How Many Maneuvers Are Required to Measure Maximal Inspiratory Pressure Accurately?

Pulmonary Physiologic Test of the Month How Many Maneuvers Are Required to Measure Maximal Inspiratory Pressure Accurately?* AndrewS. W en, MD; Marlyn S. Woo, MD; and Thomas G. Keens, MD, FCCP

Objective: To determine whether performing more maximal inspiratory pressure (MIP) maneuvers per test provides a more accurate assessment of the true maximal inspiratory strength. Design: Review of MIP data from 367 tests. Each subject was encouraged to perform 20 MIP maneuvers per test, unless the patient reached the highest measurable pressure three times, or because of poor cooperation, fatigue, or respiratory distress. From the same raw data, MIP was calculated in two ways: (1) the "short MIP" was defined as the average of the first three highest values with :55% vaiiability; the results from further maneuvers were ignored; and (2) the "long MIP" is defined as the average of the three highest values with :55% vaiiability from all recorded maneuvers. Setting: Pulmonary Physiology Laboratory, Childrens Hospital Los Angeles. Participants: One hundred seventy-eight pediatiic and adult subjects (age, 14 ± 3 [SD] years; 53% male) with suspected inspiratory muscle weakness. Measurements and results: The long MIP (91±39 em H 2 0) was significantly greater than the short MIP (82±39 em H 2 0) (p<0.000005). In 177 of 367 tests, the short MIP underestimated the peak performance. Conclusions: From the same raw data, the long MIP was significantly greater than the short MIP. In 48% of the tests, the short MIP method underestimated the peak performance determined by the long MIP method. We speculate that the difference between the long MIP and the short MIP can be attiibuted to a learning effect. (CHEST 1997; 111:802-07) Key words: inspiratmy muscle strength; learning effect; maximal inspi ratory pressure; pediatric; pulmonary function tests; ventilatory muscle strength Abbreviations: MIP =maximal inspiratory pressure

M aximal inspiratory pressure (MIP ) is a simple,

reproducible, and noninvasive test used to assess inspiratory muscle strength. MIP measurements are known to be influenced by gender, age, lung volumes, and body habitus,1- 7 and by variations in method. Some investigators 1 ·2 · 8 ·9 have attempted to incorporate the influences of multiple factors into their measurements; however, the pl ethora of confounding factors still makes the clinical application of *From the Division of Pediatric Pulmonology, Childrens Hospital Los Angeles, Department of Pediatrics, USC School of Medicine, Los Angeles. Manuscript received Feb!llaty 20, 1996; revision accepted July 22, 1996. Reprint requests: Dr. Marlyn Woo, Division of Pediatric Pulnwnology-mailstop 83, Childrens Hospital Los Angeles, 4650 Sunset Blvd, Los Angeles, CA 90027 802

MIP difficult. This study was designed to determine the importance of one specific variable in method: that is, whether performing more MIP maneuvers per test provides a more accurate assessment of inspiratory muscle strength. In spirometry, there is agreement that three appropriately performed trials are sufficient for determining peak expiratory flow rates, vital capacity, and FVC. In fact, eight attempts are considered the "practical upper limit for most subjects." 10 However, for measurement of MIP, there is no such consensus. Recent studies using MIP measurements have determined peak performance using the best of only five or fewer maneuvers per test,2 - 7 •11 · 18 while other studies used five or more maneuvers per test.19-2 3 Early study of respiratory muscle function by Pulmonary Physiologic Test of the Month

Ringqvist 1 and by Black and Hyatt 2 established the generally accepted normative data. However, their methods also differed with respect to this issue. Ringqvist 1 believed that measuring peak performance of the MIP maneuver required an extensive series of maneuvers in order for the inexperienced subject to learn the maneuver. He used an average of 10 maneuvers per test to establish his normative data. In contrast, Black and Hyatt2 established their normative data based on the best of only two technically acceptable maneuvers. Their results were generally 10 to 20 em H 2 0 less than those of Ringqvist. Though measuring MIP is simple, p erforming a long series of maneuvers at each testing session can be time-consuming and tedious. Furthermore, it is unclear whether performing more MIP maneuvers per test provides additional useful information. This study was designed to answer this question. MATERIALS AND METHODS Subjects

