EDITORIAL

Effects of hyperinflation on the respiratory muscles

M. Decramer

obstructive pulmonary disease (COPD) has a effect on the respiratory muscles, as is evi­

rrom reduced respiratory muscle strength [1-4], fibre [S- 7), and glycolytic enzyme activity [8J. These

are presumably obtained through different mocha­which hyperinflation [9, 10). increased work of (11], hypoxaemia [12], hypercapnia (13], and

[4, 14-17] may all contribute. generally accepted that hyperinflation profoundly respiratory muscle function, but it also has the

beneficial effect of decreasing airways resis-thereby improving ventilation distribution and

an increase in minute ventilation in patients using maximal expiratory flow during resting

[9]. However, it presumably shortens inspira­.IJUUI~u;:.-; and thus displaces them to a less advanla­

of their length-tension curve. Moreover, it to change inspiratory muscle geometry at

residual capacity (FRC) [10] and, fmally, 10 th'e mechanical interaction between respiratory

in a way which is still not fully understood [9,

editorial will focus on some new basic insights hyperinflation affects respiratory muscle length

'U111c ur1n It should be emphasized that hyperinOution e'ltnrl'm Prv severe in COPD. Thus, a plethysmo­ly detem1ined FRC equalling or even exceeding

lft(llctcld total lung capacity (1LC) is a relatively finding in patients with severe ait flow obstruc-1). From the point of view of inspiratory muscle

these patients are, thus, similar to normal .,.,.,.,._,_, at or even above their 1LC and, hence, ~~~X~mnllnr·v muscles are expected to operate at a

vantageous position of their length-tension animal experiments specifically address-

question may contribute 10 a better understand­to how the respiratory muscles are affected by this

increase in FRC. the significance of the distinction between acute le hyperinflation has become evident, since in State adaptive changes 10 chronic shortening

occur in lhe diaphragm. Thus, in emphyse-~msters the diaphragm drops out sarcomeces,

an a shift of the whole length-tension curve 10 length (21-24], such that the muscle adapts to

in situ operating length. Whether this adapts­OCcurs in emphysematous humans remains open

• University 1-lospitals, Kathotieke Universiteit u uven. Delgium.

to question. Indeed, ARoRA and ROCHESTER (17] failed to obtain evidence for chronic diaphragmatic shortening and sarcomere 'ctrop-out in patients with COPD. This appar­ent discrepancy with animal experiments is not readily explained. It may relate to the fact that in the patients studied, hyperinflation was less severe lhan in the em­physematous hamsters.

150

0100 ...J I-

ll a. '#.

0 e: 50

•

• • • • •

{0

• • •

• • -• ••• • • •

• •

40 60 80 FEV1 % pred

Jlig. I. - Functional residual capacity (FRC), exprened as a percent­age of prediaed total lung capacity (l'LC). plotted vs forced Mpirn­tory volume in one second (FBV 1) expressed as a percentage of the prc:dicred value. Data poinrs represent different palienls involved in our rehabilitation programme with chronic obstrocri ve pulmonary disease (COPD) and hyperinflation. As can be SC(:II, in 14 of the 22 patients FRC exceeds predicted TI.C.

In acute hyperinflation, insufficient time is available for this adaptation to develop and, as a consequence, a severe mechanical disadvantage for the inspiratory muscles is expected. We examined the changes in length undergone by the diaphragm and by the parasternal in­tercostals during hyperinflation in supine anaesthetized dogs, using piezoelectric crystals [25, 26] . During infla­tion from FRC to 1LC the parastemals shonened by about 7% [25], and the diaphragm by more than 30% (26]. As a consequence, hyperinflation is expected to induce a mechanical disadvantage, which is much more pronounced in the diaphragm than in the parasternal intercostals. Moreover, although the optimal length in the diaphragm is expected to correspond to a lung

300 M. DECRAMER

volume close to supine FRC [27, 28]. the parasternals were found to be longer than optimal at FRC and to approach their optimal length near TLC [29]. This was recently conflffiled by experiments in which the relation­ship between electrical input and force output, estimated by chunges in parasternal inLramuscular pre..o;..,urc, w~IS shown to improve with hypcrinOation f30].

