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* From the Departments of Accident & Emergency Medicine (Dr. Stell) and Respiratory Medicine (Drs. Polkey and Moxham), King’s College Hospital, London, UK; the Department of Respiratory Medicine (Dr. Rees), Guy’s Hospital, London, UK; and the Department of Respiratory Medicine (Dr. Green), The Royal Brompton Hospital, London, UK.
Correspondence to: Ian M. Stell, MBBS, Accident & Emergency Department, Bromley Hospital, Cromwell Avenue, Bromley, Kent, BR2 9AJ UK; e-mail ian.stell@bromleyh_tr.sthames.nhs.uk
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Abstract |
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Design: Descriptive study.
Setting: Emergency departments of two inner-city hospitals.
Patients: Fifty-one patients with acute asthma, and 45 patients without respiratory disease who served as control subjects.
Measurements and results: Maximum inspiratory pressure-generating capacity was measured soon after presentation by the sniff nasal inspiratory pressure (SNIP) method. The mean (SD) SNIP was 110 cm H2O (23 cm H2O) in men with asthma (mean for control subjects, 126 cm H2O [25 cm H2O]; p < 0.05) and 80 cm H2O [24 cm H2O] in women with asthma (mean for control subjects, 105 cm H2O (26 cm H2O); p < 0.01). In a second study of simultaneous SNIP and intrathoracic pressure measurements in a group of patients with acute asthma (n = 10) and control subjects (n = 11), the effect of airways obstruction on SNIP was assessed. The measurement of sniff esophageal pressure was more negative than SNIP by approximately 16% in asthmatic patients and by 4% in control subjects. Taking account of the likely effect of airways obstruction on SNIP, the reduction in inspiratory pressure-generating capacity that was observed in these patients with moderately severe acute asthma was minor and was consistent with the modest hyperinflation observed.
Conclusions: This study did not find evidence of inspiratory muscle weakness or fatigue in patients with moderately severe acute asthma presenting to the emergency department.
Key Words: asthma • respiratory insufficiency • respiratory muscles • muscle fatigue
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSummaryReferences |
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Inspiratory muscle pressure generation in patients with acute asthma may be compromised both by hyperinflation and, potentially, by inspiratory muscle fatigue. The published work1 investigating the issue of fatigue in patients with acute asthma was hampered by problems with the reproducibility of the maximal inspiratory pressure (PImax) maneuver in these ill patients, although it did not find evidence of a reduction in inspiratory muscle strength.
This suggested to us that inspiratory pressure generation in patients with acute asthma warranted further investigation. In the present study, we used the new technique of sniff nasal inspiratory pressure (SNIP) to compare inspiratory pressure generation in patients presenting with asthma to an emergency department with that in a matched group of emergency department patients who did not have asthma. A further study was performed to assess how accurately intrathoracic negative pressures generated during sniffs were reflected in the SNIP measurement. In order to assess the significance of the remaining difference in pressure-generating capacity between the asthma patients and the control subjects, an adjustment for the difference in lung volumes is suggested in the "Discussion" section.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSummaryReferences |
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Equipment
SNIP was recorded using a hand-held pressure meter that was
modified by the manufacturer from a PImax meter (Precision
Medical; Leeds, UK). This device (the "SNIP meter") is triggered by
a fall in pressure below baseline, after which it samples pressure
continuously at a frequency of 100 Hz. Once a maximum negative pressure
is reached and the pressure starts to rise again, the device ceases
recording and displays digitally the maximum negative pressure reached
(ie, the peak negative pressure).
The baseline zero of the device is automatically set to prevailing atmospheric pressure. However, the baseline can be set to other pressures if required (eg, using end-expiratory esophageal pressure as the baseline when recording intrathoracic pressures). This is achieved by resetting the zero point while the pressure transducer is exposed to the new baseline pressure. Details of the SNIP meter have been described previously.2
For SNIP recordings, a 40-cm length of polyethylene tubing of 1-mm internal diameter was attached to the transducer. The other end of the tubing was inserted into the base of a small cone. These cones, which were designed to occlude one nostril, were hand-made from activated polysiloxanone putty and included a narrow central lumen that was made to fit closely around the tubing, ending at the apex of the cone. For esophageal pressure recordings, the SNIP meter transducer was connected to a balloon catheter. The balloon catheters consisted of 10-cm thin latex balloons, a wall thickness of approximately 0.085 mm, and a balloon circumference of 2 cm (deflated), and were mounted on 110-cm-long polyethylene catheters of 1.0-mm internal diameter (Morgan Medical; Rainham, Kent, UK).