We a nalyzed raw data from 367 MIP tests performed by 178 pati ents (age, 14::+::3 [SD] years; range, 4 to 25 years; 159 children and 19 adults; 53% male; weight, 45 ::+:: 15 kg; total lung capacity, 80 ::+:: 26% predicted, and residual volume, 154::+: 85% predicted) between 1988 to 1995. Adult subjects (age, 20::+:: 2 years) performed 26 tests. At Childrens Hospital Los Angeles, MIP evaluations are performed routinely in patients with neuromuscular diseases and musculoskeletal abnorm alities. Patients had multiple MIP evaluations as clinically indicated. Patients were evaluated 2::+::3 ti mes (range, 1 to 20). Among the 178 patients, 88 had chest w all abnormalities, 5 6 had neuromu scular disease, 18 had cystic fibrosis, and seven had asthm a. Maximal Inspiratory Pressure

Tests were perform ed in the Pulmona1y Physiology Laborat01y of Childrens Hospital Los Angeles, located at 398 feet above sea level with a m ean atmospheri c pressure of 751 mm Hg. MIP was measured by a technique previously described by Nickerson and Keens.2L Measurements were perform ed with the patients in the seated position wearing nose clips and breathing via a mouthpiece. The mouthpiece was connected directly to a manifold with a safety port that could be easily occluded b y the subject's finger (Fig 1). The manifold included a 1.5-mm hole to help keep the glottis open, th ereby preventing the subj ect from generating additional negative pressure with facial or pha1yngeal muscles. The manifold was connected to a pressure gauge (Inspiratory Force Meter, model4101 ; Boehringer L aboratories, Inc. Norristown, Pa) via an isolation kit that separates the meter from the patient. The isolation kit uses an 1 8-inch surgical tube ( Tygon) (internal diameter, 1/8 inch; outer diameter, 1/4 inch; wall thickness, 1/16 inch) ( Perform ance Plastics; Akron, Ohio). The pressure gauge measures pressures from - 150 em H 2 0 to + 150 em H 2 0 in increments of 2 em H20 . As recommended b ythe manufacturer, the pressure gauge was calibrated a gainst a standard manometer annually.

FIGURE 1. Inspiratory force measurement apparatus. A =rubber mouthpiece; B= manifold wi th safe ty port and 1.5-mm air leak; C= isolation kit allowing separation of the meterfrom the patient; D = inspiratory fore~ mete r. The safety port is plugged b y th e subject's finger b efore inspiration. The air leak r emains open during the maneuver t o help keep the g lottis open.

MIPs were measured by a small group of experi enced pulmonary technicians w ho were all trained b y o nesenior pulmonary technician. Piior to testing, each patient was given the same instructions for p erforming th e MIP maneuver. Weekly supervision of pulmonary fun ction testing was performed b y the senior pulmona1y techni cian, and adjustments in instru ction and technique were instituted as needed to minimize variability. Performance of th e MIP maneuver followed an introduction and detailed instruction of the MIP maneuver bythe pulmonary technician. Patients were instructed to inhale to total lung capacity, to exh ale slowly to residual volume, to occlude the safety p01i, then to inhale maximally. Patients were instructed notto use their cheek and mouth muscles to generate addition al pressure. The inspiratory force meter measured the MIP generated. MIP was defin ed as the largest negative pressure generated at the mouth and maintained f or at east l 1 s. Values were reported as positive numbers. Demonstration of the maneuver was provided as needed. Patients were allowed to practice the maneuver as needed. Measurements were ecorded r only after th e patients were able to perform th e maneuver properly. Pulmona1y technicians provided verbal and visual feedback and encouraged patients to achieve their peak performance. Res ults of maneuvers improperly perform ed or complicated b y a nair leak were not recorded. Each attempt of the MIP maneuver lasted only a few econds s r up to a few minutes between and patients were allowed t o est o uraged t o perform each attempt. For each t est, patients were e nc the MIP maneuver at least 20 times. The test was discontinued if the pressure generated the highest value measurable by our pressure gauge (150 em H 2 0 ) three tim es, or if the subject's pressure values were decreasing because of poor cooperation, fati gue, or respiratory distress. More than 20 maneuvers were attempted as needed to establish r eproducibility within 5%. Data Analysis