Although surprising at first sight, the latter findings are in keepi.ng wilh the breathing pattern observed at elevated end-expiratory lung volume in supine anaesthe­tized and vagotomized dogs [30, 31]. Indeed, whereas dogs at FRC breathe with proportional rib cage and abdominal expansion close to the relaxation line, near TLC chest wall motion almost exclusively becomes rib cage motion, frequently even associ:ued with abdominal ind.rawlng and a fall in gastric pressure during inspira­tion. Since these changes were associated with increased diaphragmatic electromyographic (EMG) activity [30, 31J, the latter finding is indicative of ineffective diaphrag­matic contraction near TLC. The fact that in these experiments the pressure-generating capacity of the in­spiratory musculature as a whole was relatively well pre­served near TLC, supported our contention that the optimal length of the parasternal intercostals was proba­bly close to TLC rather than to FRC [311. Indeed, since hyperinflation induces a seve re ineffectiveness of the diaphragm, other muscles have to compensate for it, in order to keep the pressure generating capacity of the global inspiratory musculature relatively constant

Although, undoubtedly, th(}aforementioned experiments have contributed to our conceptual understanding of how hyperinOation affects inspiratory muscle function, it is appropriate to underline the limitations of the reasoning developed above. The analysis should not be limited to the diaphragm and the parasternal intercostals, which are primary muscles of inspiration in humans also (32], but other respiratory muscles need to be considered. These include, the triangularis sterni (33, 34], the transversus abdominis [35], the external and internal intercostals, the levators costae [36], the scalenes [37, 38] and the sterno­cleidomastoids [38]. The scalenes and sternocleidomas­toids are not electrically active during quiet bre111J1ing in supine anaesthetized dogs at FRC or approaching TLC. but they may play a major role during rcspirotion in patients with COPD [39, 40]. The scalenes should be considered as primary muscles of inspiration in mon [371. Their shortening with hyperinOation is also consirlerably less than the diaphragmatic shoncning [411.

HypcrinOation may also modify the function of respi­ratory muscles in a way which is not related to length­tension considerations. The diaphragm Oattens wilh hyperinflation and the zone of apposition diminishes ( 101 and these factors further reduce its mechanical effective­ness in generating pressures and expanding the rib cage. Hyperinflation further changes the mechanical interac­tion among costal and crural parts of the diaphragm, such that they become arranged more in series and less in parallel, which may conLribute to the diaphragm's failure as a pressure generator at high lung volumes [20).

Only scanty data are available on how hyperinflation affects Lhe action of the external and internal intercostals

[42, 43), whereas no data arc presently avai l.tble parasternal intercostal or accessory muscle force ora to rib cage motion and rib cage expanston and how these relationships are altered at elcva:S expiratory lung volume.

These new insights were obtained in animals, and it remains uncertain how far these can be extrapolated to humans and to paticnta hyperinflation. Nevertheless, several studies have v·idcd evidence to support the contention that in similar concepts presumably apply. Firstly maximal inspiratory pressure decreases sh~J~ increasing lung volumes [3, 44, 45], the actunJ generated by the inspiratory musculature (i.e. ence between maximal inspiratory pressure and tic recoil curve or the total respiratory system clearly more independent of lung volume. This that the pressure generating capacity of the muscles is relatively well preserved with in humans also. Secondly, Lhe pallem or and gastric pressure development during i "' I"J1IUOD •

normal subjects breathing at elevated end-expiratory volume is very similar 10 that observed in supine the!lzcd dogs, [46, 47]. Finally, in patients with and severe hyperinflation, diaphragmatic l>h n ..... . , _...,

more pronounced than intercostal and accessory shortening [481, and these patients exhibit signs diaphragmatic ineffectiveness correlating with the of airflow obstruction [48-50).

Our understanding of how respiratory muscle is altered in patients with hyperinflation, hn'""·"'•• mains limited and more data are required on the alterations induced in the extra-diaphragmatic tory muscles in patients. Recent evidence ob~aineel_

animal experiments clearly indicates that hypcrl is deLrimenlal to the mechanical effectiveness diaphragm but may be beneficial to the effectiveness of the parasternal intercoslals. More mation on other respiratory muscles and on the · Lion between them is needed, however, to come 10 intergrated view on how the action of the vital pump altered by increases in end-expiratory lung volume.

