Respiratory Muscle Testing.pdf

American Thoracic Society/European Respiratory Society

ATS/ERS Statement on Respiratory Muscle Testing

HIS

OINT

TATEMENT

THE

MERICAN

HORACIC

OCIETY

(ATS),

AND

THE

UROPEAN

ESPIRATORY

OCIETY

(ERS)

WAS

ADOPTED

THE

ATS B

OARD

IRECTORS

, M

ARCH

2001

AND

THE

ERS E

XECUTIVE

OMMITTEE

, J

UNE

2001

Introduction

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 520

Endurance of the Diaphragm . . . . . . . . . . . . . . . . . . . . . . 568

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 569

1. Tests of Overall Respiratory Function

G. John Gibson, William Whitelaw, Nikolaos Siafakas

5. Assessment of Respiratory Muscle Fatigue

Gerald S. Supinski, Jean Will Fitting, François Bellemare

Static Lung Volumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521

Dynamic Spirometry and Maximum Flow . . . . . . . . . . . 521

Maximum Voluntary Ventilation . . . . . . . . . . . . . . . . . . . 522

Arterial Blood Gases: Awake . . . . . . . . . . . . . . . . . . . . . . 522

Measurements during Sleep . . . . . . . . . . . . . . . . . . . . . . . 523

Tests of Respiratory Control . . . . . . . . . . . . . . . . . . . . . . . 524

Carbon Monoxide Transfer . . . . . . . . . . . . . . . . . . . . . . . . 525

Exercise Testing . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 526

Types of Fatigue . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 571

Tests of Respiratory Muscle Fatigue . . . . . . . . . . . . . . . . 572

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 578

Stephen H. Loring, Andre de Troyer, Alex E. Grassino

Pressures in the Chest Wall . . . . . . . . . . . . . . . . . . . . . . . . 580

Assessment of the Properties of the Relaxed

Human Chest Wall: Rahn Diagram . . . . . . . . . . . . . . . 580

Assessment of the Function of the Active

Chest Wall: Campbell Diagram . . . . . . . . . . . . . . . . . . . 581

Estimation of Ventilation Based on Chest

Wall Motion: Konno-Mead Diagram . . . . . . . . . . . . . . 582

Devices Used to Monitor Breathing:

