Abstracts
Impairment of (inspiratory and expiratory) respiratory muscles is a common clinical finding, not only in patients with neuromuscular disease but also in patients with primary disease of the lung parenchyma or airways. Although such impairment is common, its recognition is usually delayed because its signs and symptoms are nonspecific and late. This delayed recognition, or even the lack thereof, occurs because the diagnostic tests used in the assessment of respiratory muscle strength are not widely known and available. There are various methods of assessing respiratory muscle strength during the inspiratory and expiratory phases. These methods are divided into two categories: volitional tests (which require patient understanding and cooperation); and non-volitional tests. Volitional tests, such as those that measure maximal inspiratory and expiratory pressures, are the most commonly used because they are readily available. Non-volitional tests depend on magnetic stimulation of the phrenic nerve accompanied by the measurement of inspiratory mouth pressure, inspiratory esophageal pressure, or inspiratory transdiaphragmatic pressure. Another method that has come to be widely used is ultrasound imaging of the diaphragm. We believe that pulmonologists involved in the care of patients with respiratory diseases should be familiar with the tests used in order to assess respiratory muscle function.Therefore, the aim of the present article is to describe the advantages, disadvantages, procedures, and clinical applicability of the main tests used in the assessment of respiratory muscle strength.
Respiratory muscles; Muscle weakness; Diaphragm; Respiratory function tests; Diagnostic tests, routine
O acometimento da musculatura ventilatória (inspiratória e expiratória) é um achado clínico frequente, não somente nos pacientes com doenças neuromusculares, mas também nos pacientes com doenças primárias do parênquima pulmonar ou das vias aéreas. Embora esse acometimento seja frequente, seu reconhecimento costuma ser demorado porque seus sinais e sintomas são inespecíficos e tardios. Esse reconhecimento tardio, ou mesmo a falta de reconhecimento, é acentuado porque os exames diagnósticos usados para a avaliação da musculatura respiratória não são plenamente conhecidos e disponíveis. Usando diferentes métodos, a avaliação da força muscular ventilatória é feita para a fase inspiratória e expiratória. Os métodos usados dividem-se em volitivos (que exigem compreensão e colaboração do paciente) e não volitivos. Os volitivos, como a medida da pressão inspiratória e expiratória máximas, são os mais empregados por serem facilmente disponíveis. Os não volitivos dependem da estimulação magnética do nervo frênico associada a medida da pressão inspiratória na boca, no esôfago ou transdiafragmática. Finalmente, outro método que vem se tornando frequente é a ultrassonografia diafragmática. Acreditamos que o pneumologista envolvido nos cuidados a pacientes com doenças respiratórias deve conhecer os exames usados na avaliação da musculatura ventilatória. Por isso, o objetivo do presente artigo é descrever as vantagens, desvantagens, procedimentos de mensuração e aplicabilidade clínica dos principais exames utilizados para avaliação da força muscular ventilatória.
Músculos respiratórios; Força muscular; Diafragma; Testes de função respiratória; Testes diagnósticos de rotina
Introduction
Impairment of (inspiratory and expiratory) respiratory muscles is a common clinical
finding, not only in patients with neuromuscular disease but also in those with
respiratory diseases affecting the lung parenchyma or airways.(
11 Laghi F, Tobin MJ. Disorders of the respiratory muscles. Am J Respir
Crit Care Med. 2003 1;168(1):10-48.
,
22 Dyspnea. Mechanisms, assessment, and management: a consensus statement.
American Thoracic Society. Am J Respir Crit Care Med.
1999;159(1):321-40.
http://dx.doi.org/10.1164/ajrccm.159.1.a...
)
Inspiratory muscle weakness can cause dyspnea(
22 Dyspnea. Mechanisms, assessment, and management: a consensus statement.
American Thoracic Society. Am J Respir Crit Care Med.
1999;159(1):321-40.
http://dx.doi.org/10.1164/ajrccm.159.1.a...
) and exertion intolerance. However, diagnosis is usually delayed, because
most screening protocols for dyspnea do not include assessment of respiratory muscle
strength. In addition, when assessment of respiratory muscle strength is performed, it
includes tests that yield a high percentage of false negatives, because they depend on
patient cooperation (volitional tests). Therefore, for the appropriate investigation and
possible confirmation of respiratory muscle weakness as a cause of respiratory failure,
it is of paramount importance to be familiar with non-volitional measures and even with
techniques that are more invasive, such as the measurement of transdiaphragmatic
pressure.
The aim of the present article is to describe the advantages, disadvantages, procedures, and clinical applicability of the main diagnostic methods to assess respiratory muscle strength. Although we discuss the main measures of respiratory muscle strength, we do not specifically address the diagnosis of muscle fatigue. We also do not describe other related tests that are not specific or sensitive for confirming the diagnosis of respiratory muscle weakness, such as spirometry and arterial blood gas analysis.
Volitional tests for measuring inspiratory muscle strength
Maximal inspiratory pressure
Maximal inspiratory pressure (MIP) is the most widely used measure of respiratory
muscle strength in patients with suspected respiratory muscle weakness.(
33 American Thoracic Society/European Respiratory Society. ATS/ERS
Statement on respiratory muscle testing. Am J Respir Crit Care Med.
2002;166(4):518-624.
http://dx.doi.org/10.1164/rccm.166.4.518...
) It is determined by measuring upper airway pressure (mouth for
outpatients and trachea for intubated or tracheostomized patients) during a maximal
voluntary inspiratory effort. The measured pressure is a composite of the pressure
generated by the inspiratory muscles and the elastic recoil pressure of the lungs and
chest wall.
Advantages
It uses low-cost, portable equipment; it is easy and rapid to perform; it is
noninvasive; and it has well-established reference values, in different populations
(lower limit of normal of 60 cmH2O for females and 80 cmH2O for
males).(
44 Neder JA, Andreoni S, Lerario MC, Nery LE. Reference values for lung
function tests. II. Maximal respiratory pressures and voluntary ventilation. Braz J
Med Biol Res. 1999;32(6):719-27.
http://dx.doi.org/10.1590/S0100-879X1999...
5 Black LF, Hyatt RE. Maximal respiratory pressures: normal values and
relationship to age and sex. Am Rev Respir Dis. 1969;99(5):696-702.
-
66 Black LF, Hyatt RE. Maximal static respiratory pressures in generalized
neuromuscular disease. Am Rev Respir Dis. 1971;103(5):641-50.
) In addition, since the relationship between lung volumes and inspiratory
muscle strength is not linear,(
77 De Troyer A, Borenstein S, Cordier R. Analysis of lung volume
restriction in patients with respiratory muscle weakness. Thorax.
1980;35(8):603-10.
http://dx.doi.org/10.1136/thx.35.8.603...
) the measurement of MIP can diagnose inspiratory muscle weakness earlier
than would be possible based on changes in lung volumes.
Disadvantages
The maneuver is not intuitive and depends on patient cooperation. Therefore, a low
value might not mean weakness, but rather a lack of cooperation. MIP has high
coefficients of intraindividual and interindividual variation (10 to 13%)(
88 Caruso P, Friedrich C, Denari SD, Ruiz SA, Deheinzelin D. The
unidirectional valve is the best method to determine maximal inspiratory pressure
during weaning. Chest. 1999;115(4):1096-101.
http://dx.doi.org/10.1378/chest.115.4.10...
) and low accuracy for predicting successful extubation in mechanically
ventilated patients.(
99 Yang KL, Tobin MJ. A prospective study of indexes predicting the outcome
of trials of weaning from mechanical ventilation. N Engl J Med.
1991;324(21):1445-50.
http://dx.doi.org/10.1056/NEJM1991052332...
)
How to measure
MIP is measured from RV or from functional residual capacity (FRC). Since there is an inverse relationship between lung volume and inspiratory muscle strength,( 66 Black LF, Hyatt RE. Maximal static respiratory pressures in generalized neuromuscular disease. Am Rev Respir Dis. 1971;103(5):641-50. ) measurements from RV yield module values that are 30% higher than those obtained from measurements from FRC. Although measurements from RV yield higher values, some physicians and researchers use measurements from FRC because they more reproducible and more easily performed by patients. However, when measurements from FRC are made, it is necessary that FRC volume be known, because this volume will affect the pressure generated.
The measurement of MIP can be made with an analog or digital pressure manometer.( 1010 Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes de Função Pulmonar. J Pneumol. 2002;28(Suppl 3):S155-S165. ) Digital devices are preferred over analog devices, given that the highest MIP value occurs briefly and may go unnoticed on an analog display (Figure 1). Measurements are usually made with patients in a sitting position, with or without nose clips. Patients are asked to exhale to RV and then perform a maximal inspiratory effort, sustaining it for 1 to 2 seconds. To prevent overestimation of values because of glottal closure and pressure by the mouth muscles, there should be a 2-mm-wide opening in the mouthpiece, which can be a rigid tubular mouthpiece or a rubber mouthpiece. The latter gives slightly higher values.( 1111 Koulouris N, Mulvey DA, Laroche CM, Green M, Moxham J. Comparison of two different mouthpieces for the measurement of Pimax and Pemax in normal and weak subjects. Eur Respir J. 1988;1(9):863-7. )
Measurement of MEP and MIP with a digital pressure manometer (model MVD 300; Globalmed, Porto Alegre, Brazil). In A, positive MEP values. In B, negative MIP values.
In critically ill intubated patients who are uncooperative, the optimal measurement
of MIP is made with a one-way valve (it permits exhalation, but occludes during
inspiration) attached to the tube and takes 25 seconds (Figure 2).(
1212 Truwit JD, Marini JJ. Validation of a technique to assess maximal
inspiratory pressure in poorly cooperative patients. Chest.