1\cknow/edgmentr: These studies WCIC IUwa a 11ran1 of lhe '"NationuJ Ponds voor Wetcn.s'Ch~~ ...... Onderwek", hNational l.ottery·Belgium"J' and "•.~ ale Vcreniglllg tot SteWl aan de Gchon ~~ •

References

1. Byrd RB, Hyatt RE. - Maximal respiratory pr~s~ ill chronic obstructive lung disease. Am Rev Respir D1s, 1968. 9& 848-856. tl 2. Gilbert R. Auchincloss JH Jr, Bleb S. - Measuremc!lt maximum inspiratory pressure during routine spirometJ)'. L~• 1978, 155. 23-32. . Maai-3. Decramer M, Demedts M, Rochette F. BiUiet ~· - J mum transrespiratory pressures in obstructive lung d1sease. 8 Eur Physiopathol Respir, 1980, 16, 479-490. ·rntJ 4. Rochester DF, Braun NMT. - Determinants of m~u inspiratory pressure in chronic obstructive pulmonary dl~ Am Rev Respir Dis, 1985, 132, 42-47. "ddf 5. Campbell JA, Hughes RL, Saghal V, Frederiksen J, Slti

HYPERINFLATION AND THE RESPIRATORY MUSCLES 301

AJteflllions in intercostal muscle morphology and in p.1ticnts with obstructive lung disease. Am Rev 980. 122. 679-686. (lL. Katz H. Saghal V, Campbell JA, HRrtZ R. _ Fiber size and energy metabolites in five sepa­(rum paticnl3 with chronic obstruCtive lung disease. 1983, 44. 321-328. J. Mednmo G, Dcbessc B. Riquet M, Dcn:nnc JP.

types in coslal and cnu:al diaphntgm in normal IS with moderate chronic rcspirBiory disease.

PhvsiotltJIIIOI Re.rpiT, 198,5, 21} 351-356. 1\S tien C. Medrano G, Riquct M, Dere:nne JP.

.,.,,,y"'u"- activities in the diaphragm of normal with moderate chronic obstructive pulmonary

Eur PhysiopOJhcl Respir, 1984, 20, 535- 540. PT. - Hyperinflation (editorial). Am Rev Respir

129. 1-2. C, Macklem PT. -The respiratory muscles. New 1982, 307, 786-797.

B. Murciano D, Talamo C, Aubier M, Pariente R, I. - Work of breathing in patients with chronic

pulmonary disease in acute respiratory failure. Am Dis, 1985, 131, 822-827. ], Farkas G, Prefaut C, Thomas D, Macklem PT, -The failing inspiratory muscles under normoxic

conditions. Am Rev RespiT Dis, 1981, 124,

G, Calverley P, Talamo C, Schnader J, Roussos C.­of carbon dioxide on diaphragmatic function in human N Engl J Med, 1984, 310, 874-879.

NS, Rochester OF. - Effect of body weight and on human diaphragm muscle mass, thickness, and Physiol: Respirat Environ Exercise Physiol, 1982,

NS, Rochester DF. - Respiratory muscle strength voluntary ventilation in undernourished patients. · Dis, 1982, 126, 5-8.

•~::ne.:uer OF. -Malnutrition and the respiratory muscles. Med, 1986, 7, 91-99. NS, Rochestec DF. - COPD and human diaphragm ~~ensi,ons. Chest, 1987, 91, 719-724.

Ml•lkl~m PT, Macklem DM, De Troyer A. - A model of muscle mechanics. J Appl Physiol: Respirat Envi­

Physiol, 1983, 55, 547-557 ue.:rftrn...- M, De Troyer A, Kelly S, Macklem PT. -

of costal and crural diaphragm in dogs. Re.rpirOJ Environ Eurcise Physiol, 1984, 56,

L, Garzaniti N, Newman S, Macklem PT.- Effect and equalization of abdominal pressure on

action. J Appl Physiol, 1987, 62, 1655-1664. i OS, Kelsen SO. - Effect of elastase-induced on the force generating ability of the diaphragm. J 1982, 70, 978-988. GA, Roussos C. - Adaptability of the hamster

to exercise and/or emphysema. J Appl Physiol: E11viron Exercise Physio/, 1982, 53, 1263-1272.

GA, Roussos C. - Diaphragm in emphysematous sarcomere adaptability. J Appl Physiol: Respirat

Exercise Physiol, 1983, 54, 1635-1640, Oll~en A, Supioski GS, Kelsen SO. - Functional adapta­or diophngm to chronic hyperinflation in emphysematous

J tlppl Pllysiol, 1986. 60, 225-2.31. weo~A'""' M, De Troyer A. - Re-spiratory changes in

u11ercostnl length. J Appl Physiol: Re.rpirot Enviro11 Physiol, 1984, 57, 1254-1260.

