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* From the College of Nursing (Dr. Smeltzer), Villanova University, Villanova, PA; and the Department of Medicine (Dr. Lavietes), University of Medicine and Dentistry of New Jersey, Newark, NJ. Supported by National Institute of Nursing Research, National Institutes of Health grant R15 NR02763–01.
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Abstract |
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 TOP Abstract IntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Design: A descriptive, comparative design with repeated measures was used.
Setting: Four sets of 10 PImax and 10 PEmax measurements were obtained over a 4-week period from MS subjects in their homes. The same measurements were obtained from healthy control subjects in a private setting.
Subjects: Seventy-two MS patients and 61 healthy control subjects participated in the study.
Measurement: PImax and PEmax values were obtained by using previously published methods.
Results: Mean PEmax and PImax values for MS patients differed over the first three of the four testing sessions. By contrast, mean PEmax and PImax values for healthy control subjects differed only when the first session values were compared with values from the last three sessions. For MS patients, PEmax and PImax increased between the first and 10th trial during the first testing session, but not during the subsequent three sessions.
Conclusions: The results of this study suggest that several practice sessions should be provided in order to obtain reliable PEmax and PImax values in persons with MS. At least one practice session should be provided for healthy control subjects before identifying a baseline.
Key Words: maximal respiratory pressures • multiple sclerosis • respiratory muscle strength
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Several disease-related changes associated with multiple sclerosis (MS) have the potential to affect measurement of maximal respiratory pressures; these include systemic fatigue, muscle spasticity, incoordination of the respiratory muscles, upper extremity weakness, bulbar symptoms, and weakness of the facial muscles. Studies of measurement of inspiratory and expiratory muscle strength in other neurologic disorders have not addressed the number of trials in a testing session and number of sessions required to obtain reliable results.
The purpose of this study was to assess the reliability of measurement of PImax and PEmax in subjects with MS and in a group of healthy control subjects. This study identified the number of weekly testing sessions needed and the number of measurements needed in a single testing session to obtain reproducible results, and examined these in MS patients by level of fatigue, ambulatory status, and sex.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Subjects
A convenience sample of persons with clinically definite
MS8
was recruited from the MS clinics of two university
teaching hospitals and a chapter of the Multiple Sclerosis Society. A
second sample of healthy control subjects was recruited from the
student body, faculty, and staff of one of the universities to permit
comparison of values of subjects with MS to those of healthy control
subjects. Only persons naive to measurement of inspiratory and
expiratory pressures were included in the study. To be eligible,
subjects had to understand the procedures and be willing and able to
give informed consent and to cooperate with the testing procedures. MS
subjects were excluded if they reported an upper respiratory infection
either in the last 2 weeks or during the study; were, or appeared to
be, depressed; had fever; or were seeking treatment for an MS
exacerbation. Control subjects were free of neurologic or pulmonary
disease. The study was approved by the appropriate institutional
committees on human research.
The sample included 72 MS patients and 61 healthy control subjects. Demographic characteristics of the two groups are summarized in Table 1 . Ambulatory status of MS subjects was categorized as ambulatory, ambulatory with assistance, and nonambulatory. Ambulatory status of MS study subjects ranged from completely ambulatory with no assistance required to nonambulatory and requiring a wheelchair or motorized scooter to move from place to place. Those requiring assistive devices used a cane, crutches, or a walker for ambulation. Data on ambulatory status are missing for five subjects.
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PImax and PEmax were measured with a 200-cm magnehelic pressure gauge (No. 2000; Dwyer Instruments, Inc; Michigan City, IN). The pressure gauge measures pressures from 0 to ± 200 cm H2O in increments of 5 cm H2O. Tubing 1 inch in diameter was used to connect the gauge to a three-way valve (No. 21043; Collins/Cybermedic; Braintree, MA) and the three-way valve to a plastic unflanged mouthpiece, 2.7 cm in diameter. One arm of the three-way valve was connected by tubing to the mouthpiece, the second arm was connected to the gauge, and the third arm was open to room air. A leak was created in the system with a 16-gauge needle to prevent generation of spuriously high pressures by the buccal muscles and to assist subjects in maintaining an open glottis during the measurements. Use of the three-way valve permitted subjects to position and seal the mouthpiece before the maneuver was performed, thus reducing technical measurement errors observed in some MS patients. Such errors are associated with tremor, lack of hand coordination, upper extremity weakness, or facial muscle weakness. Measurements were obtained with subjects seated and wearing a nose clamp. Subjects were permitted to hold the mouthpiece to position it comfortably and to hold their cheeks if necessary, although none elected to do so. A minimum rest period of 90 s was provided between measurements. Subjects were coached and encouraged during the measurements to achieve the highest values possible.