1992;102(4):1216-9.
http://dx.doi.org/10.1378/chest.102.4.12...
)
Variation in inspiratory pressure during measurement of MIP with a one-way valve. The highest value usually occurs within 15 to 20 seconds.
In any method, the maneuver should be repeated 3 to 8 times, and the highest value recorded will be used for analysis. The reproducibility of the MIP measurement, with or without a one-way valve, is 10%.
Clinical applicability
Determining MIP is important in the diagnosis of inspiratory muscle weakness, which
can occur in pulmonary, cardiac, and neuromuscular diseases. In addition, the
measurement of MIP can aid in the differential diagnosis of dyspnea(
22 Dyspnea. Mechanisms, assessment, and management: a consensus statement.
American Thoracic Society. Am J Respir Crit Care Med.
1999;159(1):321-40.
http://dx.doi.org/10.1164/ajrccm.159.1.a...
); in the differential diagnosis of obstructive lung disease of unknown
origin; in assessing response to cardiopulmonary physiotherapy and rehabilitation; in
prescribing and monitoring respiratory muscle training(
1313 Caruso P, Denari SD, Ruiz SA, Bernal KG, Manfrin GM, Friedrich C, et al.
Inspiratory muscle training is ineffective in mechanically ventilated critically ill
patients. Clinics (Sao Paulo). 2005;60(6):479-84.
http://dx.doi.org/10.1590/S1807-59322005...
,
1414 Martin AD, Smith BK, Davenport PD, Harman E, Gonzalez-Rothi RJ, Baz M,
et al. Inspiratory muscle strength training improves weaning outcome in failure to
wean patients: a randomized trial. Crit Care. 2011;15(2):R84.
http://dx.doi.org/10.1186/cc10081...
); and, in critically ill patients, in assessing the possibility and
success of weaning from mechanical ventilation.(
1010 Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes
de Função Pulmonar. J Pneumol. 2002;28(Suppl 3):S155-S165.
)
Sniff nasal inspiratory pressure
The search for a method for the measurement of inspiratory muscle strength that would
overcome the limitations of MIP, as well as being noninvasive (avoiding the need for
an esophageal balloon), resulted in the proposal of measuring nasal inspiratory
pressure during a sniff.(
1515 Koulouris N, Vianna LG, Mulvey DA, Green M, Moxham J. Maximal relaxation
rates of esophageal, nose, and mouth pressures during a sniff reflect inspiratory
muscle fatigue. Am Rev Respir Dis. 1989;139(5):1213-7.
http://dx.doi.org/10.1164/ajrccm/139.5.1...
) SNIP is an acronym for sniff nasal inspiratory pressure. SNIP measures
the joint activity of the diaphragm and other inspiratory muscles and accurately
reflects esophageal pressure (Pes), having the advantage of being
noninvasive.(
1515 Koulouris N, Vianna LG, Mulvey DA, Green M, Moxham J. Maximal relaxation
rates of esophageal, nose, and mouth pressures during a sniff reflect inspiratory
muscle fatigue. Am Rev Respir Dis. 1989;139(5):1213-7.
http://dx.doi.org/10.1164/ajrccm/139.5.1...
,
1616 Héritier F, Rahm F, Pasche P, Fitting JW. Sniff nasal inspiratory
pressure. A noninvasive assessment of inspiratory muscle strength. Am J Respir Crit
Care Med. 1994;150(6 Pt 1):1678-83.
http://dx.doi.org/10.1164/ajrccm.150.6.7...
) However, the correlation between Pes and SNIP is reduced when there is
significant airway obstruction, which occurs in asthma and COPD. Electromyographic
studies have shown that, during SNIP, there is selective contraction of the muscles
involved in breathing, especially the inspiratory accessory muscles, which
demonstrates the specificity of the test.(
1717 Katagiri M, Abe T, Yokoba M, Dobashi Y, Tomita T, Easton PA. Neck and
abdominal muscle activity during a sniff. Respir Med.
2003;97(9):1027-35.
http://dx.doi.org/10.1016/S0954-6111(03)...
)
Although SNIP has a reasonable correlation with MIP,(
1818 Steier J, Kaul S, Seymour J, Jolley C, Rafferty G, Man W, et al. The
value of multiple tests of respiratory muscle strength. Thorax.
2007;62(11):975-80.
http://dx.doi.org/10.1136/thx.2006.07288...
) the former does not replace the latter and should be used as an
additional measure in the assessment of inspiratory muscle strength, because the use
of only one test can overestimate muscle weakness, whereas the use of both tests
reduces the rate of false-positive results for respiratory muscle weakness by nearly
20%.(
1818 Steier J, Kaul S, Seymour J, Jolley C, Rafferty G, Man W, et al. The
value of multiple tests of respiratory muscle strength. Thorax.
2007;62(11):975-80.
http://dx.doi.org/10.1136/thx.2006.07288...
,
1919 Laroche CM, Mier AK, Moxham J, Green M. The value of sniff esophageal
pressures in the assessment of global inspiratory muscle strength. Am Rev Respir Dis.
1988;138(3):598-603.
http://dx.doi.org/10.1164/ajrccm/138.3.5...
)
Advantages
It uses pressure manometers, which are simple and inexpensive equipment that also
measures MIP; it is easy to perform, because it is based on an intuitive maneuver,
which makes the measurement more reproducible; and it has well-established normal
values, in different populations (lower limit of normal of 60 cmH2O for
females and 70 cmH2O for males; Table
1).(
2020 Uldry C, Fitting JW. Maximal values of sniff nasal inspiratory pressure
in healthy subjects. Thorax. 1995;50(4):371-5.
http://dx.doi.org/10.1136/thx.50.4.371...
21 Polkey MI, Moxham J. Clinical aspects of respiratory muscle dysfunction
in the critically ill. Chest. 2001;119(3):926-39.
http://dx.doi.org/10.1378/chest.119.3.92...
22 Araújo PR, Resqueti VR, Nascimento Junior J, Carvalho Lde A, Cavalcanti
AG, Silva VC, et al. Reference values for sniff nasal inspiratory pressure in healthy
subjects in Brazil: a multicenter study. J Bras Pneumol.
2012;38(6):700-7.
http://dx.doi.org/10.1590/S1806-37132012...
23 Chaudri MB, Liu C, Watson L, Jefferson D, Kinnear WJ. Sniff nasal
inspiratory pressure as a marker of respiratory function in motor neuron disease. Eur
Respir J. 2000;15(3):539-42.
http://dx.doi.org/10.1034/j.1399-3003.20...
-
2424 Stefanutti D, Benoist MR, Scheinmann P, Chaussain M, Fitting JW.
Usefulness of sniff nasal pressure in patients with neuromuscular or skeletal
disorders. Am J Respir Crit Care Med. 2000;162(4 Pt 1):1507-11.
http://dx.doi.org/10.1164/ajrccm.162.4.9...
)
Disadvantages
It depends on patient cooperation, it cannot be used in mechanically ventilated patients, it can underestimate values in patients with marked airway obstruction, and it should be used with caution in those with nasal obstruction.
How to measure
The maneuver can be performed in any body position (the most common is sitting),
because, despite minor variations, changes in body position do not result in
significant changes in SNIP. (
2020 Uldry C, Fitting JW. Maximal values of sniff nasal inspiratory pressure
in healthy subjects. Thorax. 1995;50(4):371-5.
http://dx.doi.org/10.1136/thx.50.4.371...
) One nostril should be completely closed by a nose plug to prevent
pressure from leaking, whereas the other nostril should be absolutely patent. After a
period of quiet breathing, the maneuver begins with a fast deep inspiration from FRC
and the mouth closed. A firm verbal command is needed, given that the maneuver should
be short (≤ 500 ms) and explosive so that it causes the collapse of the unplugged
nostril. Ten maneuvers should be performed. However, if there is a considerable
increase in the values obtained in the last maneuvers, up to ten more maneuvers can
be performed. Twenty maneuvers are also necessary when the values of the first ten
maneuvers are below predicted values and when inspiratory muscle weakness due to
exertion is suspected, such as in neuromuscular diseases. (
2626 Lofaso F, Nicot F, Lejaille M, Falaize L, Louis A, Clement A, et al.
Sniff nasal inspiratory pressure: what is the optimal number of sniffs? Eur Respir J.
2006;27(5):980-2.
) The highest value recorded in this series of maneuvers is used for
analysis.
Clinical applicability
SNIP is very useful in assessing inspiratory muscle strength and has high
specificity(
1717 Katagiri M, Abe T, Yokoba M, Dobashi Y, Tomita T, Easton PA. Neck and
abdominal muscle activity during a sniff. Respir Med.
2003;97(9):1027-35.
http://dx.doi.org/10.1016/S0954-6111(03)...
) compared with MIP. In recent years, SNIP has been used for diagnosis and
monitoring of muscle weakness in various pathologies in which a deficit in
inspiratory muscle strength is part of the natural history of the disease, such as in
neuromuscular(
2323 Chaudri MB, Liu C, Watson L, Jefferson D, Kinnear WJ. Sniff nasal
inspiratory pressure as a marker of respiratory function in motor neuron disease. Eur
Respir J. 2000;15(3):539-42.
http://dx.doi.org/10.1034/j.1399-3003.20...
) and pulmonary(
2525 Uldry C, Janssens JP, de Muralt B, Fitting JW. Sniff nasal inspiratory
pressure in patients with chronic obstructive pulmonary disease. Eur Respir J.