MIP was calculated from the raw data in two ways . The "short MIP" was defin ed as the a verage of the first three highest values with oS:5% vaiiability. The results from further maneuvers were ignored. The "long MIP" was defin ed a s the average of the three highest values from all recorded maneuvers with oS:5% variability. Finally, knowing the peak performance determined from all recorded maneuvers for each test, we calculated the minimum CHEST I 111 I 3 I MARCH , 1997

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number of maneuvers required to reach peak p erformance three times with oS:5% variability for each test. Statistical Analysis

Parameters are expressed as mean ±SD unless otherwise indicated. Data were analyzed using the paired, one-tailed, Student's t test. Values of p < 0.025 were considered statistically significant.

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Our study showed that from the same raw data, the long MIP was significantly greater than the short MIP (mean difference, 9±13 em H 2 0 ). This relationship is seen among children and adults (Fig 2), and female subjects (long MIP, 94±40 em H 2 0 ; short MIP, 84±40 em H 2 0; p < 0.000005) and male subjects (long MIP, 87±38 em H 2 0 ; short MIP, 79±38 em H 2 0 ; p < 0.000005). In fact, in 177 of 367 tests (48%), the long MIP was larger than the corresponding short MIP. The distribution of MIP results is presented in Figure 3. Examples of individual MIP tests are presented in Figures 4 and 5. The minimum number of maneuvers to determine the long MIP by the long MIP method was greater than the minimum number of maneuvers required to determine the short MIP by the short MIP method (Fig 6). In 65% of the tests, 10 or more maneuvers were required to determine peak performance. Thirty-six patients (19 female and 17 male) were diagnosed as having abnormal MIP by the short MIP Method, but normal MIP by the long MIP method when we compared our results with normative data presented by Ringqvist 1 (MIP defined as abnormal if less than mean-2 SDs ). Therefore, even though the

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short MIP method required fewer attempts per test, in some cases, the short MIP method underestimated peak performance. We analyzed data from the 22 patients who were tested on at least four separate occasions with each test separated by at least 1 week. Between the first and fourth tests, there was no significant difference (p > 0.025) in the peak performances (first test, 80±33 em H 2 0; fourth test, 97±36 em H 2 0 ) and in the minimum number of maneuvers to reach peak performance (first test, 14±7; fourth test, 14±6). No complications from the MIP maneuver were observed. Only 10 of 367 (3%) tests were discontinued because of fatigue. Of the 10 patients, seven had neuromuscular disease, one had systemic lupus ery-

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thematosus, and two had pulmonary hypertension. Otherwise, performing 20 maneuvers per test was well tolerated by all patients.

DISCUSSION

Our study demonstrates that MIP values calculated by the long MIP method were significantly greater than values determined by the short MIP method in children and adults, and in both male and female subjects. In almost half of the tests, the short MIP underestimated the long MIP. Therefore, performing the MIP maneuver more times resulted in higher MIP values. The short MIP method assumes that peak performance is observed once results have been reproduced three times. Our observation that the short MIP underestimated the long MIP supports a recent study by Aldrich and Spiro 23 which observed that reproducibility does not establish maximal effort. Because it is unlikely that inspiratory muscle strength increases over the few minutes needed to perform an entire test, even if the long MIP also does not reflect maximal effort, the higher values certainly are a closer reflection of true inspiratory muscle strength. We speculate that the difference between the long MIP and short MIP is due to the learning effect previously noted by Ringqvist. 1 Many studies have used five or fewer maneuvers per test to establish normative data; 2 - 7 and to evaluate the effects of anesthetics, 14 corticosteroids, 11 cigarette smoking,3 and assisted-mechanical ventilation/ 5 and to evaluate diseases like cystic fibrosis, 16 heart failure ,18 and COPDP However, we found that even though the