Calibration Technique: The measurement device was calibrated with low-, medium-, and high-range pressures generated by one investigator. This calibration produced identical values obtained simultaneously on the magnehelic pressure gauge and a mercury manometer. Prior to testing each subject, the testing device was calibrated to zero.
Protocol: With the three-way valve open to room air, the mouthpiece was inserted in the subjects' mouths and subjects were asked to form a seal around the mouthpiece with their lips. For PEmax, subjects were asked to inhale to total lung capacity (obtained by having subjects fill their lungs by taking as deep a breath as possible); the three-way valve was then turned to the closed position (connected to the gauge), and subjects were instructed to exhale with their maximal expiratory effort, producing a single expiratory effort. For PImax, subjects were asked to exhale to residual volume (obtained by having subjects empty their lungs by exhaling as much as possible), the three-way valve was then turned to the closed position (connected to the gauge), and subjects were instructed to inhale with their maximal inspiratory effort, producing a single inspiratory effort. For measurements to be considered technically acceptable, there could be no audible air leak around the mouthpiece detected by the investigator or reported by the subject, the subject had to report a successful effort, and pressure had to be maintained for at least 1 second.
PEmax measurements were obtained before PImax measurements in all subjects because of previous data5 6 indicating that expiratory muscles are more impaired in persons with MS than inspiratory muscles, and because of our desire to minimize the effects of more fatiguing measurements of inspiratory pressures on expiratory measurements. PEmax and PImax measurements were repeated a maximum of 10 times; fewer than 10 measurements were taken if the subject reported being unable to continue because of fatigue or if two consecutive pressures decreased 10 cm H2O or more from the maximum pressure obtained previously by that subject after three technically acceptable measurements. Subjects were tested four times: the initial testing period was followed by repeat testing 1, 2, and 3 weeks later. A maximum of 10 PEmax and 10 PImax measurements were obtained during each session. The number of testing sessions (four sessions over 4 weeks) was selected because previous studies have shown that maximum values generally have been reached by the third session and plateaued by the fourth session.2
Level of Fatigue: Prior to and following completion of the testing, all subjects were asked to indicate their level of fatigue on a visual analog scale (10-cm horizontal line), with anchors of "no fatigue" (scored as 0) and "severe fatigue" (scored as 10). Subjects indicated their level of fatigue by making a mark at the point on the horizontal line that best reflected their systemic fatigue level. Ratings of fatigue on the 10-cm visual analog scale were categorized as low (0 to 3.3), moderate (3.4 to 6.6), or high (> 6.6). In pilot work, MS patients have been able to distinguish between their fatigue levels before and after testing and from one session to the next. This method has been used in other studies to assess the degree of fatigue experienced by patients with MS.10
All MS subjects were tested in their homes to minimize the inconvenience and systemic MS-related fatigue resulting from efforts of traveling to the MS clinic or the researcher's office. The control subjects were tested in a private office. For each subject, testing was conducted in the same setting and at the same time each day to minimize the effects of late afternoon fatigue reported in MS. Subjects were asked not to modify their activities or level of exercise during the course of their participation in the study; they were asked to avoid any extremely fatiguing activities the day before and day of testing.
Statistical Analysis
Descriptive statistics were used to describe the sample.
PEmax and PImax values over the four testing
sessions and within each session were analyzed by repeated measures
analysis of variance (ANOVA) to identify changes in values over the
course of the four sessions and over the 10 measurements in each
session; Scheffe post-hoc analyses were conducted to identify specific
differences between sessions and between measurements within sessions
(p < 0.05). Two-factor repeated measures ANOVA was used to examine
differences in the number of measurements within sessions by categories
of fatigue, ambulatory status, and sex. Paired t tests were
used to compare pre- and post-testing fatigue scores. Although absolute
values (cm H2O) and percent of predicted values
of maximal respiratory pressures were calculated, results presented
here are based on the prediction equations of Black and
Hyatt.9
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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These results indicate that two practice sessions are needed for MS patients to produce reliable PEmax and PImax values by the third testing session. Healthy control subjects needed one practice in order to obtain reliable PEmax and PImax values by the second session.
