American Journal of Respiratory and Critical Care Medicine

Maximal expiratory mouth pressure is a well established test that is used to assess expiratory muscle strength. However, low values are difficult to interpret, as they may result from technical difficulties in performing the test, particularly in patients with facial muscle weakness or bulbar dysfunction. We hypothesized that measuring the gastric pressure during a cough, a natural maneuver recruiting the expiratory muscles, might prove to be a useful additional test in the assessment of expiratory muscle function. Mouth expiratory and cough gastric pressures were measured in 99 healthy volunteers to obtain normal values and in 293 patients referred for respiratory muscle assessment to compare the two measurements. Between-occasion within-subject coefficient of variation, assessed in 24 healthy volunteers, was 10.3% for mouth pressure and 6.9% for cough. Mean ± SD cough gastric pressure for normal males was 214.4 ± 42.2 and 165.1 ± 34.8 cm H2O for females. In 171 patients deemed weak by a low mouth expiratory pressure, 42% had a normal cough gastric pressure. In 105 patients deemed weak by a low cough gastric pressure, 5.7% had a normal expiratory mouth pressure. Low maximal expiratory mouth pressures do not always indicate expiratory muscle weakness. Cough gastric pressure provides a useful complementary test for the assessment of expiratory muscle strength.

The measurement of expiratory muscle strength is of clinical importance, as weakness impairs cough (1), which is considered to protect against chest infection, a serious cause of morbidity and mortality in patients with respiratory and neuromuscular disease. Maximal static expiratory mouth pressure (PeMAX) is the only commonly used test for the assessment of expiratory muscle strength (2, 3). PeMAX is a volitional, noninvasive maneuver that when high values are found excludes expiratory muscle weakness (4). In a proportion of patients, particularly those with facial muscle weakness or bulbar dysfunction, technical difficulties may limit the usefulness of PeMAX. Low values are difficult to interpret, as they may result from poor effort, difficulties with the maneuver, or true expiratory muscle weakness.

As the main expiratory muscles (the abdominal muscles) are used in cough, measurement of cough esophageal and abdominal pressures has been used previously in small numbers of patients to assess expiratory muscle strength (58). Progressive curarization in normal subjects leads to similar declines in cough pressures and PeMAX (5), suggesting that cough could be a reliable reflection of expiratory muscle strength. In the assessment of inspiratory muscle strength, the maximum sniff has proved to be a useful complementary test to maximal static inspiratory pressures. A natural maneuver, it is reproducible and easy for patients to perform (9). Cough, like a sniff, is a natural maneuver, and we hypothesized that cough gastric pressure (cough Pga) might prove to be a useful additional test of expiratory muscle strength.

To test this hypothesis, we measured cough Pga, as well as PeMAX, in 99 normal volunteers to establish sex-specific normal values. We then measured expiratory muscle strength in 293 patients referred to our laboratory for assessment of respiratory muscle function to determine the relationship between cough Pga and PeMAX. Some of the normal subject data have previously been presented in abstract form (10).

PeMAX and cough Pga were measured in 99 healthy volunteers (62 males) and 293 patients (188 males) referred to our laboratory for assessment of respiratory muscle function. In 24 healthy volunteers, repeated measurements were made on two to three occasions to determine between-occasion within-subject reproducibility. All subjects gave informed consent, and the local ethics committee approved the study.

Measurement of PEMAX

PeMAX was measured using a flanged mouthpiece attached to a metal tube with a three-way tap that allowed the airway to be closed (11). The system contained a small leak to reduce the use of the buccal muscles during the expiratory maneuver. Proximal to the three-way tap, a 70-cm fine polyethylene catheter connected the tube to a Validyne MP45-1 differential pressure transducer (Validyne Corp., Northridge, CA) linear over the range of 0–200 cm H2O. Subjects were seated and asked to make a maximum expiratory maneuver (Valsalva maneuver) at total lung capacity and to maintain the expiratory pressure for at least 1.5 seconds. Consecutive efforts were made at 30-second intervals until no further increase in PeMAX occurred, which was usually achieved after five to six efforts.

Measurement of Cough Pga

Gastric pressures were measured using a balloon catheter (Ackrad Laboratories, Cranford, NJ) passed per nasally, after local anesthesia of the nasal mucosa and pharynx. The tip of the balloon was placed at 70 cm from the nostril, and correct placement in the stomach was confirmed by a positive deflection during a sniff maneuver or gentle compression of the abdomen. The catheter was connected to a Validyne MP45-1 differential pressure transducer linear over the range of 0–400 cm H2O, and 3 ml of air were used to inflate the balloon. Seated subjects were asked to perform maximal single coughs at 30-second intervals until no further increase of cough Pga was observed. This was usually achieved after three to six efforts. Although no specific instructions were given, subjects reported that coughs were usually made near to total lung capacity. Both PeMAX and cough Pga maneuvers were displayed on a computer screen to provide visual feedback, and an experienced operator was present to provide encouragement.