short MIP method used an average of nine maneuvers to determine peak performance, the short MIP still underestimated the long MIP almost half of the time. When Black and H yatt2 reported normative data in healthy adults who performed only two technically satisfactory measurements, they recognized that their data were generally 10 to 20 em H 2 0 less than those reported by Ringqvist 1 who used an "extensive series of measurements" for each test. Interestingly, what is described as an "extensive series of measurements" by Ringqvist 1 was an average of only 10 maneuvers. In our study, 65% of the tests required more than 10 maneuvers to observe peak performance. Other studies have also suggested the presence of a learning effect. Enright et al3 studied elderly patients who performed only five maneuvers per test and observed that the highest value was most frequently observed at the fifth maneuver. Wagener et al 20 observed that MIPs determined by the best of five maneuvers were 5% less than MIPs determined by the best of 20 maneuvers (p<0.001). 20 In adults witl1 COPD, Fiz et aP 9 observed that a minimum of nine maneuvers were needed to observe peak performance . Larson et al 12 studied adults with COPD who performed five maneuvers per test and who were tested once a week for a total of five times. They observed a significant increase in MIP values between the first and fourth test. 12 Though Larson et al divided the performance of maneuvers over several weeks, their patients did not reach peak performance until a total of 15 to 20 maneuvers had been performed. Because children are known to require more instruction and assistance in performing pulmonary

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function tests that involve complicated breathing maneuvers,24 the difference between the long MIP and the short MIP may be more apparent in our study population than in others. However, our observation that the long MIP was also greater than the short MIP among adult patients suggests that the learning effect is important among both adults and children. If the difference between the long MIP and the short MIP is due to a learning effect, it is unclear whether the benefits of this learning effect can be retained. Wagener et al20 observed that in children who performed 20 attempts per t set several times, there was no increase in MIP after the first day of testing. Similarly, we found that among patients who had MIP evaluations at least four times on different dates, there was no significant difference between the peak performance a t the first test and at the fourth test. The MIP at the fourth test was greater than the MIP at the first test. Although this difference was not statistically s ignificant, its presence does suggest a trend of increasing inspiratory muscle strength. Considering that m any of the patients had changes in therapy after their first pulmonary function evaluation, this finding may reflect real increases in inspiratory muscle strength. However, if these patients did increase their MIP because of an increased understanding of the MIP maneuver, we expect they would have required f ewer tatempts to reach their peak performance as they became more experienced. Instead, between the first test when patients were least experienced, and the fourth test when patients were most experienced, there was no difference in the minimum number of maneuvers needed to reach peak performance . Therefore, it is unlikely that the le arning effect i s retained from week to week, and patients who have previously performed the MIP maneuve r should still be treated as though they are inexperienced. We compared our data with normative data presented by Ringqvist,1 who (like the long MIP method) used an "an extensive series" of maneuvers per test. We found that 36 of our patients were diagnosed as having decreased inspiratory muscle strength by the short MIP method, but were diagnosed as having normal muscle strength by the long MIP method. This overdiagnosis of inadequate muscle strength and the 9± 13 em H 2 0 underestimation of muscle strength by the short MIP method is especially important because MIP measurements are used to monitor changes over time in patients at risk for respiratory failure. The refore, we conclude that the difference benveen the long MIP and the short MIP is clinically significant. 806

