rro m Effects of hyperinflation on the ...

EDITORIAL
Effects of hyperinflation on the respiratory muscles
M. Decramer
obstructive pulmonary disease (COPD) has a
effect on the respiratory muscles, as is evireduced 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 resisthereby 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 advanlaof 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,
rrom
editorial will focus on some new basic insights
hyperinflation affects respiratory muscle length
'U111c ur1n It should be emphasized that hyperi nOution
e'ltnrl'm Prv severe in COPD. Thus, a pleth ysmoly detem1ined FRC equalling or even exceeding
lft(llctcld total lung capacity (1LC) is a relatively
finding in patients with severe ait flow obstruc1). 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 addressquestion 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~ms ters 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-
lla.
•
•
'#.
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 M pirntory volume in one second (FBV1 ) 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 ins piration. 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 shon cning [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 avail.tble
parasternal intercostal or accessory muscle forceora
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 ins piratory musculature (i.e.
ence between maximal inspiratory pressure and
tic recoil curve
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
vol ume 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.
or
WCIC IU
wa
1\cknow/edgmentr: These studies
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
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\Stien 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 EnviPhysiol, 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 adaptadiophngm to chronic hyperinflation in emphysematous
J tlppl Pllysiol, 1986. 60, 225-2.3 1.
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,
or
301
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. Oil martin JJ. Oibson OJ. - Abnormalities of
motion in patients with chronic airflo w obstmctio~
1984, 39. 264-27 1.
.
50. Oil martin
Oibso n OJ. - Mechanisms of Pllr1ld
cage motion in patients with obstructive pulmonaryo
Am Rev Re3pir Dis, 1986. 134, 68~87 .
rr.