1997;10(6):1292-6.
http://dx.doi.org/10.1183/09031936.97.10...
) diseases.
Inspiratory mouth pressure
Inspiratory mouth pressure (Pm) is measured with a pressure sensor attached to a
mouthpiece (as in the measurement of MIP) or to a tracheal tube.(
2727 Baydur A, Behrakis PK, Zin WA, Jaeger M, Milic-Emili J. A simple method
for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis.
1982;126(5):788-91.
) It is usually used in three clinical situations. First, it is used as an
indirect measure of Pes during a sniff, when esophageal catheters are not available
or when esophageal catheter placement is not possible. In this situation, a
limitation of Pm is that, for patients, its measurement is more difficult than that
of SNIP.(
33 American Thoracic Society/European Respiratory Society. ATS/ERS
Statement on respiratory muscle testing. Am J Respir Crit Care Med.
2002;166(4):518-624.
http://dx.doi.org/10.1164/rccm.166.4.518...
) Its second use is in ascertaining the correct placement of the
esophageal catheter, which is discussed later. Finally, Pm is also used in the
measurement of P0.1, which is the pressure generated in the first 100 ms
of an inspiratory effort against a closed airway, and it correlates better with the
measurement of respiratory drive than with the measurement of MIP.
Advantages
It is a simple, noninvasive method, it can use the same instruments used in the measurement of MIP and SNIP, and it is an alternative method in patients with contraindication to esophageal catheters (esophageal varices or severe hypoxemia) or in patients in whom an esophageal catheter cannot be placed (intolerance to passage of catheters or airway anatomical changes).
Disadvantages
For patients, measurements made through the mouth are more difficult than nasal
measurements, and the former provide no additional advantages over the latter. As
occurs with MIP, Pm does not differentiate between which respiratory muscle is
affected. In patients with severe expiratory flow limitation and parenchymal disease,
the transmission of pressure along the airways may be affected, and, in such cases,
Pm may not be an accurate measure of alveolar pressure.(
33 American Thoracic Society/European Respiratory Society. ATS/ERS
Statement on respiratory muscle testing. Am J Respir Crit Care Med.
2002;166(4):518-624.
http://dx.doi.org/10.1164/rccm.166.4.518...
) As occurs with MIP, values can be affected by the type of mouthpiece
used.(
1111 Koulouris N, Mulvey DA, Laroche CM, Green M, Moxham J. Comparison of two
different mouthpieces for the measurement of Pimax and Pemax in normal and weak
subjects. Eur Respir J. 1988;1(9):863-7.
)
How to measure
In the measurement of Pm, the cross-sectional area of the mouthpiece should be wide
enough to prevent errors arising from the Bernoulli effect (a reduction of the
cross-sectional area of a tube leads to an increase in the speed of the gas flow and
a decrease in pressure). In addition, the compliance of the cheeks can distort the
measurement, and, to work around this limitation, the cheeks need to be supported by
both hands during the measurement. In the measurement of P0.1, the distal
end of the mouthpiece should be closed for verification of the correct positioning of
the esophageal balloon.(
2727 Baydur A, Behrakis PK, Zin WA, Jaeger M, Milic-Emili J. A simple method
for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis.
1982;126(5):788-91.
) Pm can be measured nonvolitionally as well, by means of phrenic nerve
stimulation,(
2828 Hamnegåard CH, Wragg S, Kyroussis D, Mills G, Bake B, Green M, et al.
Mouth pressure in response to magnetic stimulation of the phrenic nerves. Thorax.
1995;50(6):620-4.
http://dx.doi.org/10.1136/thx.50.6.620...
29 Hughes PD, Polkey MI, Kyroussis D, Hamnegard CH, Moxham J, Green M.
Measurement of sniff nasal and diaphragm twitch mouth pressure in patients. Thorax.
1998;53(2):96-100.
http://dx.doi.org/10.1136/thx.53.2.96...
-
3030 de Bruin PF, Watson RA, Khalil N, Pride NB. Use of mouth pressure
twitches induced by cervical magnetic stimulation to assess voluntary activation of
the diaphragm. Eur Respir J. 1998;12(3):672-8.
http://dx.doi.org/10.1183/09031936.98.12...
) a topic that is discussed further below.
Clinical applicability
It is mainly used as an indirect measure of Pes during a sniff,(
11 Laghi F, Tobin MJ. Disorders of the respiratory muscles. Am J Respir
Crit Care Med. 2003 1;168(1):10-48.
) in order to confirm inspiratory muscle weakness(
22 Dyspnea. Mechanisms, assessment, and management: a consensus statement.
American Thoracic Society. Am J Respir Crit Care Med.
1999;159(1):321-40.
http://dx.doi.org/10.1164/ajrccm.159.1.a...
); and for verifying the correct positioning of the esophageal balloon
(Figure 3) by using the Baydur
test(
2727 Baydur A, Behrakis PK, Zin WA, Jaeger M, Milic-Emili J. A simple method
for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis.
1982;126(5):788-91.
,
3131 Baydur A, Cha EJ, Sassoon CS. Validation of esophageal balloon technique
at different lung volumes and postures. J Appl Physiol (1985).
1987;62(1):315-21.
)-see How to measure in the next item.
Comparison between inspiratory mouth pressure (Pm) and inspiratory esophageal pressure (Pes) during mouth occlusion (Baydur maneuver), for ascertaining the correct location of the esophageal catheter. Note the good correlation between the two measurements.
Transdiaphragmatic pressure
Transdiaphragmatic pressure (Pdi) is the difference between gastric pressure (Pga) and Pes (Pdi = Pga − Pes; Figure 4) and translates the force generated by the diaphragm rather than by the other respiratory muscles.
Transdiaphragmatic pressure. The top curve represents esophageal pressure, the middle curve represents gastric pressure, and the bottom curve represents transdiaphragmatic pressure (Pdi). In this example, there are differences in the esophageal and gastric pressure measurement range.
Advantages
The strength of the diaphragm, which is the main inspiratory muscle, being
responsible for 60 to 70% of the tidal volume in normal breathing, has
well-established reference values in volunteers of different groups (lower limit of
normal of 70 cmH2O for females and 80 cmH2O for males during a
sniff),(
3232 Polkey MI, Harris ML, Hughes PD, Hamnegärd CH, Lyons D, Green M, et al.
The contractile properties of the elderly human diaphragm. Am J Respir Crit Care Med.
1997;155(5):1560-4.
http://dx.doi.org/10.1164/ajrccm.155.5.9...
) as well as in patients with different respiratory diseases (Table 1).(
3333 de Troyer A, Yernault JC. Inspiratory muscle force in normal subjects
and patients with interstitial lung disease. Thorax.
1980;35(2):92-100.
http://dx.doi.org/10.1136/thx.35.2.92...
,
3434 Laporta D, Grassino A. Assessment of transdiaphragmatic pressure in
humans. J Appl Physiol (1985). 1985;58(5):1469-76.
)
Disadvantages
It is an invasive method, which depends on passing catheters through the nose into the distal esophagus and stomach and which uses materials that are not readily available in most public hospitals. It depends on an experienced examiner for correct placement of the catheters.
How to measure
Pdi can be measured with air-filled latex balloon catheters, fluid-filled catheters,
or microtransducer catheters.(
3535 Akoumianaki E, Maggiore SM, Valenza F, Bellani G, Jubran A, Loring SH,
et al. The application of esophageal pressure measurement in patients with
respiratory failure. Am J Respir Crit Care Med. 2014;189(5):520-31.
http://dx.doi.org/10.1164/rccm.201312-21...
,
3636 Beda A, Güldner A, Carvalho AR, Zin WA, Carvalho NC, Huhle R, et al.
Liquid- and air-filled catheters without balloon as an alternative to the air-filled
balloon catheter for measurement of esophageal pressure. PLoS One.
2014;9(9):e103057.
http://dx.doi.org/10.1371/journal.pone.0...
) The use of balloon catheters requires passing a catheter into the
esophagus and another one into the stomach, although a catheter with two balloons,
which prevents the need for a second catheter, has recently been placed on the
market.(
3737 Chiumello D, Gallazzi E, Marino A, Berto V, Mietto C, Cesana B, et al. A
validation study of a new nasogastric polyfunctional catheter. Intensive Care Med.
2011;37(5):791-5.
http://dx.doi.org/10.1007/s00134-011-217...
) The microtransducer catheter makes Pes and Pga measurements with only
one catheter, as well as having the advantage of being better tolerated by patients
and having a fast response time, which ensures more accurate measurements in fast
maneuvers,(
3838 Stell IM, Tompkins S, Lovell AT, Goldstone JC, Moxham J. An in vivo
comparison of a catheter mounted pressure transducer system with conventional balloon
catheters. Eur Respir J. 1999;13(5):1158-63.
http://dx.doi.org/10.1034/j.1399-3003.19...
) such as measurements using magnetic stimulation of the phrenic nerve.