CONCLUSION

In conclusion, our study demonstrates that from the same raw data, the long MIP was significantly greater than the short MIP. Therefore, attempting 20 maneuvers per test, as in the long MIP method, provides a more accurate assessrhent of the true inspiratory muscle strength. We speculate that the difference between the long MIP and the short MIP is due to a learning effect. In patients who performed the MIP maneuver four times, with each evaluation separated b y a we ek, there was no difference in peak performance or in the minimum number of maneuvers needed to reach peak p erformance between the first and fourth tests. Therefore , we s peculate that the learning effect is not retained from week to week, and that patients who have previously perform ed the MIP maneuver should still be treated as though they are inexperienced. ACKNOWLEDGME NTS : The authors thank Margaret Wen for her invaluable assistance with data entry. \Ne also thank Michael Stabile, MS , RPFT, and the staff at the Childrens Hospital Los Angeles Pulmonary Physiology Laboratory for their technical assistan ce. REFERENCES 1 Ringqvist T. The ventilatory capacity in healthy patients: an analysis of causal factors with special reverence to respiratory forces. Scand J Clin Lab Invest 1966; 18(suppl 88):8-170 2 Black LF, Hyatt RE. Maxi mal respiratory pressures: normal values and relationship to age and sex. A m R ev Respir Dis 1969; 99:696-702 3 Enright PL, Kronmal RA, Manolio TA, et la. Respiratoty muscle strength in the elderly. Am J Respir Crit Care Med 1994; 149:430-38 4 Enright PL, Adams AB, Boyle PJ, et al. Spirometry and maximal respiratOty pressure references from healthy Minnesota 65- to 85-year-old women and men. Chest 1995; 108:663-69 5 Smyth R, Chapman KR, Rebuck A. Maximal inspiratory and expiratory pressures in adolescents. Chest 1984; 86:568-72 6 Wilson SH, Cooke NT, Edwards RHT, et la. Predicted normal values for maxi mal respiratory press ures in Caucasian adults and children. Thorax 1984; 39:535-38 / 7 Leech J , Ghezzo H , Stevens D, e tal. Respirator)\ pressures and fun ction in young adults. Am Rev Respir :Dis 1983; 128 :17-23 ' 8 Bruschi C, Cerveri I, Zoia M, et la. Reference values of maxi mal respiratory mouth pressures: a population based study. Am Rev Respir Dis 1 992; 146:790-93 9 Rochester DF. Tests of respiratory muscle fun ction. Clin Chest Med 1988; 9:249-61 10 American Thoracic Society. Standardization of spirometry: 1994 update. Am J Respir Crit Care Med 1995; 152:1107-36 11 Weiner P, Azgad Y, Weiner M. The effect of corticosteroids on inspiratory muscle performance in hu mans. Chest 1993; 104:1788-91 12 Larson JL, Covey MK, Vitalo CA, et al. Maximal inspiratory press ure: learning effect and test -retest r eliability in patients with chronic o bstructive pulmonary disease. Chest 1993; 104:448-53 13 NavaS, Ambrosino N, Crotti P, eta!. Recruitm ent of s ome Pulmonary Physiologic Test of the Month

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respiratory muscles during three maximal inspiratory manoeuvres. Thorax 1993; 48:702-07 Gallart L, Gea J, Aguar C, et al. Effects of interpleural bupivacaine on respiratory muscle strength and pulmonary function. Anesthesiology 1995; 83:48-55 Johnson D , Gallagher C, Cavanaugh M, et la. The lack of effect of routine magnesium administration on respiratory function in mechanically ventilated patients. Chest 1993; 104:536-41 Sawyer EH, Clanton TL. Improved pulmonary function and exercise tolerance with inspiratory muscle conditioning in children with cystic fibrosis . Chest 1993; 104:1490-97 Nishimura Y, Tsutsumi M, Nakata H, et al. Relationship between respiratory muscle strength and lean body mass in men with COPD. Chest 1995; 107:1232-36 Nishimura Y, Maeda H, Tanaka K, et la. Respiratory muscle strength and hemodynamics in chronic heart failure. Chest 1994; 105:355-59

19 Fiz JA, Montserrat JM, Picado C, et al . How many manoeuvres should be done to measure maximal inspiratory mouth pressure in patients with chronic airflow obstruction. Thorax 1989; 44:419-21 20 Wagener J, Hibbert M, Landau L. Maximal respiratory pressures in children. Am Rev Respir Dis 1984; 129:873-75 21 Nickerson B, Keens TG. Measuring ventilatory muscle endurance in humans as sustainable inspiratory pressure. J Appl Physiol 1982; 52:768-72 22 Perez T, Becquart LA, Stach B, et al. Inspiratory muscle strength and endurance in steroid-dependent asthma. Am J Respir Crit Care Med 1996; 153:610-15 23 Aldrich T, Spiro P. Maximal inspiratory pressure: does reproducibility indicate full effort? Thorax 1995; 50:40-3 24 Platzker ACG, Keens TG. Pulmonary function testing in pediatric patients. In: Wilson AF, ed. Pulmonary function testing: indications and interpretations . New York: Grune & Stratton, 1985;275-92

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