Pneumograph, Magnetometer, and

Respiratory Inductive Plethysmograph . . . . . . . . . . . . 583

Optical Devices Used to Measure Chest

Wall Motion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 584

Inferring Respiratory Muscle Contribution to

Breathing from Chest Wall Motion . . . . . . . . . . . . . . . 584

Inferring Respiratory Muscle Contribution to

Breathing from the Esophageal–Gastric

Pressure Relationship: Macklem Diagram . . . . . . . . . . 585

Inferring Respiratory Muscle Contribution to

Breathing from Pressure–Volume Relationships . . . . 585

Inferring Diaphragm Activation and

Electromechanical Effectiveness from EMG . . . . . . . 585

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 586

Malcolm Green, Jeremy Road, Gary C. Sieck, Thomas

Similowski

Pressure Measurements . . . . . . . . . . . . . . . . . . . . . . . . . . . 528

Devices for Measuring Pressures . . . . . . . . . . . . . . . . . . . 528

Techniques for Pressure Measurement . . . . . . . . . . . . . . 530

Volitional Tests of Respiratory Muscle Strength . . . . . . 531

Pressures Obtained via Phrenic Nerve Stimulation . . . . 535

Abdominal Muscle Stimulation . . . . . . . . . . . . . . . . . . . . 542

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 542

3. Electrophysiologic Techniques for the Assessment of

Respiratory Muscle Function

Thomas K. Aldrich, Christer Sinderby, David K. McKenzie,

Marc Estenne, Simon C. Gandevia

Electromyography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 548

Stimulation Tests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 554

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 556

Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 557

7. Imaging Respiratory Muscle Function

4. Tests of Respiratory Muscle Endurance

Neil B. Pride, Joseph R. Rodarte

Thomas Clanton, Peter M. Calverly, Bartolome R. Celli

Transmission Radiography . . . . . . . . . . . . . . . . . . . . . . . . . 588

Ultrasound . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 589

Volumetric Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 591

Nuclear Medicine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 591

Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 591

Measures of Respiratory Muscle Activity

Used in Endurance Testing . . . . . . . . . . . . . . . . . . . . . . 559

Ventilatory Endurance Tests . . . . . . . . . . . . . . . . . . . . . . 562

Endurance to External Loads . . . . . . . . . . . . . . . . . . . . . . 564

Am J Respir Crit Care Med Vol 166. pp 518–624, 2002

DOI: 10.1164/rccm.166.4.518

Internet address: www.atsjournals.org

6. Assessment of Chest Wall Function

2. Tests of Respiratory Muscle Strength

American Thoracic Society/European Respiratory Society

519

8. Tests of Upper Airway Function

9. Tests of Respiratory Muscle Function in Children

Neil J. Douglas, Samuel T. Kuna

Claude Gaultier, Julian Allen, Sandra England

Electromyography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 593

Upper Airway Resistance . . . . . . . . . . . . . . . . . . . . . . . . . 594

Indirect Laryngoscopy . . . . . . . . . . . . . . . . . . . . . . . . . . . . 596

Fiberoptic Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 596

Computed Tomographic Scanning . . . . . . . . . . . . . . . . . . 596

Magnetic Resonance Imaging . . . . . . . . . . . . . . . . . . . . . . 597

Acoustic Reflection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 597

Flow–Volume Loops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 597

Polysomnography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 597

Muscle Biopsy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598

Strength, Fatigue, and Endurance of Upper

Airway Muscles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598

Site of Pharyngeal Airway Closure during Sleep . . . . . . 598

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 598

Physiology of the Developing Respiratory Pump . . . . . . 601

Tests of Respiratory Function . . . . . . . . . . . . . . . . . . . . . . 601

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 607

10. Assessment of Respiratory Muscle Function in the

Intensive Care Unit

Martin J. Tobin, Laurent Brochard, Andrea Rossi

Breathing Pattern . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 610

Lung Volumes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 611

Pressure Measurements . . . . . . . . . . . . . . . . . . . . . . . . . . . 611

Prediction of Weaning . . . . . . . . . . . . . . . . . . . . . . . . . . . . 617

Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 619

Introduction

Over the last 25 years, great efforts have been made to de-

velop techniques to assess respiratory muscle function. Re-

search output in this area has progressively increased, with the

number of peer reviewed articles published on respiratory mus-

cle function having increased remarkably during the 1995–2000

period compared with 1980–1985.

This official joint statement represents the work of an ex-

pert ATS/ERS committee, which reviewed the merits of cur-

rently known techniques available to evaluate respiratory mus-

cle function. The statement consists of 10 sections, each addressing

a major aspect of muscle function or a particular field of appli-

cation. Each section addresses the rationale for the techniques,

their scientific basis, the equipment required, and, when perti-

nent, provides values obtained in healthy subjects or in pa-

tients. Some of the techniques reviewed in this statement have

thus far been used primarily in clinical research and their full

potential has not yet been established; however, they are men-

tioned for the purpose of stimulating their further development.

Through continued efforts in the area of respiratory muscle

testing, it is anticipated that there will be further enhancement

of diagnostic and treatment capabilities in specialties such as

intensive care, sleep medicine, pediatrics, neurology, rehab-

ilitation, sports medicine, speech therapy, and respiratory

medicine.

Am J Respir Crit Care Med Vol 165. pp 520–520, 2002

DOI: 10.1164/rccm.2102104

Internet address: www.atsjournals.org

1. Tests of Overall Respiratory Function

Routine measurements of respiratory function, that is, vol-

umes, flows, and indices of gas exchange, are nonspecific in re-

lation to diagnosis but give useful indirect information about

respiratory muscle performance. On occasion, the presence of

respiratory muscle dysfunction is first suspected from the pat-

tern of conventional respiratory function tests. More fre-

quently, they are of use in assessing the severity, functional

consequences, and progress of patients with recognized mus-

cle weakness.

Disadvantages

VC has poor specificity for the diagnosis of respiratory muscle

weakness. In mild weakness, it is generally less sensitive to

changes than are maximum pressures (13).

Applications

Serial measurements of VC should be routine in monitoring

progress of patients with acute and chronic respiratory muscle

weakness.

Measurement of postural change of VC gives a simple in-

dex of weakness of the diaphragm relative to the other inspira-

tory muscles.