When using latex balloon catheters, which are the most common ones, one catheter is placed into the distal esophagus and one is placed into the stomach. To ensure correct positioning, it is necessary to observe the Pes and Pga curves. This is easy because, during inspiration, Pes becomes negative and Pga becomes positive, in a mirror image (Figure 5). The final step to ensure that the Pes detected by the balloon catheter is correct is to compare it with the Pm measured by using the closed mouthpiece. If the esophageal positioning is correct, that is, if it reflects pleural pressure well, the variation in Pes will be at least 80% of the variation in Pm. This confirmatory test is known as the Baydur test( 2727 Baydur A, Behrakis PK, Zin WA, Jaeger M, Milic-Emili J. A simple method for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis. 1982;126(5):788-91. ) and has been validated for different lung volumes and postural positions.( 3131 Baydur A, Cha EJ, Sassoon CS. Validation of esophageal balloon technique at different lung volumes and postures. J Appl Physiol (1985). 1987;62(1):315-21. )
Example of simultaneous recording of esophageal and gastric pressures during forced inspiration. Note that as esophageal pressure becomes more negative, gastric pressure becomes positive, creating a mirror image of the two curves.
Pdi can be measured during normal breathing or during maximal inspiratory maneuvers, usually during a sniff. In addition, Pdi can be measured during magnetic stimulation of the phrenic nerve, which is discussed in Non-volitional tests for measuring inspiratory muscle strength (see Electrical and magnetic phrenic nerve stimulation).
Clinical applicability
Because it is an invasive method that requires complex equipment and is complex to
perform, it is used almost exclusively to determine respiratory muscle
strength.(
3535 Akoumianaki E, Maggiore SM, Valenza F, Bellani G, Jubran A, Loring SH,
et al. The application of esophageal pressure measurement in patients with
respiratory failure. Am J Respir Crit Care Med. 2014;189(5):520-31.
http://dx.doi.org/10.1164/rccm.201312-21...
) Its main use is to enable a more representative measurement of diaphragm
strength, especially in patients with airway obstruction, in whom Pes would not be
accurately reflected by Pm or by SNIP.(
33 American Thoracic Society/European Respiratory Society. ATS/ERS
Statement on respiratory muscle testing. Am J Respir Crit Care Med.
2002;166(4):518-624.
http://dx.doi.org/10.1164/rccm.166.4.518...
,
1818 Steier J, Kaul S, Seymour J, Jolley C, Rafferty G, Man W, et al. The
value of multiple tests of respiratory muscle strength. Thorax.
2007;62(11):975-80.
http://dx.doi.org/10.1136/thx.2006.07288...
)
Non-volitional tests for measuring inspiratory muscle strength
Electrical and magnetic phrenic nerve stimulation
The use of non-volitional tests for measuring inspiratory muscle strength is
recommended when patients have difficulty understanding or performing the maneuvers,
generating low values during the volitional maneuvers (MIP, SNIP, or Pm); or when
there is considerable variation in the measurements, which is probably secondary to
different levels of effort. To obtain maximal involuntary inspiratory contraction,
there are two possible methods that yield similar results: electrical stimulation or
magnetic (twitch) stimulation of the phrenic nerve. Both are based on stimulating the
cervical phrenic nerve, which is superficial (Figure
6). Electrical stimulation is painful, and there are reports of it inducing
convulsion; however, it is more specific for diaphragm stimulation than is magnetic
stimulation.(
3939 Wragg S, Aquilina R, Moran J, Ridding M, Hamnegard C, Fearn T, et al.
Comparison of cervical magnetic stimulation and bilateral percutaneous electrical
stimulation of the phrenic nerves in normal subjects. Eur Respir J.
1994;7(10):1788-92.
http://dx.doi.org/10.1183/09031936.94.07...
) Magnetic phrenic nerve stimulation causes minimal discomfort, which is
well tolerated by most patients.(
4040 Similowski T, Fleury B, Launois S, Cathala HP, Bouche P, Derenne JP.
Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve
stimulation in conscious humans. J Appl Physiol (1985).
1989;67(4):1311-8.
) Its principle is to create a magnetic field in the cervical region by
placing small coils over this region. Pdi values are similar with magnetic and
electrical stimulation.(
4040 Similowski T, Fleury B, Launois S, Cathala HP, Bouche P, Derenne JP.
Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve
stimulation in conscious humans. J Appl Physiol (1985).
1989;67(4):1311-8.
) Since magnetic phrenic nerve stimulation provides greater safety and
comfort, its use has surpassed that of electrical stimulation.
Phrenic nerve magnetic stimulation coil placed on the anterior cervical area of a volunteer.
Advantages
It allows the measurement of inspiratory muscle strength, irrespective of patient
cooperation or understanding. The reason for it is that the diaphragm is innervated
exclusively by the phrenic nerve, and this enables overall muscle stimulation.
Magnetic stimulation easily penetrates tissues and bones, preferentially activating
larger neural fibers rather than smaller fibers, which are responsible for mediating
pain.(
4141 Man WD, Moxham J, Polkey MI. Magnetic stimulation for the measurement of
respiratory and skeletal muscle function. Eur Respir J.
2004;24(5):846-60.
http://dx.doi.org/10.1183/09031936.04.00...
) There are well defined Pdi values after bilateral cervical magnetic
stimulation (lower limit of normal of 20 cmH2O for females and
males).(
4040 Similowski T, Fleury B, Launois S, Cathala HP, Bouche P, Derenne JP.
Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve
stimulation in conscious humans. J Appl Physiol (1985).
1989;67(4):1311-8.
)
Disadvantages
Since the magnetic field can stimulate other cervical nerves and muscles, its use is
usually less specific for the measurement of diaphragm strength than is that of
electrical stimulation, although this difference does not appear to be clinically
relevant.(
3939 Wragg S, Aquilina R, Moran J, Ridding M, Hamnegard C, Fearn T, et al.
Comparison of cervical magnetic stimulation and bilateral percutaneous electrical
stimulation of the phrenic nerves in normal subjects. Eur Respir J.
1994;7(10):1788-92.
http://dx.doi.org/10.1183/09031936.94.07...
,
4040 Similowski T, Fleury B, Launois S, Cathala HP, Bouche P, Derenne JP.
Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve
stimulation in conscious humans. J Appl Physiol (1985).
1989;67(4):1311-8.
) Another disadvantage is that magnetic stimulation equipment is not
readily available and is costly.
How to measure
The device consists of a base with a capacitor connected to a coil that is placed
over the site to be stimulated. The type of coil has considerable influence on the
intensity and form of the magnetic field generated. Initially, the most widely used
coil was the 90-mm circular coil placed on the posterior cervical area at the level
of the seventh cervical vertebra. This coil, however, created a larger magnetic field
and ended up stimulating other neural fibers in the neck and upper intercostal
muscles. The coil currently in use is the 45-mm figure-of-eight coil, which creates a
field more focused on the phrenic nerve when it is placed over the posterior edge of
the sternocleidomastoid muscle at the level of the cricoid cartilage. With one
figure-of-eight coil, it is possible to measure the force generated by one
hemidiaphragm alone, and with two coils activated simultaneously, it is possible to
measure the force generated by both hemidiaphragms together.(
33 American Thoracic Society/European Respiratory Society. ATS/ERS
Statement on respiratory muscle testing. Am J Respir Crit Care Med.
2002;166(4):518-624.
http://dx.doi.org/10.1164/rccm.166.4.518...
,
3939 Wragg S, Aquilina R, Moran J, Ridding M, Hamnegard C, Fearn T, et al.
Comparison of cervical magnetic stimulation and bilateral percutaneous electrical
stimulation of the phrenic nerves in normal subjects. Eur Respir J.
1994;7(10):1788-92.
http://dx.doi.org/10.1183/09031936.94.07...
,
4040 Similowski T, Fleury B, Launois S, Cathala HP, Bouche P, Derenne JP.
Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve
stimulation in conscious humans. J Appl Physiol (1985).
1989;67(4):1311-8.
) The measurements most commonly made using magnetic phrenic nerve
stimulation are those of Pdi and Pm. Although the measurement of Pm is noninvasive,
it depends on the glottis remaining open after magnetic stimulation, and this may
result in considerably underestimated values in patients with increased airway
resistance and severe parenchymal disease. A disadvantage of measuring Pdi is the
need for insertion of esophageal and gastric catheters.
Clinical applicability
It is used mainly in research and clinical settings when one wants to avoid variability related to patient cooperation or when patients cannot cooperate properly, such as mechanically ventilated patients or those who cannot understand or perform the requested maneuvers.
Diaphragm ultrasound
In recent years, there has been a great increase in interest in the use of ultrasound
to assess the diaphragm.(
4242 Lerolle N, Diehl JL. Ultrasonographic evaluation of diaphragmatic
function. Crit Care Med. 2011;39(12):2760-1.
http://dx.doi.org/10.1097/CCM.0b013e3182...
) The literature has demonstrated that diaphragm ultrasound is a useful
tool for bedside assessment, because it is noninvasive and radiation-free, it is
readily available in hospitals, and it allows repeated assessments. Diaphragm
ultrasound has accuracy similar to that of fluoroscopy for assessment of diaphragm
motion.(
4343 Houston JG, Fleet M, Cowan MD, McMillan NC. Comparison of ultrasound
with fluoroscopy in the assessment of suspected hemidiaphragmatic movement
abnormality. Clin Radiol. 1995;50(2):95-8.
http://dx.doi.org/10.1016/S0009-9260(05)...
) There have been some recent articles in different publications
discussing the use of ultrasound for assessment of diaphragm function in mechanically
ventilated patients, especially for predicting extubation failure,(
4444 Matamis D, Soilemezi E, Tsagourias M, Akoumianaki E, Dimassi S, Boroli
F, et al. Sonographic evaluation of the diaphragm in critically ill patients.
Technique and clinical applications. Intensive Care Med.
2013;39(5):801-10.
http://dx.doi.org/10.1007/s00134-013-282...
