Juan G., Calverley P., Talamo C., Schnader J., Roussos C. Effect of carbon dioxide on diaphragmatic function in human beings. N. Engl. J. Med. 1984, 310:874-879.
23. Kanter R.K., Fordyce W.E. Central contribution to hypoventilation during severe inspiratory resistive loads. Crit. Care Med. 1993, 21:1915-1922.
24. Kellog R.H. Central chemical regulation of respiration. Handbook of Physiology 1964, 507-534. American Physiological Society, Washington, DC. W.O. Fenn, H. Rahn (Eds.).
25. Killian K. Dyspnea. J. Appl. Physiol. 2006, 101:1013-1014.
26. Kufel T.J., Pineda L.A., Junega R.G., Hathwar R., Mador M.J. Diaphragmatic function after intense exercise in congestive heart failure patients. Eur. Respir. J. 2002, 20:1399-1405.
27. Laghi F., Cattapan S.E., Jubran A., Parthasarathy S., Warshawsky P., Choi Y.S., Tobin M.J. Is weaning failure caused by low-frequency fatigue of the diaphragm?. Am. J. Respir. Crit Care Med. 2003, 167:120-127.
28. Laghi F., Harrison M.J., Tobin M.J. Comparison of magnetic and electrical phrenic nerve stimulation in assessment of diaphragmatic contractility. J. Appl. Physiol. 1996, 80:1731-1742.
29. Laghi F., Langbein W.E., Antonescu-Turcu A., Jubran A., Bammert C., Tobin M.J. Respiratory and skeletal muscles in hypogonadal men with chronic obstructive pulmonary disease. Am. J. Respir. Crit Care Med. 2005, 171:598-605.
30. Laghi F., Tobin M.J. Disorders of the respiratory muscles. Am. J. Respir. Crit Care Med. 2003, 168:10-48.
31. Laghi F., Topeli A., Tobin M.J. Does resistive loading decrease diaphragmatic contractility before task failure?. J. Appl. Physiol. 1998, 85:1103-1112.
32. Libet B., Feinstein B.L., Wright E.W. Tendon afferents in autogenetic inhibition in man. Electroencephalogr. Clin. Neurophysiol. 1959, 11:129-140.
33. Loring S.H., Mead J. Abdominal muscle use during quiet breathing and hyperpnea in uninformed subjects. J. Appl. Physiol. 1982, 52:700-704.
34. Macklem P.T., Gross D., Grassino G.A., Roussos C. Partitioning of inspiratory pressure swings between diaphragm and intercostal/accessory muscles. J. Appl. Physiol. 1978, 44:200-208.
35. Mador M.J., Rodis A., Magalang U.J., Ameen K. Comparison of cervical magnetic and transcutaneous phrenic nerve stimulation before and after threshold loading. Am. J. Respir. Crit Care Med. 1996, 154:448-453.
36. Mantilla C.B., Seven Y.B., Hurtado-Palomino J.N., Zhan W.Z., Sieck G.C. Chronic assessment of diaphragm muscle EMG activity across motor behaviors. Respir. Physiol. Neurobiol. 2011, 177:176-182.
37. Mantilla C.B., Seven Y.B., Zhan W.Z., Sieck G.C. Diaphragm motor unit recruitment in rats. Respir. Physiol. Neurobiol. 2010, 173:101-106.
38. McKenzie D.K., Allen G.M., Butler J.E., Gandevia S.C. Task failure with lack of diaphragm fatigue during inspiratory resistive loading in human subjects. J. Appl. Physiol. 1997, 82:2011-2019.
39. McKenzie D.K., Bigland-Ritchie B., Gorman R.B., Gandevia S.C. Central and peripheral fatigue of human diaphragm and limb muscles assessed by twitch interpolation. J. Physiol. 1992, 454:643-656.
40. McKenzie D.K., Gandevia S., Gorman R.B., Southon F.C. Dynamic changes in the zone of apposition and diaphragm length during maximal respiratory efforts. Thorax 1994, 49:634-638.
41. Morelot-Panzini C., Demoule A., Straus C., Zelter M., Derenne J.P., Willer J.C., Similowski T. Dyspnea as a noxious sensation: inspiratory threshold loading may trigger diffuse noxious inhibitory controls in humans. J. Neurophysiol. 2007, 97:1396-1404.
42. Parthasarathy S., Jubran A., Laghi F., Tobin M.J. Sternomastoid, rib cage, and expiratory muscle activity during weaning failure. J. Appl. Physiol. 2007, 103:140-147.
43. Raux M., Straus C., Redolfi S., Morelot-Panzini C., Couturier A., Hug F., Similowski T. Electroencephalographic evidence for pre-motor cortex activation during inspiratory loading in humans. J. Physiol. 2007, 578:569-578.
44. Sassoon C.S., Gruer S.E., Sieck G.C. Temporal relationships of ventilatory failure, pump failure, and diaphragm fatigue. J. Appl. Physiol. 1996, 81:238-245.
45. Sieck G.C., Fournier M. Diaphragm motor unit recruitment during ventilatory and nonventilatory behaviors. J. Appl. Physiol. 1989, 66:2539-2545.
46. Similowski T., Attali V., Bensimon G., Salachas F., Mehiri S., Arnuf I., Lacomblez L., Zelter M., Meininger V., Derenne J.P. Diaphragmatic dysfunction and dyspnoea in amyotrophic lateral sclerosis. Eur. Respir. J. 2000, 15:332-337.
47. Similowski T., Straus C., Attali V., Duguet A., Derenne J.P. Cervical magnetic stimulation as a method to discriminate between diaphragm and rib cage muscle fatigue. J. Appl. Physiol. 1998, 84:1692-1700.
48. Sinderby C., Beck J., Spahija J., Weinberg J., Grassino A. Voluntary activation of the human diaphragm in health and disease. J. Appl. Physiol. 1998, 85:2146-2158.
49. Strohl K.P., Mead J., Banzett R.B., Loring S.H., Kosch P.C. Regional differences in abdominal muscle activity during various maneuvers in humans. J. Appl. Physiol. 1981, 51:1471-1476.
50. Tobin M.J., Laghi F., Jubran A. Ventilatory failure, ventilator support and ventilator weaning. Compr. Physiol. 2012, 2:2871-2921.
51. Tobin M.J., Perez W., Guenther S.M., Lodato R.F., Dantzker D.R. Does rib cage-abdominal paradox signify respiratory muscle fatigue?. J. Appl. Physiol. 1987, 63:851-860.
52. Tobin M.J., Perez W., Guenther S.M., Semmes B.J., Mador M.J., Allen S.J., Lodato R.F., Dantzker D.R. The pattern of breathing during successful and unsuccessful trials of weaning from mechanical ventilation. Am. Rev. Respir. Dis. 1986, 134:1111-1118.
53. Tremoureux L., Raux M., Jutand L., Similowski T. Sustained preinspiratory cortical potentials during prolonged inspiratory threshold loading in humans. J. Appl. Physiol. 2010, 108:1127-1133.
54. Ward M.E., Eidelman D., Stubbing D.G., Bellemare F., Macklem P.T. Respiratory sensation and pattern of respiratory muscle activation during diaphragm fatigue. J. Appl. Physiol. 1988, 65:2181-2199.
55. Watchko J.F., Standaert T.A., Mayock D.E., Twiggs G., Woodrum D.E. Ventilatory failure during loaded breathing: the role of central neural drive. J. Appl. Physiol. 1988, 65:249-255.
56. Woodbury D.M., Karler R. The role of carbon dioxide in the nervous system. Anesthesiology 1960, 21:686-703.