Two identical SNIP meters (designated A and B) were used in the study. They were validated by comparison with a standard laboratory pressure transducer and by comparison with each other. In the comparison with a standard laboratory pressure transducer, in six healthy subjects simultaneous pressure recordings were made from two identical balloon catheters both positioned in the mid-esophagus, 40 cm from the nares, and were filled with 0.5 mL air. In each subject, one balloon was connected to SNIP meter B and one was connected to the laboratory pressure transducer (Precision Medical; Leeds UK), which had an operating range of + 300 to -300 cm H2O and had been calibrated with a water manometer. The subjects performed two series of 10 sniffs of varying strengths, with the baseline of SNIP meter B being reset before each series. The two SNIP meters were compared to each other by connecting the transducers of both of them to the same catheter and recording the simultaneous readings from a series of sniffs of varying strengths in one subject.
Spirometry
Peak expiratory flow rates (PEFRs) were recorded with a Wright
peak flowmeter (Ferraris Medical, Enfield, London, UK), calibrated at
the start of the study by the manufacturer. FEV1
and FVC were recorded with a hand-held spirometer (Micromedical;
Rochester, Kent, UK), the calibration of which was checked with a 1-L
gas syringe.
First Study
Subjects:
Patients in the emergency departments of two
London hospitals who had received diagnoses of acute asthma and were
between the ages of 15 and 60 years were invited to participate.
Patients likely to be eligible were identified by the investigators
from their clinical features at presentation. This recruitment was made
without the advantage of the patients’ previous records in order to
minimize the delay before obtaining data. Patients with COPD, those who
were smokers, or those with poor nasal airflow in either nostril, for
example due to nasal congestion, were excluded. Efforts were made to
see each patient within 30 min of arrival at the hospital. For the data
collected on an individual patient to be eligible for subsequent
inclusion in the analysis, a case definition of asthma that was based
on the following three criteria was applied later after a review of the
case notes: (1) a previous diagnosis of asthma; (2) a diagnosis, by the
responsible clinician, of acute asthma on this emergency department
visit with no other diagnosis that would be likely to affect the
respiratory system; and (3) a substantial improvement in airways
obstruction in response to bronchodilator therapy.
Control Subjects:
The control group was drawn from the same
local population as the patients with asthma. A control group was used
because SNIP is a volitional test that might not be performed well by
those who are ill (or injured). The control group was selected to
control for this potential problem. Patients attending the emergency
departments with acute problems not affecting the nervous system,
chest, or abdomen, who were aged 15 to 60 years, were eligible to take
part in the study. The control subjects to be recruited were selected
to give an age range comparable to that of the patients with
asthma. Potentially eligible patients were identified from the
computerized patient register. Patients with poor nasal airflow again
were excluded, as were patients with known airways obstruction.
Study Protocol:
The investigators were based within the
emergency department and endeavored to see the patients and record the
measurements as soon as possible after the arrival of patients at the
hospital. For ethical reasons, all patients with asthma received
nebulized albuterol before the recordings were made. For each patient
and control subject the following data were recorded: age; sex; height;
PEFR (best of three); and spirometry (best of two reproducible
recordings of FEV1 and FVC). Subjects then occluded
one nostril with the cone connected to SNIP meter B, and, following an
initial explanation and coaching, performed 15 maximal sniffs while
seated from functional residual capacity (FRC) through the other
nostril. Each maneuver was observed closely. Those maneuvers not taken
from FRC at the end of a relaxed tidal expiration were excluded.
Feedback on performance was provided, and the subjects were encouraged
to make the strongest sniffs possible. If the 15th sniff was the
strongest, then one or more further sniffs were recorded until no
further increase in sniff pressure was observed. Subjects rested, as
necessary, between sniffs, and supplementary oxygen was given as
required. The most negative of the 15 sniffs was used in the subsequent
analysis.
Follow-up:
To assess the baseline comparability of the
inspiratory muscle strength of the patients with asthma with that of
the control subjects, a follow-up study was undertaken. All patients
were asked at presentation if they were willing to be followed up, and
attempts were made beginning 6 weeks after the initial presentation to
contact each patient by telephone and to repeat the measurements at a
time when the patient was well. Measurements were made either at the
hospital or at home during a visit by one of the investigators
(I.M.S.).
Second Study
To assess the extent to which intrathoracic negative-pressure
generation was reflected in the SNIP measurement during maximal sniffs,
a subgroup of patients with asthma was recruited who were willing to
have intrathoracic pressure measurements made. For practical reasons,
this subgroup was recruited from among admitted patients so that the
procedure could be undertaken in the more settled ward environment.