) and for diagnosis and monitoring of inadvertent injury occurring during
surgery.(
4545 Lerolle N, Guérot E, Dimassi S, Zegdi R, Faisy C, Fagon JY, et al.
Ultrasonographic diagnostic criterion for severe diaphragmatic dysfunction after
cardiac surgery. Chest. 2009;135(2):401-7.
http://dx.doi.org/10.1378/chest.08-1531...
) There have also been articles discussing the use of ultrasound for
diagnosis and monitoring of diaphragm paralysis in outpatients. (
4646 Gottesman E, McCool FD. Ultrasound evaluation of the paralyzed
diaphragm. Am J Respir Crit Care Med. 1997;155(5):1570-4.
http://dx.doi.org/10.1164/ajrccm.155.5.9...
,
4747 Summerhill EM, El-Sameed YA, Glidden TJ, McCool FD. Monitoring recovery
from diaphragm paralysis with ultrasound. Chest. 2008;133(3):737-43.
http://dx.doi.org/10.1378/chest.07-2200...
)
Advantages
It is a noninvasive, radiation-free method; it can be repeated several times over a
short period of time; it uses a basically configured ultrasound system, which is a
piece of equipment that has become common in hospitals and clinics; and the learning
time is not long. Finally, normal values for diaphragm thickening and motion are well
established (Table 1). For males and females,
diaphragm motion during quiet breathing should be at least 11 mm, and during deep
breathing, it should be at least 47 mm. For males and females, diaphragm thickening
after inspiration to TLC should be at least 1.5% or 20%.(
4848 Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ.
Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal
subjects. Muscle Nerve. 2013;47(6):884-9.
http://dx.doi.org/10.1002/mus.23702...
49 Boussuges A, Gole Y, Blanc P. Diaphragmatic motion studied by m-mode
ultrasonography: methods, reproducibility, and normal values. Chest.
2009;135(2):391-400.
http://dx.doi.org/10.1378/chest.08-1541...
-
5050 Testa A, Soldati G, Giannuzzi R, Berardi S, Portale G, Gentiloni Silveri
N. Ultrasound M-mode assessment of diaphragmatic kinetics by anterior transverse
scanning in healthy subjects. Ultrasound Med Biol. 2011;37(1):44-52.
http://dx.doi.org/10.1016/j.ultrasmedbio...
)
Disadvantages
It is an operator-dependent method, and, in obese patients with abdominal distention or extensive dressings, it can be difficult to obtain good quality images. Diaphragm motion is affected by abdominal pressure and contents, and this decreases the relationship between diaphragm motion and variation in lung volume during the maneuvers, thus requiring the concomitant use of a pneumotachograph.
How to measure
The use of ultrasound allows us to measure diaphragm dome motion and diaphragm
thickness in the zone of apposition to the rib cage (Figure 7A and B). Diaphragm dome
motion is measured with a (cardiac or convex) low-frequency (3-5 MHz) transducer,
which is held against the highest point of the diaphragm (the diaphragm dome).
Depending on the method used, the transducer can be placed in the
transverse(
5050 Testa A, Soldati G, Giannuzzi R, Berardi S, Portale G, Gentiloni Silveri
N. Ultrasound M-mode assessment of diaphragmatic kinetics by anterior transverse
scanning in healthy subjects. Ultrasound Med Biol. 2011;37(1):44-52.
http://dx.doi.org/10.1016/j.ultrasmedbio...
) or longitudinal(
4949 Boussuges A, Gole Y, Blanc P. Diaphragmatic motion studied by m-mode
ultrasonography: methods, reproducibility, and normal values. Chest.
2009;135(2):391-400.
http://dx.doi.org/10.1378/chest.08-1541...
) direction in the subcostal region, the reference being the point between
the midclavicular and anterior axillary lines. The diaphragm is visualized in B-mode,
and diaphragm excursion is measured in M-mode, which reduces interobserver
variability. (
5151 Rahn H, Otis A, Fenn WO. The pressure-volume diagram of the thorax and
lung. Fed Proc. 1946;5(1 Pt 2):82.
) It is important to assess motion not only during normal breathing but
also during fast and slow deep inspiration. Assessing motion during a sniff is useful
because it enhances the detection of paradoxical motion of the diaphragm, which may
not occur during normal breathing. Motion measurement of the right and left
hemidiaphragms yields equal values, but measurement on the right is easier because of
the presence of the liver, which creates an acoustic window (Figure 7A).
Ultrasound imaging of the diaphragm. In A, an ultrasound scan for assessment of diaphragm motion. The top image is a B-mode image, and the gray arrow indicates the diaphragm, which is seen as a more echogenic line. The bottom image is the top image in M-mode and serves to measure diaphragm excursion (distances between A-A and B-B points) during breathing at rest. In A, diaphragm motion was 19.5 and 18.1 mm and was, therefore, normal. In B, an ultrasound scan for assessment of diaphragm thickening. The top image is a B-mode image, and the white arrow indicated the diaphragm, which is seen as a more echogenic line. The bottom image is the top image in M-mode and serves to measure diaphragm thickening during inspiration (A-A points) and the next expiration (B-B points). In B, diaphragm thickening was 1.3 mm and was, therefore,
Diaphragm thickening is measured with a high-frequency (7-10 MHz) transducer placed
in the zone of apposition of the diaphragm to the midaxillary line. Diaphragm
thickness is the distance between the two hyperechogenic lines representing its
borders (Figure 7B). This thickness is usually
measured at FRC and also at TLC after a maximal inspiration.(
4848 Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ.
Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal
subjects. Muscle Nerve. 2013;47(6):884-9.
http://dx.doi.org/10.1002/mus.23702...
) Diaphragm thickening should increase by at least 20% at TLC when
compared with the value obtained at FRC.
Clinical applicability
Diaphragm ultrasound can be used at the bedside or in an outpatient setting. It
allows the assessment of two useful fundamental parameters: diaphragm motion and
diaphragm thickness. In addition, it can be performed in different body positions.
The respiratory diseases about which there exist the largest number of studies with
the use of diaphragm ultrasound are COPD and diaphragm paralysis, and there are
studies with the use of diaphragm ultrasound in weaning from mechanical
ventilation.(
4747 Summerhill EM, El-Sameed YA, Glidden TJ, McCool FD. Monitoring recovery
from diaphragm paralysis with ultrasound. Chest. 2008;133(3):737-43.
http://dx.doi.org/10.1378/chest.07-2200...
,
4848 Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ.
Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal
subjects. Muscle Nerve. 2013;47(6):884-9.
http://dx.doi.org/10.1002/mus.23702...
)
Volitional tests for measuring expiratory muscle strength
Maximal expiratory pressure
Maximal expiratory pressure (MEP) is the most widely used measure of expiratory
muscle strength in critically ill patients and in outpatients.(
33 American Thoracic Society/European Respiratory Society. ATS/ERS
Statement on respiratory muscle testing. Am J Respir Crit Care Med.
2002;166(4):518-624.
http://dx.doi.org/10.1164/rccm.166.4.518...
)
Advantages
It is simple and rapid to perform; it uses low-cost, low-complexity equipment (the
same used for measuring MIP); and it has well-established reference values (lower
limit of normal of 120 cmH2O for females and 150 cmH2O for
males; Table 1).(
5252 Coelho CM, Carvalho RM, Gouvêa DS, Novo Júnior JM. Comparisons among
parameters of maximal respiratory pressures in healthy subjects. J Bras Pneumol.
2012;38(5):605-13.
http://dx.doi.org/10.1590/S1806-37132012...
)
Disadvantages
It depends on patient cooperation and on the coordination between the patient and the examiner, as well as having low accuracy for predicting cough capacity. It has a high rate of false-positive results for expiratory muscle weakness because it can overestimate the number of patients with expiratory muscle weakness, given that low values are caused by submaximal efforts or air leaks around the mouthpiece, which is common in patients with facial muscle weakness.
How to measure
MEP is measured with a pressure manometer. Measurements are usually made with patients in a sitting position and with a nose clip, although the use of a nose clip is not necessary. MEP can be measured from TLC or from FRC. Patients perform a maximal expiratory effort and sustain it for 1 to 2 seconds. The maneuver should be repeated 3 to 8 times, and the highest value recorded is used for analysis. Since there is a direct relationship between lung volume and expiratory muscle strength,( 5151 Rahn H, Otis A, Fenn WO. The pressure-volume diagram of the thorax and lung. Fed Proc. 1946;5(1 Pt 2):82. ) measurements from TLC yield higher values than those obtained from measurements from FRC.
Clinical applicability
Its major use is in assessing cough strength, given that one of the phases of cough
is explosive expiration and expiratory muscle weakness correlates with respiratory
infections(
5353 Irwin RS, Boulet LP, Cloutier MM, Fuller R, Gold PM, Hoffstein V, et al.
Managing cough as a defense mechanism and as a symptom. A consensus panel report of
the American College of Chest Physicians. Chest. 1998;114(2 Suppl
Managing):133S-181S.
) and extubation failure.(
5454 Khamiees M, Raju P, DeGirolamo A, Amoateng-Adjepong Y, Manthous CA.
Predictors of extubation outcome in patients who have successfully completed a
spontaneous breathing trial. Chest. 2001;120(4):1262-70.
http://dx.doi.org/10.1378/chest.120.4.12...
)
Cough gastric pressure
Measuring Pga during a cough is a useful additional test in the assessment of expiratory muscle weakness, because abdominal muscles are the primary muscles responsible for expiratory flow.