Decrarner M, Jiang TX, Reid MB, Kelly S, Macklem PT,

Demedts M. - Relationship between diaphragm length and abdominal dimensions. J Appl Physiol, 1986, 61, 1815-1820. 27. Kim MJ, Druz WS, Danon J, Machnach W, Sharp IT.­Mechanics of the canine diaphragm. J Appl Physiol, 1976, 41, 369-382. 28. Road J, Ncwman S, Derenne JP, Grassino A. - In vivo length-force relationship of canine diaphragm. J Appl Physiol, 1986, 60. 63-70. 29. Farkas GA, Decramer M, Rochester OF, De Troyer A. -Contractile properties of intercostal muscles and their func­tional significance. J Appl Physiol, 1985, 59, 528-535. 30. Jiang TX, De Schepper K, Demedts M, Decramer M. -Effects of acute hyperinflation on the mechanical effectiveness of the parasternal intercostals. Am Rev Respir Dis, (in press). 31. Decramer M, Jiang TX, Demedts M. - Effects of acute hyperinflation on inspiratory muscle. J Appl Physiol, 1987,63, 1493-1498. 32. De Troyer A, Sampson M. -Activation of th·e parasternal intercostals during breathing efforts in human subjects. J Appl Physiol: Respiral Environ Exercise Physiol, 1982, 52, 524-529. 33. De Troyer A, Ninane V. -The triangularis sterni: a pri­mary muscle of breathing in the dog. J Appl Physiol, 1986, 60, 14-21. 34. Ninane V, Decramer M, De Troyer A. - Coupling be­tween the parasternal intercostal and triangularis sterni in the dog. J Appl Physiol, 1986, 61, 539-544. 35. Gilmartin J, Ninane V, De Troyer A.- Abdominal muscle use during breathing in the anesthetized dog. Respir Physiol, 1987, 70, 159-171. 36. Goldman MD, Loh L, Sears TA. -The respiratory activity of human levator costae muscles and its modification by posture. J Physiol (Lond), 1985, 362, 189-204. 37. De Troyer A, Estenne M. -Coordination between rib cage muscles and diaphragm during quiet breathing in humans. J Appl Physiol: RespirOJ Environ Exercise Physiol, 1984, 57, 899-906. 38. Parkas GA, Rochester DF. - Contractile characteristics and operating lengths of canine neck inspiratory muscles. J Appl Physiol, 1986, 61, 220-226. 39. Oronbaek P, Skouby AP.- The activity pattern of the dia­phragm and some muscles of the neck and ll11nk in chronic asthmatics and normal controls. Acta Med Scand, 1960, 168, 41~25. 40. Skarvan K, Mikulenka V.- The ventilatory function of sternocleidomastoid and scalene muscles in patients with pul­monary emphysema. Respiration, 1970, 27, 480-492. 41. Sharp IT, Danon I, Druz WS, Ooldberg NB, Fishman H, Machnach W. - Respiratory muscle function in patients with chronic obstructive pulmonary disease: its relationship to dis­ability and to respiratory therapy. Am Rev Re.rpir Dis, 1974, 110, 154-167. 42. De Troyer A, Kelly S, Zin WA. - Mechanical action of the intercostal muscles on the ribs. Science, 1983, 220, 87-88. 43. De Troyer A, Kelly S, Macklem PT. Zin WA. - Mechan­ics of intercostal space and actions of external and internal intercostal muscles. J Clin Invest, 1985, 75, 850-857. 44. Ringqvist T.- The ventilatory capacity in healthy subjects. Scand J Clin Lab Invest, 1966, 18 (Suppl. 88), 1-113. 45. Rahn H, Otis AB, Chadwick LE, Fenn WO. -The pres­sure-volume diagram of the thorax and the lung. Am J Physiol, 1946, 146, 161-178. 46. Wolfson DA, Strohl KP, Dimarco AF, Altose MD. -Effects of an increase in end-expiratory volume on the pattern of thoracoabdominal movement. Respir Physiol, 1983, 53, 273-283.

302 M . DBCRAMBR

47. Camus P, Deameules MJ. - Chest wall movement& and breathing pattern at different lung volumes. Che.st, 1982, 243 (Abstract). 48. Sharp JT, Ooldberg NB, Dnn WS, F"I.Shman HC, Danon J. - Thoracoalxlominnl motion in chrome obstructive pulmo­nary disease. Am Rev Respir Dis, 1977, 115, 47-56.

49. Oilmartin JJ. Oibson OJ. - Abnormalities of motion in patients with chronic airflo w obstmctio~ 1984, 39. 264-27 1. . 50. Oil martin rr. Oibson OJ. - Mechanisms of Pllr1ld cage motion in patients with obstructive pulmonaryo Am Rev Re3pir Dis, 1986. 134, 68~87.