STATIC LUNG VOLUMES

Rationale and Scientific Basis

The most frequently noted abnormality of lung volumes in pa-

tients with respiratory muscle weakness is a reduction in vital

capacity (VC). The pattern of abnormality of other subdivi-

sions of lung volume is less consistent. Residual volume (RV)

is usually normal or increased, the latter particularly with

marked expiratory weakness (1). Consequently, total lung ca-

pacity (TLC) is less markedly reduced than VC, and the RV/

TLC and FRC/TLC ratios are often increased without neces-

sarily implying airway obstruction.

The VC is limited by weakness of both the inspiratory mus-

cles, preventing full inflation, and expiratory muscles, inhibit-

ing full expiration. In addition to the direct effect of loss of

muscle force, reductions in compliance of both the lungs (2)

and chest wall (3) also contribute to the reduction of VC in pa-

tients with chronic respiratory muscle weakness. In severe

weakness, the TLC and VC relate more closely to lung com-

pliance than to the distending force (4, 5) (Figure 1). The

mechanism of reduced lung compliance is unclear. Contrary to

earlier suggestions, it is probably not simply due to wide-

spread microatelectasis (6). Static lung volumes may also be

affected in some patients by coexistent lung or airway disease.

Vital capacity, thus, reflects the combined effect of weakness

and the static mechanical load on the respiratory muscles.

In mild respiratory muscle weakness, VC is less sensitive

than maximum respiratory pressures. However, the curvilin-

ear relation between VC and maximum inspiratory pressure

(5) (Figure 2) implies that, in more advanced disease, marked

reductions in VC can occur with relatively small changes in

maximum pressures.

In patients with isolated or disproportionate bilateral dia-

phragmatic weakness or paralysis, the VC shows a marked fall

in the supine compared with the erect posture because of the

action of gravitational forces on the abdominal contents. In

some patients, this postural fall may exceed 50%. In most nor-

mal subjects, VC in the supine position is 5–10% less than

when upright (7) and a fall of 30% or more is generally associ-

ated with severe diaphragmatic weakness (8).

DYNAMIC SPIROMETRY AND MAXIMUM FLOW

Rationale and Scientific Basis

Airway resistance is normal in uncomplicated respiratory

muscle weakness (14). Airway function may appear to be su-

pernormal when volume-corrected indices such as FEV

/VC

or specific airway conductance are used (2).

The maximum expiratory and maximum inspiratory flow–

volume curves characteristically show a reduction in those flows

that are most effort dependent, that is, maximum expiratory

flow at large lung volumes (including peak expiratory flow) and

maximum inspiratory flow at all lung volumes (2, 5) (Figure 3).

The descending limb of the maximum expiratory flow–volume

curve may suggest supernormal expiratory flow when this is re-

lated to absolute volume (2, 3). With severe expiratory weak-

ness, an abrupt fall in maximum expiratory flow is seen imme-

diately before RV is reached (1). In health the FEV

is usually

less than the forced inspiratory volume in 1 second. Reversal of

this ratio is seen with upper (extrathoracic) airway obstruction,

as well as in respiratory muscle weakness, and may give a

pointer to these diagnoses during routine testing.

The effect of coughing can be visualized on the maximum ex-

piratory flow–volume curve in healthy subjects as a transient flow

exceeding the maximum achieved during forced expiration. The

absence of such supramaximal flow transients during coughing

presumably results in impaired clearance of airway secretions

and is associated with more severe expiratory muscle weakness

(15). Even with quadriplegia, however, some patients can gener-

ate an active positive pleural pressure in expiration (16). This can

allow them to achieve the pressure required for flow limitation

may still be reliable as

an index of airway function. Impaired maximal flow in some

neuromuscular diseases may also reflect poor coordination of

the respiratory muscles rather than decreased force per se.

Oscillations of maximum expiratory and/or inspiratory

flow—the so-called sawtooth appearance—are seen particu-

larly when the upper airway muscles are weak and in patients

with extrapyramidal disorders (17) (Figure 4).

Methodology and Equipment

Recommendations and requirements for the measurement of

VC and other lung volumes are covered in detail elsewhere (9, 10).

Methodology and Equipment

Advantages

Recommendations and requirements for maximum flow–vol-

ume curves are covered in detail elsewhere (9, 10).