Advantages
It has well-established reference values (lower limit of normal of 95
cmH2O for females and 130 cmH2O for males; Table 1),(
5555 Man WD, Kyroussis D, Fleming TA, Chetta A, Harraf F, Mustfa N, et al.
Cough gastric pressure and maximum expiratory mouth pressure in humans. Am J Respir
Crit Care Med. 2003;168(6):714-7.
http://dx.doi.org/10.1164/rccm.200303-33...
) and its specificity is greater than that of MEP. Therefore, the negative
predictive value of cough Pga is higher than that of MEP alone. A previous study
showed that 42% of patients with reduced MEP actually had normal cough Pga
values.(
5555 Man WD, Kyroussis D, Fleming TA, Chetta A, Harraf F, Mustfa N, et al.
Cough gastric pressure and maximum expiratory mouth pressure in humans. Am J Respir
Crit Care Med. 2003;168(6):714-7.
http://dx.doi.org/10.1164/rccm.200303-33...
)
Disadvantages
Its main disadvantage is that it is an invasive method that requires the insertion of a catheter with a pressure sensor into the stomach.
How to measure Pga is typically measured with a catheter, following
the same recommendations as those already described for the measurement of Pdi
(see Transdiaphragmatic pressure). Patients in a sitting position
are instructed to inhale to TLC and then cough with maximum force, repeating the
maneuver at 30-second intervals until the values stop increasing. Typically, up to
six maneuvers are necessary.(
5555 Man WD, Kyroussis D, Fleming TA, Chetta A, Harraf F, Mustfa N, et al.
Cough gastric pressure and maximum expiratory mouth pressure in humans. Am J Respir
Crit Care Med. 2003;168(6):714-7.
http://dx.doi.org/10.1164/rccm.200303-33...
)
Clinical applicability
It is used to rule out expiratory muscle weakness, especially in patients suspected of having reduced cough strength due to expiratory pump impairment, such as patients with neuromuscular disease and critically ill patients immediately before or after extubation.
Non-volitional tests for measuring expiratory muscle strength
Gastric pressure after magnetic stimulation of the anterior abdominal wall muscles
In uncooperative patients, expiratory muscle strength can be assessed by measuring
Pga after neural magnetic stimulation of the abdominal wall muscles.(
33 American Thoracic Society/European Respiratory Society. ATS/ERS
Statement on respiratory muscle testing. Am J Respir Crit Care Med.
2002;166(4):518-624.
http://dx.doi.org/10.1164/rccm.166.4.518...
,
5656 Kyroussis D, Mills GH, Polkey MI, Hamnegard CH, Koulouris N, Green M, et
al. Abdominal muscle fatigue after maximal ventilation in humans. J Appl Physiol
(1985). 1996;81(4):1477-83.
,
5757 Kyroussis D, Polkey MI, Mills GH, Hughes PD, Moxham J, Green M.
Simulation of cough in man by magnetic stimulation of the thoracic nerve roots. Am J
Respir Crit Care Med. 1997;156(5):1696-9.
http://dx.doi.org/10.1164/ajrccm.156.5.9...
) Magnetic stimulation is produced by placing a circular coil over the
dorsal spine, at the level of the eighth to tenth thoracic vertebra (T8 to
T10).(
5656 Kyroussis D, Mills GH, Polkey MI, Hamnegard CH, Koulouris N, Green M, et
al. Abdominal muscle fatigue after maximal ventilation in humans. J Appl Physiol
(1985). 1996;81(4):1477-83.
,
5858 Suzuki J, Tanaka R, Yan S, Chen R, Macklem PT, Kayser B. Assessment of
abdominal muscle contractility, strength, and fatigue. Am J Respir Crit Care Med.
1999;159(4 Pt 1):1052-60.
http://dx.doi.org/10.1164/ajrccm.159.4.9...
)
Advantages
Values are independent of patient cooperation.
Disadvantages
This measurement is invasive because it requires passage of a catheter into the
stomach, and there exists only one study that reported reference values, in a small
sample of individuals (lower limit of normal of 10 cmH2O for females and
males; Table 1).(
1818 Steier J, Kaul S, Seymour J, Jolley C, Rafferty G, Man W, et al. The
value of multiple tests of respiratory muscle strength. Thorax.
2007;62(11):975-80.
http://dx.doi.org/10.1136/thx.2006.07288...
)
How to measure
This measurement can be made with a balloon catheter or a microtransducer catheter placed into the stomach. To ensure the correct positioning of the catheter, it is necessary to observe the pressure curve, which, during inspiration, should have positive values (Figure 4). Another means to ensure correct positioning in the stomach is to employ manual compression of the epigastrium and observe an increase in Pga. When the catheter is correctly positioned in the stomach, magnetic stimulation is performed over the dorsal spine, between T8 and T10, and the pressure variation is recorded. Approximately 5 measurements are performed at intervals of at least 30 seconds to avoid muscle potentiation.
Clinical applicability
This measurement is used to confirm possible expiratory muscle weakness,(
4343 Houston JG, Fleet M, Cowan MD, McMillan NC. Comparison of ultrasound
with fluoroscopy in the assessment of suspected hemidiaphragmatic movement
abnormality. Clin Radiol. 1995;50(2):95-8.
http://dx.doi.org/10.1016/S0009-9260(05)...
,
5959 Merletti R, Botter A, Troiano A, Merlo E, Minetto MA. Technology and
instrumentation for detection and conditioning of the surface electromyographic
signal: state of the art. Clin Biomech (Bristol, Avon).
2009;24(2):122-34.
http://dx.doi.org/10.1016/j.clinbiomech....
) especially in individuals with difficulty performing volitional tests
intended to assess cough strength, such as patients with neuromuscular disease and
critically ill patients.
Electromyography
Electromyography is the study of muscle activity based on analysis of
electromyographic signals, which are electrical manifestations generated during
voluntary or stimulated contractions. It can performed with electrodes attached to
the skin (surface electromyography)(
5959 Merletti R, Botter A, Troiano A, Merlo E, Minetto MA. Technology and
instrumentation for detection and conditioning of the surface electromyographic
signal: state of the art. Clin Biomech (Bristol, Avon).
2009;24(2):122-34.
http://dx.doi.org/10.1016/j.clinbiomech....
) or with fine needles inserted into the surface of the muscle that is
assessed (needle electromyography).(
6060 Daube JR, Rubin DI. Needle electromyography. Muscle Nerve.
2009;39(2):244-70.
http://dx.doi.org/10.1002/mus.21180...
,
6161 Rubin DI. Needle electromyography: basic concepts and patterns of
abnormalities. Neurol Clin. 2012;30(2):429-56.
http://dx.doi.org/10.1016/j.ncl.2011.12....
) In the case of respiratory muscles, there is a third option, which is
the use of esophageal electrode catheters to perform crural diaphragm
electromyography.(
6262 Luo YM, Moxham J, Polkey MI. Diaphragm electromyography using an
oesophageal catheter: current concepts. Clin Sci (Lond).
2008;115(8):233-44.
http://dx.doi.org/10.1042/CS20070348...
,
6363 Luo YM, Polkey MI, Johnson LC, Lyall RA, Harris ML, Green M, et al.
Diaphragm EMG measured by cervical magnetic and electrical phrenic nerve stimulation.
J Appl Physiol (1985). 1998;85(6):2089-99.
)
Advantages
Surface electromyography is a noninvasive, easy-to-use method, being quite useful for continuous monitoring. It is extremely sensitive for detecting muscle contractions.( 6464 Criswell E. Cram's Introduction to Surface Electromyography. 2nd ed. Burlington (MA): Jones & Bartlett Learning; 2010. ) Needle electromyography is minimally invasive and mildly painful.
Disadvantages
The major problem in performing surface electromyography is interference from the activity of other muscle groups (cross-talk). Because electromyography is highly sensitive, it is often difficult to isolate the activity of only one muscle group. Another disadvantage is the limited standardization for analysis of the signal, which can be interpreted visually through its amplitude and duration components or through a numerical value obtained by squaring the signal amplitude and subsequently extracting the root square of the result (root mean square value). Diaphragm electromyography with esophageal catheters is invasive and depends on materials and skills that are highly specific and are still not readily available, although there is a mechanical ventilation apparatus available on the market that has a ventilation mode based on the acquisition of esophageal electromyography signals (the Neurally Adjusted Ventilatory Assist [NAVA] mode of ventilation of the Servo ventilators; Maquet, Sweden). In this apparatus, esophageal electromyography monitoring can be performed even with the patient off the ventilator. Finally, there are no population reference values, which makes it difficult to use this measurement as an index of diagnosis of muscle weakness.
How to measure
The received signals are amplified and filtered, and this can be adjusted and will
depend on the characteristics of the acquired signal. The most commonly employed
method is electromyography with electrodes over the muscle, after the region has been
thoroughly cleaned to improve the transmission of the electrical signal.(
5959 Merletti R, Botter A, Troiano A, Merlo E, Minetto MA. Technology and
instrumentation for detection and conditioning of the surface electromyographic
signal: state of the art. Clin Biomech (Bristol, Avon).
2009;24(2):122-34.
http://dx.doi.org/10.1016/j.clinbiomech....
) It is also possible to use needles inserted intramuscularly, thereby
obtaining a signal that is less noisy and more representative of a particular muscle
activity. In obese individuals, needle electromyography of the abdominal muscles has
a more significant result than that obtained with surface electrode electromyography.
Often, needle insertion is ultrasound guided in order to prevent bleeding or
perforation of other organs.(
6060 Daube JR, Rubin DI. Needle electromyography. Muscle Nerve.
2009;39(2):244-70.
http://dx.doi.org/10.1002/mus.21180...