All signals were digitized via an NB-MIO-16 analog-digital converter (National Instruments, Austin, TX) and acquired on a Macintosh PowerMac 7600 computer (Apple Inc., Cupertino, CA) running LabVIEW 4 software (National Instruments). The sampling rate was 100 Hz.

Data and Statistical Analysis

For PeMAX, the computed 1-second averaged sustained pressure was recorded. For cough Pga, the peak value was recorded, with Pga at resting end expiration before cough used as the zero reference point. The lower limits of PeMAX and cough Pga were set at 1.96 SDs below the mean values obtained in our population of healthy volunteers (i.e., the 95% confidence interval). Statistical analysis was performed on SPSS 10.1 for Windows (SPSS, Chicago, IL). Linear regression was used to assess the relationship between PeMAX and cough Pga, whereas the coefficient of variation was used to determine between-occasion within-subject reproducibility.

Anthropometric data of the normal volunteers and patients are presented in Table E1 of the online supplement. In the normal volunteers, mean PeMAX ± SD for males was 128.9 ± 25.8 cm H2O and for females was 95.6 ± 17.6 cm H2O, giving sex-specific lower limits of normal of 78.3 and 61.0 cm H2O, respectively. Sex had a significant effect on cough Pga (mean cough Pga ± SD for males was 214.4 ± 42.2 cm H2O and for females was 165.1 ± 34.8 cm H2O, 95% confidence intervals, −65.7, −33.2; p < 0.0001), giving sex-specific lower limits of normal of 131.7 and 96.9 cm H2O, respectively. There was no linear relationship between age and cough Pga (r2=0.007, p = 0.40). Between-occasion within-subject coefficient of variation was 10.3% for PeMAX and 6.9% for cough Pga. There was a significant correlation between PeMAX and cough Pga (r2 = 0.48, p < 0.001). Healthy volunteer and patient data are illustrated in Figure 1

, and the agreement between measures was assessed in a Bland-Altman plot (Figure 2) .

Two hundred ninety-three patients were assessed in our laboratory, and there were no side effects associated with the insertion of the balloon catheter into the stomach via the nose. Using the healthy subjects' sex-specific lower 95% confidence intervals as cutoffs for “normal” values, there was close agreement between the two tests in excluding expiratory muscle weakness (Table 1)

TABLE 1. A 2 × 2 table dividing referred male and female patients according to normal and low cough gastric pressure and maximal static expiratory mouth pressure values

Normal Cough Pga

Low Cough Pga
Normal PEMAX825
Low PEMAX3566
Normal PEMAX341

Definition of abbreviations: cough Pga = cough gastric pressure; PEMAX = maximal static expiratory mouth pressure.

. In 122 patients with a PeMAX higher than the lower 95% confidence interval (i.e., “normal PeMAX”), more than 95% also had a cough Pga above the lower 95% confidence interval (“normal cough Pga”). However, in 171 patients deemed weak by a low PeMAX value (i.e., below the lower 95% confidence interval), 72 of these patients (42%) had a normal cough Pga, suggesting that there is a high “false-positive” rate in using PeMAX to detect expiratory muscle weakness. Among these patients only 36% had a diagnosis of neuromuscular disorder (amyotrophic lateral sclerosis, myotonic dystrophy, or inflammatory myositis) in which expiratory muscle weakness is a recognized feature, whereas the remainder had diagnoses of obstructive airways disease (n = 14), interstitial lung disease (n = 7), neuralgic amyotrophy (n = 6), hyperventilation (n = 5), obstructive sleep apnea (n = 2), and undiagnosed (n = 8) (Table 2)

TABLE 2. Final diagnoses of referred patients


Amyotrophic lateral sclerosis4324
Myotonic dystrophies133
Myopathies (including mitochondrial)81
Neuromuscular junction disorders32
Inflammatory myositis25
Neuralgic amyotrophy259
Idiopathic diaphragm paralysis173
Mediastinal lesion41
Postcardiothoracic surgery116
Postpolio syndrome43
Multiple sclerosis21
Spinal cord trauma31
Myelopathy (including HTLV-1)32
Connective tissue disease212
Obstructive airways disease229
Interstitial lung disease45
Obstructive sleep apnea21
Hyperventilation syndrome27

Definition of abbreviation: HTLV-1 = human T-cell leukemia virus type 1.

. In comparison, in 105 patients with a low cough Pga, only six patients (5.7%) had a normal PeMAX, suggesting that cough Pga has a low “false-positive” rate (see Table 1).

Gastric pressures during PeMAX were available in 43 of the 72 patients with a “false-positive” PeMAX; although there was an increase compared with corresponding mouth pressures (95% confidence intervals, 1.42 to 10.04 cm H2O, p = 0.01), the mean absolute difference in pressures was clinically small (5.73 cm H2O). This suggests that the use of the more natural maneuver of a cough rather than the measurement of gastric pressure per se explains the additional positive predictive value of cough Pga over PeMAX.

This study describes the measurement of cough Pga and establishes normal values. The study shows that cough Pga may provide useful complementary information in the assessment of expiratory muscle strength, particularly in patients with a low PeMAX measurement. Before enlarging on these points, it is appropriate to discuss the method.