Measurements were made on the first day of hospital admission. A
control group was recruited from laboratory staff with normal lung
function because it was anticipated that recruitment of a subgroup of
the control patients from the main study would be difficult. Patients
and control subjects were aged 15 to 50 years, were nonsmokers,
and were without other significant illnesses. In the patients
and control subjects, a conventional balloon catheter was passed to the
mid-esophagus, with its distal tip 40 cm from the external nares. This
catheter was connected to SNIP meter A. The baseline zero was set to
end-expiratory esophageal pressure during tidal breathing. SNIP meter B
was connected to a cone occluding the other nostril. The simultaneous
readings of both SNIP meters were recorded while the patients and
control subjects performed two series of 10 sniffs with feedback and
encouragement to perform the strongest sniffs possible. The baseline of
SNIP meter A was reset before each series.
Reproducibility
It is conventional to record SNIP in a series of 10 or 15
sniffs. This number of measurements is taken to allow the subject to
become familiar with the technique and on the assumption that there
will be a number of measurements, usually toward the end of the series,
that lie close to the true maximum. An assessment of reproducibility
was performed from an analysis of the last five SNIP measurements in
each series of 
15 sniffs. Within-session reproducibility was
assessed by calculating the intraclass correlation coefficient. This
dimensionless index is derived from one-way analysis of variance and
equals the ratio of the between-subject variation to total variation.
The index would equal unity in perfect reproducibility and should be
> 0.6 for a method of measurement to be useful.3
This
index was calculated for sniffs in the first study (1) analyzing all
series together and (2) analyzing the four subgroups of asthmatic
patients and control subjects at presentation and follow-up.
In order to explore the question of whether 15 sniffs, rather than 10, are necessary in order to obtain a reliable maximal sniff, the ordinal number (1st to 16th) of the maximum SNIP and the maximum SNIP measurement in the first 10 were recorded.
Statistical Analysis
The mean SNIP values at presentation for men and women with
asthma were compared to those in control subjects by unpaired
t tests. The changes in SNIP between presentation and
follow-up were compared by paired t tests. Reproducibility
was compared using the intraclass correlation
coefficient.4
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSummaryReferences |
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The strongest SNIP generally was recorded in the second half of each series of sniffs (Fig 1 ), and this was independent of the diagnosis or acuteness of the condition. The strongest SNIP was recorded after the 10th sniff in 32 of 51 patients (63%) patients with asthma at presentation and in 15 of the 25 (60%) of these seen for follow-up. The corresponding figures for the control subjects were 29 to 65 subjects (64%) at presentation and 13 of the 17 subjects (76%) seen for follow-up. For individual subjects, the maximum SNIP was not achieved any earlier in the series of sniffs at follow-up than it had been at presentation (mean, 0.8 sniffs later). In the 89 subjects with the strongest sniff after the 10th sniff in the series, the strongest SNIP recorded would have been, on average, 12 cm H2O (SD, 8.6 cm H2O) lower if only the first 10 sniffs had been recorded.
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSummaryReferences |
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In the same way, the small difference in SNIP between those patients judged to need hospital admission and those who were discharged from the hospital is likely to be due to differences in hyperinflation rather than to inspiratory muscle fatigue.
Critique of the Method
Hyperinflation:
An approximate estimate of the effect of
hyperinflation on inspiratory pressure-generating capacity can be made
from the published data of the dependence of sniff pressures on lung
volume.5
Wanke and colleagues5
developed
equations for the dependence of maximal sniff pressures
(ie, mouth pressure measured in the oropharynx, which is
very similar to SNIP) on FRC measurements. Although FRC was not
measured in the present study, estimates can be made from known data of
FRC changes in patients with acute asthma using FEV1 as the
basis for comparison1
6
7
8
(Fig 3
). On this basis, the FRC for the patients in the present study can be
estimated as approximately 40% above that predicted, an increase that
would be associated, using the equations of Wanke et al,5
with an approximate 20% reduction in SNIP. Although this adjustment is
an indirect estimate, taken in conjunction with the adjustment for
impaired pressure transmission discussed above, it is highly unlikely
that there is any remaining difference in inspiratory
pressure-generating capacity between the patients with asthma and the
control subjects.