,
6161 Rubin DI. Needle electromyography: basic concepts and patterns of
abnormalities. Neurol Clin. 2012;30(2):429-56.
http://dx.doi.org/10.1016/j.ncl.2011.12....
) Finally, it is also possible to use esophageal electromyography, in
which one seeks to study the activity of the crural diaphragm by positioning the
electrodes 1 to 3 cm above the esophageal-gastric junction.(
6262 Luo YM, Moxham J, Polkey MI. Diaphragm electromyography using an
oesophageal catheter: current concepts. Clin Sci (Lond).
2008;115(8):233-44.
http://dx.doi.org/10.1042/CS20070348...
,
6363 Luo YM, Polkey MI, Johnson LC, Lyall RA, Harris ML, Green M, et al.
Diaphragm EMG measured by cervical magnetic and electrical phrenic nerve stimulation.
J Appl Physiol (1985). 1998;85(6):2089-99.
)
Clinical applicability
Electromyography is a reliable method for continuous monitoring, especially of certain respiratory muscles, such as abdominal expiratory muscles and inspiratory accessory muscles, provided that care is taken in the technical preparation. Its major use is in monitoring the same individual continuously, because absolute values do not allow comparisons between individuals. Surface electromyography is used for qualitative assessment of recruitment of inspiratory accessory muscles and abdominal expiratory muscles. When this assessment needs to be more specific or quantitative (usually for research purposes), the method used is needle electromyography. In addition to being used for research purposes, diaphragm electromyography is used as a guide in the NAVA mode of ventilation.
Final considerations
Respiratory muscle impairment is present not only in respiratory diseases but also in various other diseases, and its proper assessment depends on the use of appropriate tests. Noninvasive volitional tests are still the most commonly used tests in clinical practice, because they are more widely known and because of their ease of use in different centers. However, patients highly suspected of having ventilatory muscle weakness and with difficulty understanding these tests should undergo additional assessment with more invasive, non-volitional tests, although they are not readily available and, to date, they have been mostly used in research centers.
References
-
1Laghi F, Tobin MJ. Disorders of the respiratory muscles. Am J Respir Crit Care Med. 2003 1;168(1):10-48.
-
2Dyspnea. Mechanisms, assessment, and management: a consensus statement. American Thoracic Society. Am J Respir Crit Care Med. 1999;159(1):321-40.
» http://dx.doi.org/10.1164/ajrccm.159.1.ats898 -
3American Thoracic Society/European Respiratory Society. ATS/ERS Statement on respiratory muscle testing. Am J Respir Crit Care Med. 2002;166(4):518-624.
» http://dx.doi.org/10.1164/rccm.166.4.518 -
4Neder JA, Andreoni S, Lerario MC, Nery LE. Reference values for lung function tests. II. Maximal respiratory pressures and voluntary ventilation. Braz J Med Biol Res. 1999;32(6):719-27.
» http://dx.doi.org/10.1590/S0100-879X1999000600007 -
5Black LF, Hyatt RE. Maximal respiratory pressures: normal values and relationship to age and sex. Am Rev Respir Dis. 1969;99(5):696-702.
-
6Black LF, Hyatt RE. Maximal static respiratory pressures in generalized neuromuscular disease. Am Rev Respir Dis. 1971;103(5):641-50.
-
7De Troyer A, Borenstein S, Cordier R. Analysis of lung volume restriction in patients with respiratory muscle weakness. Thorax. 1980;35(8):603-10.
» http://dx.doi.org/10.1136/thx.35.8.603 -
8Caruso P, Friedrich C, Denari SD, Ruiz SA, Deheinzelin D. The unidirectional valve is the best method to determine maximal inspiratory pressure during weaning. Chest. 1999;115(4):1096-101.
» http://dx.doi.org/10.1378/chest.115.4.1096 -
9Yang KL, Tobin MJ. A prospective study of indexes predicting the outcome of trials of weaning from mechanical ventilation. N Engl J Med. 1991;324(21):1445-50.
» http://dx.doi.org/10.1056/NEJM199105233242101 -
10Sociedade Brasileira de Pneumologia e Tisiologia. Diretrizes para Testes de Função Pulmonar. J Pneumol. 2002;28(Suppl 3):S155-S165.
-
11Koulouris N, Mulvey DA, Laroche CM, Green M, Moxham J. Comparison of two different mouthpieces for the measurement of Pimax and Pemax in normal and weak subjects. Eur Respir J. 1988;1(9):863-7.
-
12Truwit JD, Marini JJ. Validation of a technique to assess maximal inspiratory pressure in poorly cooperative patients. Chest. 1992;102(4):1216-9.
» http://dx.doi.org/10.1378/chest.102.4.1216 -
13Caruso P, Denari SD, Ruiz SA, Bernal KG, Manfrin GM, Friedrich C, et al. Inspiratory muscle training is ineffective in mechanically ventilated critically ill patients. Clinics (Sao Paulo). 2005;60(6):479-84.
» http://dx.doi.org/10.1590/S1807-59322005000600009 -
14Martin AD, Smith BK, Davenport PD, Harman E, Gonzalez-Rothi RJ, Baz M, et al. Inspiratory muscle strength training improves weaning outcome in failure to wean patients: a randomized trial. Crit Care. 2011;15(2):R84.
» http://dx.doi.org/10.1186/cc10081 -
15Koulouris N, Vianna LG, Mulvey DA, Green M, Moxham J. Maximal relaxation rates of esophageal, nose, and mouth pressures during a sniff reflect inspiratory muscle fatigue. Am Rev Respir Dis. 1989;139(5):1213-7.
» http://dx.doi.org/10.1164/ajrccm/139.5.1213 -
16Héritier F, Rahm F, Pasche P, Fitting JW. Sniff nasal inspiratory pressure. A noninvasive assessment of inspiratory muscle strength. Am J Respir Crit Care Med. 1994;150(6 Pt 1):1678-83.
» http://dx.doi.org/10.1164/ajrccm.150.6.7952632 -
17Katagiri M, Abe T, Yokoba M, Dobashi Y, Tomita T, Easton PA. Neck and abdominal muscle activity during a sniff. Respir Med. 2003;97(9):1027-35.
» http://dx.doi.org/10.1016/S0954-6111(03)00133-1 -
18Steier J, Kaul S, Seymour J, Jolley C, Rafferty G, Man W, et al. The value of multiple tests of respiratory muscle strength. Thorax. 2007;62(11):975-80.
» http://dx.doi.org/10.1136/thx.2006.072884 -
19Laroche CM, Mier AK, Moxham J, Green M. The value of sniff esophageal pressures in the assessment of global inspiratory muscle strength. Am Rev Respir Dis. 1988;138(3):598-603.
» http://dx.doi.org/10.1164/ajrccm/138.3.598 -
20Uldry C, Fitting JW. Maximal values of sniff nasal inspiratory pressure in healthy subjects. Thorax. 1995;50(4):371-5.
» http://dx.doi.org/10.1136/thx.50.4.371 -
21Polkey MI, Moxham J. Clinical aspects of respiratory muscle dysfunction in the critically ill. Chest. 2001;119(3):926-39.
» http://dx.doi.org/10.1378/chest.119.3.926 -
22Araújo PR, Resqueti VR, Nascimento Junior J, Carvalho Lde A, Cavalcanti AG, Silva VC, et al. Reference values for sniff nasal inspiratory pressure in healthy subjects in Brazil: a multicenter study. J Bras Pneumol. 2012;38(6):700-7.
» http://dx.doi.org/10.1590/S1806-37132012000600004 -
23Chaudri MB, Liu C, Watson L, Jefferson D, Kinnear WJ. Sniff nasal inspiratory pressure as a marker of respiratory function in motor neuron disease. Eur Respir J. 2000;15(3):539-42.
» http://dx.doi.org/10.1034/j.1399-3003.2000.15.18.x -
24Stefanutti D, Benoist MR, Scheinmann P, Chaussain M, Fitting JW. Usefulness of sniff nasal pressure in patients with neuromuscular or skeletal disorders. Am J Respir Crit Care Med. 2000;162(4 Pt 1):1507-11.
» http://dx.doi.org/10.1164/ajrccm.162.4.9910034 -
25Uldry C, Janssens JP, de Muralt B, Fitting JW. Sniff nasal inspiratory pressure in patients with chronic obstructive pulmonary disease. Eur Respir J. 1997;10(6):1292-6.
» http://dx.doi.org/10.1183/09031936.97.10061292 -
26Lofaso F, Nicot F, Lejaille M, Falaize L, Louis A, Clement A, et al. Sniff nasal inspiratory pressure: what is the optimal number of sniffs? Eur Respir J. 2006;27(5):980-2.
-
27Baydur A, Behrakis PK, Zin WA, Jaeger M, Milic-Emili J. A simple method for assessing the validity of the esophageal balloon technique. Am Rev Respir Dis. 1982;126(5):788-91.
-
28Hamnegåard CH, Wragg S, Kyroussis D, Mills G, Bake B, Green M, et al. Mouth pressure in response to magnetic stimulation of the phrenic nerves. Thorax. 1995;50(6):620-4.
» http://dx.doi.org/10.1136/thx.50.6.620 -
29Hughes PD, Polkey MI, Kyroussis D, Hamnegard CH, Moxham J, Green M. Measurement of sniff nasal and diaphragm twitch mouth pressure in patients. Thorax. 1998;53(2):96-100.
» http://dx.doi.org/10.1136/thx.53.2.96 -
30de Bruin PF, Watson RA, Khalil N, Pride NB. Use of mouth pressure twitches induced by cervical magnetic stimulation to assess voluntary activation of the diaphragm. Eur Respir J. 1998;12(3):672-8.