Advantages and Limitations of Cough Pga

Measurement of abdominal pressure during cough offers an alternative to static mouth pressure as the principal expiratory muscles, the abdominal muscles, are also used in cough (1, 12). By measuring the gastric pressure response rather than mouth pressures, cough Pga may avoid the problems of leakage around mouthpieces in some patients with facial weakness. However, the main advantage is that as a natural dynamic maneuver, cough may be technically easier to perform than PeMAX. This is supported by the finding that measurement of the gastric pressure during PeMAX did not markedly improve the maximum values obtained with the static maneuver. However, although cough Pga is a good expression of abdominal muscle strength, it does not include the contribution, albeit small, of the expiratory rib cage muscles (such as the internal nonparasternal intercostals), which in contrast is reflected by PeMAX and the expiratory esophageal pressure.

A possible limitation of this study is that lung volumes were not standardized during the cough maneuver. Increasing lung volume may alter abdominal muscle length and increase elastic recoil pressure. However, a previous study from our laboratory suggested that lung volume had a very small effect on expiratory muscle strength assessed with nonvolitional methods (1). Furthermore, it was observed that the majority of patients coughed at or near TLC. Additional studies are required to quantify the effects of lung volume upon cough Pga, but it is unlikely that lung volume will have a major effect on the clinical utility of the test.

The principal disadvantage of the cough Pga measurement is that it requires the insertion of a balloon catheter via the nose. Although there are some hypothetical risks to the use of topical anesthesia, patients and operators usually prefer it, and the relief of local discomfort outweighs the minimal risks. The amounts of topical anesthesia used are considerably less than the maximum dose recommended by the British Thoracic Society in their guidelines on flexible diagnostic bronchoscopy (13) and are highly unlikely to lead to toxic blood levels (14). We have performed the measurement of esophageal, gastric, and transdiaphragmatic pressures for over 20 years, and there has never been an adverse event secondary to local anesthetic use. An obvious question is whether the small amounts of local anesthesia used can impair maximum voluntary cough, as topically (and intravenously) administered local anesthetic agents are widely used to inhibit cough. Although lignocaine has been shown to suppress mechanically induced (15) as well as ammonia and capsacin-induced cough (16), it has not been shown to suppress maximum voluntary cough (17).

Clinical Evaluation of Expiratory Muscle Strength

Quantification of expiratory muscle strength is of clinical importance, particularly in patients with neuromuscular disease. Weakness may predispose to chest infections, impair cough, and increase mortality. We have previously demonstrated that maximum cough flow is related to twitch gastric pressures, a nonvolitional measure of expiratory muscle strength (1). Bach and Saporito have shown that a peak cough flow greater than 160 L/min predicts successful extubation and decannulation in patients with neuromuscular respiratory failure (18), whereas Chaudri and colleagues have demonstrated an association between the absence of cough spikes and increased mortality in amyotrophic lateral sclerosis (19).

PeMAX is a well established, simple noninvasive test of expiratory muscle strength, and the values recorded in our normal population were similar to previously reported studies using a flanged mouthpiece (3). A high value excludes severe weakness of the expiratory muscles, but difficulties arise when interpreting low values. As a volitional test, there are the usual limitations of understanding, cooperation, and motivation of subjects. Underestimation can also occur if there is a leak around the mouthpiece (a particular problem in patients with facial muscle weakness). In bulbar patients, a nonfunctioning glottis can cause an uncomfortable choking sensation, making mouth pressure measurements difficult (12). Some of these difficulties can be overcome by using a nonvolitional technique to assess expiratory muscle strength. Our laboratory has previously described magnetic stimulation over the thoracic vertebrae and the recording of twitch gastric pressures (1, 20); however, normal data are limited, and interpretation is difficult because of submaximal activation of the abdominal muscles.

In this study, we have demonstrated that there is a linear relationship between cough Pga and PeMAX. The range of normal values and the between-occasion within-subject reproducibility are similar between the two tests. This study also shows that 42% of patients considered to have expiratory muscle weakness from measurement of PeMAX have a normal cough Pga. Hence, cough Pga may be useful in excluding expiratory muscle weakness in patients found to have a low PeMAX. If expiratory muscle weakness is defined as the presence of a low PeMAX and low cough Pga, PeMAX would have a positive predictive value of 58% and cough Pga a positive predictive value of 94%.

In summary, PeMAX is the conventional test for assessing expiratory muscle strength. However, caution needs to be exercised when interpreting low values, as a low PeMAX may not always indicate expiratory muscle weakness. Cough gastric pressure provides a useful complementary test, particularly in patients who have difficulty performing the PeMAX maneuver.

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Correspondence and requests for reprints should be addressed to William Man, BSc (Hon), MBBS (Hon), MRCP, Respiratory Muscle Laboratory, Department of Respiratory Medicine, King's College Hospital, Bessemer Road, London SE5 9PJ, UK. E-mail:


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