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Effect of Treatment Before SNIP Measurements Were Recorded:
For ethical reasons, all of the patients with asthma were treated with
nebulized albuterol shortly before the measurements were taken. This
would have led to some bronchodilation and to a partial reduction in
hyperinflation in many of the patients, and hence some reduction in
load.16
This possibly could have led to resolution of
high-frequency fatigue had it been present, although there is good
evidence that LFF resolves gradually over several hours.14
Severity of Asthma in the Patients Studied:
This study
assessed patients with acute asthma that was severe enough to cause
breathlessness and, in many cases, hospital admission, but it did not
necessitate mechanical ventilation. Although inspiratory muscle fatigue
could be important in cases of more severe asthma, some evidence of
developing fatigue might be expected at a less severe stage. We would
suggest that any reduction in respiratory muscle strength in more
severely affected patients is as likely to be the result of
hyperinflation as fatigue. Nevertheless, such patients, although few in
number and difficult to study, would be the most appropriate for
further investigation concerning the possibility of fatigue.
Choice of the SNIP Technique:
The most reliable available
method for studying the contractility of the diaphragm is the
nonvolitional technique of magnetic phrenic nerve stimulation and the
measurement of transdiaphragmatic pressure.17
However, the
practical difficulties involved have, to date, prevented such
measurements in patients with acute asthma. The virtues of the SNIP
method are its ease of use and portability, enabling inspiratory muscle
strength measurements to be taken quickly and reliably in ill patients.
The finding in patients with acute asthma of moderate severity that
inspiratory muscle strength is near normal (having allowed for
hyperinflation) reduces the need for complex studies in this patient
group.
Comparison With Previous Studies:
Inspiratory muscle strength
and endurance have been studied7
18
in the laboratory
after bronchospasm induced by histamine inhalation. These studies have
shown the inspiratory muscles to be relatively resistant to fatigue,
with no loss of inspiratory muscle strength once corrections had been
made for hyperinflation. However, the healthy volunteers with stable
asthma in these laboratory studies may not be fully comparable to
patients presenting to the hospital with acute asthma who may have been
ill for some time.
Very few data are available investigating this issue in patients with naturally occurring attacks of asthma. One study1 of 20 patients with acute asthma (FEV1, 36% predicted) suggested that inspiratory muscle strength was comparable to predicted values. However, the investigators encountered difficulties in obtaining reproducible measurements of PImax to measure inspiratory muscle strength.
Several possible explanations have been suggested for why the inspiratory muscles may be fatigue-resistant, particularly in patients with asthma. These suggestions include diaphragm ischemia being reduced by negative intrathoracic pressure promoting diaphragmatic blood flow, the compensatory mechanisms within the diaphragm17 that might exist at a biochemical level,7 increased muscle thickness,19 the central drive being reduced to avoid excessive loading of the diaphragm,20 or extradiaphragmatic inspiratory muscles, such as the scalenes, being more resistant to fatigue during hyperinflation as they operate closer to their optimal lengths.21
Practical Issues Concerning the SNIP Method:
Most studies
using SNIP to measure inspiratory muscle strength have hitherto been
conducted in patients in stable condition. This study confirms that
because of the learning effect, a number of sniff maneuvers need to be
performed in order to be confident of obtaining a maximal or
near-maximal reading. Recording 15 rather than the conventional 10
measurements will lead to a higher maximal reading in about half of the
patients studied, typically by about 10%. The reproducibility of the
SNIP measurement was as good in the ill patients (ie,
acute measurements) as it was in the well patients (ie,
measurements made after recovery), and the number of sniffs required to
reach the maximum was also similar in both groups. This suggests that
ill patients grasped the technique as quickly as those who were well.
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Summary |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionSummaryReferences |
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Footnotes |
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Received for publication March 1, 2001. Accepted for publication March 27, 2001.
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This article has been cited by other articles:
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  J-W. Fitting Sniff nasal inspiratory pressure: simple or too simple? Eur. Respir. J., May 1, 2006; 27(5): 881 - 883. [Full Text] [PDF]
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F. Lofaso, F. Nicot, M. Lejaille, L. Falaize, A. Louis, A. Clement, J-C. Raphael, D. Orlikowski, and B. Fauroux Sniff nasal inspiratory pressure: what is the optimal number of sniffs? Eur. Respir. J., May 1, 2006; 27(5): 980 - 982. [Abstract] [Full Text] [PDF]
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 T. Ritz and W. T. Roth Behavioral Interventions in Asthma: Breathing Training Behav Modif, October 1, 2003; 27(5): 710 - 730. [Abstract] [PDF]
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 E. R. McFadden Jr. Acute Severe Asthma Am. J. Respir. Crit. Care Med., October 1, 2003; 168(7): 740 - 759. [Abstract] [Full Text] [PDF]
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