VC has excellent standardization, high reproducibility and well-

established reference values. It is easily performed, widely avail-

able, and economical. It is quite sensitive for assessing progress

in moderate to severe respiratory muscle weakness. The rate of

decline has been shown to predict survival in both amyotrophic

lateral sclerosis (11) and Duchenne muscular dystrophy (12).

Advantages

Maximum flow–volume curves are easily performed, widely

available, and economical. Peak expiratory flow can be ob-

tained with simple portable devices.

through most of expiration so that FEV

522

AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 166 2002

Figure 1. Relation between static

lung compliance and total lung

capacity in 25 patients with

chronic respiratory muscle weak-

ness of varying severity. Dashed

line is regression line. Reprinted

by permission from Reference 5.

Disadvantages

Intersubject variability is greater than for VC. Reference val-

ues for

V ·

Figure 3. Schematic maximum expiratory and inspiratory flow–vol-

ume curves in a patient with severe respiratory muscle weakness ( solid

line ) compared with predicted ( dotted line ). Volume is expressed in ab-

solute terms (i.e., percent predicted). Note marked reductions in FVC,

E max at higher volumes, and I max at all volumes. Note also the

blunted contour of the expiratory curve and the abrupt cessation of

E max at RV. In the midvolume range, E max exceeds that predicted

for the absolute lung volume.

Applications

Visual inspection may suggest the likelihood of weakness.

The sawtooth appearance in an appropriate context may

suggest weakness or dyscoordination of upper airway muscles.

However, this appearance is nonspecific and is seen also in

some subjects with obstructive sleep apnea, nonapneic snor-

ing, and thermal injury of the upper airway.

ARTERIAL BLOOD GASES: AWAKE

Rationale and Scientific Basis

MAXIMUM VOLUNTARY VENTILATION

In chronic muscle weakness, even when quite severe, Pa

and

difference are usually only mildly ab-

normal (2, 21). In acute muscle weakness, Pa

Rationale and Scientific Basis

O 2

may be more

markedly reduced, but the picture may be complicated by

atelectasis or respiratory infection (22).

With mild weakness, Pa

The maximum voluntary ventilation was formerly recommended

as a more specific test for muscle weakness than volume mea-

surements but, in practice, the proportionate reduction is usu-

ally similar to that of VC (18, 19). Disproportionate reductions

may be seen in Parkinson’s disease (20), in which the ability to

perform frequent alternating movements is impaired.

is usually less than normal (19,

22), implying alveolar hyperventilation. In the absence of pri-

mary pulmonary disease, daytime hypercapnia is unlikely un-

less respiratory muscle strength is reduced to

CO 2

40% of pre-

50% of predicted (19) (Figures

5 and 6). Elevation of venous bicarbonate concentration occa-

sionally gives an important clue to otherwise unsuspected hy-

percapnia. Patients with muscle weakness are less able than

normal subjects to compensate for minor changes in respira-

tory function. If hypercapnia is established or incipient, even

minor infections may cause a further rise in Pa

Methodology and Equipment

Recommendations and requirements are covered elsewhere (10).

Advantages

No advantages are perceived in most situations.

Disadvantages

, as also may

injudicious use of sedative drugs or uncontrolled oxygen.

CO 2

The test depends on motivation and is tiring for the subject.

Applications

Advantages

Maximum voluntary ventilation is not generally recommended

for patients with known or suspected respiratory muscle weak-

ness but may be helpful in the assessment and monitoring of

patients with extrapyramidal disorders.

Arterial blood gases assess the major functional consequence

of respiratory muscle weakness. In patients with Duchenne

muscular dystrophy, hypercapnia has been shown to predict

shorter survival (12).

Figure 2. Curvilinear relation of

maximum static inspiratory pres-

sure (inspiratory muscle strength)

to vital capacity in 25 patients with

chronic weakness of varying sever-

ity. Dashed line and statistics relate

to logarithmic regression. Solid line

represents relationship calculated

from a standard maximal static pres-

sure–volume diagram assuming nor-

mal elastic properties of the respi-

ratory system. The greater than

expected reduction in VC is due

to reduced compliance of the lungs

and chest wall. Reprinted by per-

mission from Reference 5.

Figure 4. Maximum expiratory and

inspiratory flow–volume curves, show-

ing “sawtooth” oscillations of flow.

max at standard percentages of FVC may present

problems of interpretation.

the alveolar–arterial P

dicted and VC is reduced to

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