Number of Measurements Within a Testing Session
The mean values of each of the 10 measurements of
PEmax and PImax in each of the four testing
sessions were calculated for the two groups separately (Fig 1
) to determine the number of measurements within each session needed for
MS patients and healthy controls to obtain consistent values. In MS
patients, significant differences were detected between the 10 values
of PEmax obtained in the first testing session
["within-subject" F (9, 71) = 11.661; p = 0.0001].
Post hoc analyses demonstrated differences when the first
and second PEmax values were compared with other
values in the first testing session. No significant differences were
found among the 10 PEmax measurements obtained in
any of the remaining three testing sessions. In MS patients, the only
differences in PImax values within a testing
session occurred during the first testing session
[within-subject F (9, 71) = 10.355; p = 0.0001]
when the first four values in the first testing session were compared
with values obtained later in that session.
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Significant differences were found for healthy control subjects' PImax values when the first three PImax values of the first testing session were compared with values obtained later in that session [within-subject F (9, 60) = 22.7; p = 0.0001]. In the second testing session, the first and second values differed when compared with the fifth through 10th values and the ninth and 10th values, respectively. In the third testing session, no significant differences among measurements were found. In the fourth testing session, the only significant difference was between the second and 10th values.
Three technically correct measurements in the third testing session are needed to obtain three reliable PImax and PEmax values in MS patients. In healthy control subjects, five technically correct values in the second testing session are needed to obtain three reproducible values. Because the values of the first few measurements of PEmax and PImax differed from later measurements in MS patients' first two testing sessions and in all four testing sessions for healthy control subjects, analyses were repeated on mean PEmax and PImax values for each testing session after the first three PEmax and PImax values obtained in each testing session were deleted. This was done to determine whether the number of testing sessions needed to obtain reliable results was a function of the differences demonstrated in the first few measurements obtained during testing sessions. Results of repeated measures ANOVA using the fourth through 10th values of each of the four testing sessions duplicated the results, demonstrating that two practice sessions were required by MS patients in order to obtain reliable PEmax and PImax values by the third testing session, and one practice session was required by healthy control subjects to produce reliable PEmax and PImax values by the second testing session.
Sex
No interactions between sex of MS patients and repeated
measurements (four testing sessions) of PEmax or
PImax were detected by two-factor repeated measures ANOVA.
No interactions between sex and number of measurements (10 measurements
in each session) were detected in any of the four PEmax
sessions. There was an interaction between sex and repeated measures of
PImax in the first testing session only [F (1
,9) = 2.016; p = 0.04].
Fatigue
MS patients' ratings of their general level of fatigue before and
immediately after testing were compared; patients rated their fatigue
level as significantly greater after testing (paired t test
(68) = 5.7; p = 0.0001]. Ratings of fatigue did not differ across
the four testing sessions. Analysis of PEmax and
PImax values by level of fatigue demonstrated no
interaction between PEmax or
PImax values and fatigue level during the four
testing sessions or with the 10 measurements obtained in each of the
four testing sessions.
Ambulatory Status
Mean values of MS patients' PEmax and
PImax differed by category of ambulatory status, with less
disabled patients having higher values. While there are significant
differences in PEmax [F (2, 66) = 13.864;
p = 0.0001] and PImax [F (2,
66) = 8.914; p = 0.0004] by ambulatory status, no interactions
were detected between number of testing sessions or number of
measurements within each testing session.
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Number of Measurements in a Single Testing Session
Three technically correct measurements in the third testing
session were needed in MS patients and five measurements in the second
testing session by healthy control subjects to obtain reproducible
PImax and PEmax values. The number of
measurements needed to obtain the highest values of PImax
has been the subject of several studies. In one study, when healthy
subjects performed PImax tests 10 or more times, pressures
were higher than those reported by other researchers who used only two
and three measurements.12
Others have reported that in
healthy young adults, the maximal value of PImax was
related to the number of trials carried out, with values continuing to
increase up to 10 trials.13
In a study that examined the
number of trials needed to obtain reproducible PImax values
in patients with chronic airflow limitation, subjects were asked to
perform 20 PImax maneuvers each separated by 30 to 40
s.1
A minimum of nine PImax maneuvers were
required to obtain reproducible PImax values in
inexperienced, untrained patients with chronic airflow limitation. In a
study of elderly healthy subjects, six measurements of
PImax and PEmax were usually necessary to
obtain three acceptable measurements in the healthy
elderly.7
The increases in values that were obtained with
repeated measurements in these studies again suggest that learning may
be important in the reproducibility of these measurements.