» http://dx.doi.org/10.1183/09031936.98.12030672 -
31Baydur A, Cha EJ, Sassoon CS. Validation of esophageal balloon technique at different lung volumes and postures. J Appl Physiol (1985). 1987;62(1):315-21.
-
32Polkey MI, Harris ML, Hughes PD, Hamnegärd CH, Lyons D, Green M, et al. The contractile properties of the elderly human diaphragm. Am J Respir Crit Care Med. 1997;155(5):1560-4.
» http://dx.doi.org/10.1164/ajrccm.155.5.9154857 -
33de Troyer A, Yernault JC. Inspiratory muscle force in normal subjects and patients with interstitial lung disease. Thorax. 1980;35(2):92-100.
» http://dx.doi.org/10.1136/thx.35.2.92 -
34Laporta D, Grassino A. Assessment of transdiaphragmatic pressure in humans. J Appl Physiol (1985). 1985;58(5):1469-76.
-
35Akoumianaki E, Maggiore SM, Valenza F, Bellani G, Jubran A, Loring SH, et al. The application of esophageal pressure measurement in patients with respiratory failure. Am J Respir Crit Care Med. 2014;189(5):520-31.
» http://dx.doi.org/10.1164/rccm.201312-2193CI -
36Beda A, Güldner A, Carvalho AR, Zin WA, Carvalho NC, Huhle R, et al. Liquid- and air-filled catheters without balloon as an alternative to the air-filled balloon catheter for measurement of esophageal pressure. PLoS One. 2014;9(9):e103057.
» http://dx.doi.org/10.1371/journal.pone.0103057 -
37Chiumello D, Gallazzi E, Marino A, Berto V, Mietto C, Cesana B, et al. A validation study of a new nasogastric polyfunctional catheter. Intensive Care Med. 2011;37(5):791-5.
» http://dx.doi.org/10.1007/s00134-011-2178-4 -
38Stell IM, Tompkins S, Lovell AT, Goldstone JC, Moxham J. An in vivo comparison of a catheter mounted pressure transducer system with conventional balloon catheters. Eur Respir J. 1999;13(5):1158-63.
» http://dx.doi.org/10.1034/j.1399-3003.1999.13e36.x -
39Wragg S, Aquilina R, Moran J, Ridding M, Hamnegard C, Fearn T, et al. Comparison of cervical magnetic stimulation and bilateral percutaneous electrical stimulation of the phrenic nerves in normal subjects. Eur Respir J. 1994;7(10):1788-92.
» http://dx.doi.org/10.1183/09031936.94.07101788 -
40Similowski T, Fleury B, Launois S, Cathala HP, Bouche P, Derenne JP. Cervical magnetic stimulation: a new painless method for bilateral phrenic nerve stimulation in conscious humans. J Appl Physiol (1985). 1989;67(4):1311-8.
-
41Man WD, Moxham J, Polkey MI. Magnetic stimulation for the measurement of respiratory and skeletal muscle function. Eur Respir J. 2004;24(5):846-60.
» http://dx.doi.org/10.1183/09031936.04.00029004 -
42Lerolle N, Diehl JL. Ultrasonographic evaluation of diaphragmatic function. Crit Care Med. 2011;39(12):2760-1.
» http://dx.doi.org/10.1097/CCM.0b013e31822a55e9 -
43Houston JG, Fleet M, Cowan MD, McMillan NC. Comparison of ultrasound with fluoroscopy in the assessment of suspected hemidiaphragmatic movement abnormality. Clin Radiol. 1995;50(2):95-8.
» http://dx.doi.org/10.1016/S0009-9260(05)82987-3 -
44Matamis D, Soilemezi E, Tsagourias M, Akoumianaki E, Dimassi S, Boroli F, et al. Sonographic evaluation of the diaphragm in critically ill patients. Technique and clinical applications. Intensive Care Med. 2013;39(5):801-10.
» http://dx.doi.org/10.1007/s00134-013-2823-1 -
45Lerolle N, Guérot E, Dimassi S, Zegdi R, Faisy C, Fagon JY, et al. Ultrasonographic diagnostic criterion for severe diaphragmatic dysfunction after cardiac surgery. Chest. 2009;135(2):401-7.
» http://dx.doi.org/10.1378/chest.08-1531 -
46Gottesman E, McCool FD. Ultrasound evaluation of the paralyzed diaphragm. Am J Respir Crit Care Med. 1997;155(5):1570-4.
» http://dx.doi.org/10.1164/ajrccm.155.5.9154859 -
47Summerhill EM, El-Sameed YA, Glidden TJ, McCool FD. Monitoring recovery from diaphragm paralysis with ultrasound. Chest. 2008;133(3):737-43.
» http://dx.doi.org/10.1378/chest.07-2200 -
48Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ. Two-dimensional ultrasound imaging of the diaphragm: quantitative values in normal subjects. Muscle Nerve. 2013;47(6):884-9.
» http://dx.doi.org/10.1002/mus.23702 -
49Boussuges A, Gole Y, Blanc P. Diaphragmatic motion studied by m-mode ultrasonography: methods, reproducibility, and normal values. Chest. 2009;135(2):391-400.
» http://dx.doi.org/10.1378/chest.08-1541 -
50Testa A, Soldati G, Giannuzzi R, Berardi S, Portale G, Gentiloni Silveri N. Ultrasound M-mode assessment of diaphragmatic kinetics by anterior transverse scanning in healthy subjects. Ultrasound Med Biol. 2011;37(1):44-52.
» http://dx.doi.org/10.1016/j.ultrasmedbio.2010.10.004 -
51Rahn H, Otis A, Fenn WO. The pressure-volume diagram of the thorax and lung. Fed Proc. 1946;5(1 Pt 2):82.
-
52Coelho CM, Carvalho RM, Gouvêa DS, Novo Júnior JM. Comparisons among parameters of maximal respiratory pressures in healthy subjects. J Bras Pneumol. 2012;38(5):605-13.
» http://dx.doi.org/10.1590/S1806-37132012000500010 -
53Irwin RS, Boulet LP, Cloutier MM, Fuller R, Gold PM, Hoffstein V, et al. Managing cough as a defense mechanism and as a symptom. A consensus panel report of the American College of Chest Physicians. Chest. 1998;114(2 Suppl Managing):133S-181S.
-
54Khamiees M, Raju P, DeGirolamo A, Amoateng-Adjepong Y, Manthous CA. Predictors of extubation outcome in patients who have successfully completed a spontaneous breathing trial. Chest. 2001;120(4):1262-70.
» http://dx.doi.org/10.1378/chest.120.4.1262 -
55Man WD, Kyroussis D, Fleming TA, Chetta A, Harraf F, Mustfa N, et al. Cough gastric pressure and maximum expiratory mouth pressure in humans. Am J Respir Crit Care Med. 2003;168(6):714-7.
» http://dx.doi.org/10.1164/rccm.200303-334BC -
56Kyroussis D, Mills GH, Polkey MI, Hamnegard CH, Koulouris N, Green M, et al. Abdominal muscle fatigue after maximal ventilation in humans. J Appl Physiol (1985). 1996;81(4):1477-83.
-
57Kyroussis D, Polkey MI, Mills GH, Hughes PD, Moxham J, Green M. Simulation of cough in man by magnetic stimulation of the thoracic nerve roots. Am J Respir Crit Care Med. 1997;156(5):1696-9.
» http://dx.doi.org/10.1164/ajrccm.156.5.9702008 -
58Suzuki J, Tanaka R, Yan S, Chen R, Macklem PT, Kayser B. Assessment of abdominal muscle contractility, strength, and fatigue. Am J Respir Crit Care Med. 1999;159(4 Pt 1):1052-60.
» http://dx.doi.org/10.1164/ajrccm.159.4.9803025 -
59Merletti R, Botter A, Troiano A, Merlo E, Minetto MA. Technology and instrumentation for detection and conditioning of the surface electromyographic signal: state of the art. Clin Biomech (Bristol, Avon). 2009;24(2):122-34.
» http://dx.doi.org/10.1016/j.clinbiomech.2008.08.006 -
60Daube JR, Rubin DI. Needle electromyography. Muscle Nerve. 2009;39(2):244-70.
» http://dx.doi.org/10.1002/mus.21180 -
61Rubin DI. Needle electromyography: basic concepts and patterns of abnormalities. Neurol Clin. 2012;30(2):429-56.
» http://dx.doi.org/10.1016/j.ncl.2011.12.009 -
62Luo YM, Moxham J, Polkey MI. Diaphragm electromyography using an oesophageal catheter: current concepts. Clin Sci (Lond). 2008;115(8):233-44.
» http://dx.doi.org/10.1042/CS20070348 -
63Luo YM, Polkey MI, Johnson LC, Lyall RA, Harris ML, Green M, et al. Diaphragm EMG measured by cervical magnetic and electrical phrenic nerve stimulation. J Appl Physiol (1985). 1998;85(6):2089-99.
-
64Criswell E. Cram's Introduction to Surface Electromyography. 2nd ed. Burlington (MA): Jones & Bartlett Learning; 2010.
-
*Study carried out in the Department of Pulmonology, Instituto do Coração - Incor, Heart Institute - University of São Paulo School of Medicine Hospital das Clínicas, São Paulo, Brazil.
-
Financial support: None.
Publication Dates
-
Publication in this collection
Mar-Apr 2015
History
-
Received
27 Oct 2014 -
Accepted
05 Feb 2015