Because 10 PEmax and PImax measurements were obtained in each of the four testing sessions in the present study, it is not known if learning or mastery could be achieved with fewer than 10 measurements in each session. To answer that question, another study would be necessary comparing results obtained after fewer than 10 measurements.
Testing of Patients With Neurologic and Neuromuscular Disorders
Although a number of researchers have examined maximal respiratory
pressures in patients with neurologic and neuromuscular diseases and
reported decreased values,4
14
15
16
no previous study has
addressed the number of measurement efforts in a single testing session
or the number of testing sessions needed to account for learning or
mastery effect in these patients. The findings of this study suggest
that patients with neurologic impairment may require at least two
practice testing sessions, more than healthy control subjects require,
to produce reliable values at the third testing session. These findings
suggest that obtaining PImax and PEmax values
during a single session and recording only the highest value obtained
in that session is likely to produce inaccurate results in persons with
MS. MS subjects' PEmax values reached a plateau by the
third session with remarkably little difference between values from one
measurement to the next in the third and fourth testing sessions;
control subjects, on the other hand, continued to increase their values
across the four testing sessions and across the 10 measurements within
each testing session, a finding consistent with that of
others.13
Recent studies have shown that persons with MS experience respiratory muscle weakness earlier in the course of the disease than previously reported and that expiratory muscle weakness is more severe than inspiratory muscle weakness.5 6 17 When it is severe, expiratory muscle weakness in persons with MS may lead to a weak, ineffective cough and inability to clear the airway, leading to respiratory complications that have been and remain a common cause of morbidity and mortality in MS.18 19 20 Because efforts were made in this study to minimize measurement error in MS subjects by allowing subjects to place the mouthpiece in their mouths prior to their PImax and PEmax efforts and eliminating the need for them to hold the testing device and bring it to their lips, the expiratory muscle weakness seen in MS subjects can be considered a true finding rather than a spurious one resulting from measurement error.
Fatigue, so common and disabling in persons with MS,21 was expected to affect their PEmax and PImax values. However, PEmax and PImax values in MS patients did not differ by fatigue level and were not affected by fatigue level over multiple testing sessions or measurements within a session, even though most patients reported increased fatigue after testing. Ambulatory status did affect the number of measurements of PEmax needed, but only during the first testing session; thus, providing two practice sessions before obtaining the true baseline measurement should address this effect. Sex and fatigue level did not affect the number of testing sessions or the number of measurements within testing sessions required to obtain consistent results.
Of interest is that PEmax was less than expected in this
study, even in healthy control subjects. Although the expiratory muscle
weakness in persons with physical limitations due to MS may be
attributed to deconditioning associated with lack of physical activity,
the explanation for decreased PEmax in healthy control
subjects, to 73.3% of predicted (norm 
80% of predicted), is less
obvious. Although normal PImax and PEmax values
were first published three decades ago and have been used by clinicians
and researchers for more than 30 years, large variations in these
values have been reported.9
12
14
Several authors have
demonstrated values in healthy subjects to be higher than published
norms9
and attribute these differences to a learning
effect that can be demonstrated by requiring a greater number of
repetitions of the measurements.1
12
By contrast, other
authors have suggested that these norms may overestimate
PImax by as much as 15% and PEmax by a greater
percentage.7
Methodologic differences, including variation
in the mouthpiece used in studies, and a learning effect have been
identified as two factors that may be responsible for these
variations.4
22
The selection of the Black and Hyatt standards9 for this study requires comment. The mouthpiece used enabled subjects with weakness of the cheeks to grasp the mouthpiece and make a tight seal with their lips. While previous data have shown that subjects develop greater pressures when using unflanged as opposed to flanged mouthpieces,22 the mouthpiece used here most closely resembled that used by Black and Hyatt (ie, without flanges). The fact that the data obtained with this mouthpiece were very similar to data previously collected in MS patients using the standard Black and Hyatt apparatus9 further supports use of these standards in this study.
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Conclusion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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Footnotes |
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Abbreviations: ANOVA = analysis of variance; MS = multiple sclerosis; PEmax = maximal expiratory pressure; PImax = maximal inspiratory pressure
Received for publication June 9, 1998. Accepted for publication January 12, 1999.
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References |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionReferences |
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This article has been cited by other articles:
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  F K Mutluay, H N Gurses, and S Saip Effects of multiple sclerosis on respiratory functions Clinical Rehabilitation, April 1, 2005; 19(4): 426 - 432. [Abstract] [PDF]
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= mean values for first testing
session; 
= mean values for second testing session; 
= mean
values for third testing session; x = mean values for fourth testing
session.