Abstract
Anthropometric variables will influence maximal respiratory pressure (MRP) values. Since significant variations exist in pulmonary nomograms amongst different races, it is important that tribe specific tables of normal maximal inspiratory pressures (MIP) and maximal expiratory pressures (MEP) be developed. To date, MRP prediction equations do not exist for Hopi children.
PURPOSE:
The purpose of this study was to develop MRP reference values and prediction equations for Hopi children in the ages 4–13 years.
METHODS:
A cross-sectional study was undertaken with 288 healthy children (125 male, 163 female), a 36% representative population of all the Hopi Native children attending Hopi Tribal Elementary Schools in Arizona. MIP and MEP values were measured.
RESULTS:
Age and the inverse of body mass were consistently significant predictors of the MRPs for both sexes. Predictions using the derived Hopi equations were significantly different (p≤0.001) than those using the equations for Navajo and Caucasian youth across both sexes, making it important for this population to have specific formulae to provide more accurate reference values.
CONCLUSIONS:
These data were collected from the children of Hopi ancestry resulting in MIP and MEP reference equations which should be used when measuring MIP and MEP in these children ages 4–13 years.
Keywords: maximal inspiratory pressure, respiratory muscle strength, maximal respiratory pressure equations, Native American youth
INTRODUCTION
Maximal respiratory pressures (MRPs) indicate respiratory muscle strength and are important values to be included in a robust respiratory function test.1,2,3 Moreover, reference values for MRPs are crucial in the diagnosis and prognosis of respiratory diseases, neuromuscular weakness and health status in general.4,5 The American Thoracic Society (ATS)6 proposes that spirometric reference equations published in the third National Health and Nutrition Examination Study (NHANES III)7 should be used whenever possible. Notwithstanding the recommendation of the ATS, NHANES III accuracy is questionable if used for specific ethnic groups that were not included in the NHANES III study. Specifically, Native American individuals or children under the age of 8 years of age were not tested in NHANES III. Since the publishing of NHANES III, we have published spirometry reference equations for two different American Tribes: Hopi children8, Navajo children9, and Navajo adolescents.10 Also, we have published maximal pressure reference values for Navajo children.11 These studies showed that the specifically derived Navajo children, Hopi children, and Navajo adolescent equations were more accurate predictors of pulmonary function than the recommended NHANES III equations. Additionally, even though these groups were all Native American people, the pulmonary function test results were significantly different from each other suggesting that not all Native American tribes are monolithically anthropomorphically identical. For example, standing height and sitting height are noticeably different between the Hopi and Navajo people and will, by virtue of these differences, have different spirometric data set outcomes - an intertribal difference - just as we see racial differences between Black and Caucasian children spirometric equations.12
Anthropometric data are vital to the development of a pulmonary function test nomograms and MRP equations. Since anthropometric differences such as sitting height, standing height, and body mass vary significantly between ethnic groups,13, 14 it is important that only nomograms and prediction equations specifically derived for each ethnic group be used. Unfortunately, there is no study or prediction equation relating anthropometric data to the respiratory muscle strength of Native American Hopi children exists Therefore, the purpose of this study was to measure respiratory muscle strength in Hopi children ages 4–13 years, and to derive the tribe-specific reference values to be used in medical practice.
METHODS
Recruitment
Before any data were collected, the research design was reviewed and approved by the Institutional Review Board for Human Subjects of the Hopi Nation, the Institutional Review Board for Human Subjects of Northern Arizona University, the Hopi Tribal Council, the Hopi Health Department, the Hopi Parent-Teacher groups at the elementary schools, the Principals of the Hopi Schools, and the Hopi parents and/or guardians of the children who gave their approval to proceed with the study. Additionally, the student’s assent was also obtained prior to performing the MRP testing and data collection.
The elementary school principals of the Hopi Nation were contacted and asked to send letters about the study home with all of the children so that the parents or guardians could decide whether their children would participate in the study. Students who were ultimately tested and included in the statistical analysis of this study had to have parents and grandparents on both paternal and maternal lines who were of pure Hopi descent. Children who had a parent from other tribes or ethnic backgrounds were still tested but were excluded from the final population data set and statistical analysis of the study. The final number of students who were included in the analysis were 288 children, (n=125 males; n=163 females), which represented 36% of all Hopi children attending Hopi elementary schools.
The principle investigator and one research assistant were trained in the correct procedures for pulmonary function testing and in gathering maximal inspiratory pressure (MIP) and maximal expiratory pressure (MEP) data. Other co-workers conducted medical questionnaire interviews in English which was the dominant language of all of the Native Hopi children.
Measurements
Standing height was measured to the nearest cm in stocking feet rounding up when ≥0.5 cm according to standard procedures with the participant standing erect with the head in the Frankfort plane and the back against the standing stadiometer (Seca Stadiometer, model 213, Irvington, NJ). Sitting height was measured to the nearest cm rounding up when >0.5 cm according to standard procedures with the child sitting erect on a high-backed wooden chair that had a metric measurement on the back rest of the chair. Body mass was measured using a double beam adjustable balance (Health-O-Meter, model 401KL, McCook, IL) that was zeroed before body mass was determined. Body mass index (kg.m2) was derived from body mass and standing height.
Since only children with healthy pulmonary systems were to be used in the study, medical research personnel auscultated all bronchopulmonary segments of the lungs to rule out the presence of adventitious sounds such as wheezing, rhonchi, or crackles. Additionally, a novel respiratory questionnaire was developed in consultation with the Hopi school nurses and a pulmonologist that reflected the living conditions of Hopi families on the Hopi Reservation. There was no suitable questionnaire available because this study had not been done previously. This respiratory questionnaire was administered to all of the children participating in the study, but its use was to help determine if any outlier data was due to undetected pulmonary problems. Questions included inquiries about the history of lung disease, thoracic surgery, medication use, use of tobacco or other smoke producing ceremonial plants, home heating and cooking fuels, the presence of farm animals or pets at home, and exposures to a variety of allergens or dust. The Indian Health Service (IHS) has one hospital on the Hopi Reservation, however, Hopi families usually do not have a family physician. If there were questions about the child’s medical background, a school nurse was often an important information source who could document the presence of any respiratory disease, medication use, or allergy history.
Maximal Respiratory Pressures
The MIP and MEP maneuvers were demonstrated to each child after giving their assent and each child practiced the correct maneuver before any data was collected. This was done to reduce mistakes due to naivete. Participants wore a nose clip and stood when performing the MIP and MEP maneuvers. To measure MIP and MEP, a differential pressure gauge (Magnehelic Pressure Manometer, Dwyer Instruments, Michigan City, IN; linear range: 0–300 cm H2O) was used and connected to a mouthpiece with a 2 mm leak to accommodate for the use of the buccal muscles during the test trial.15,16 Calibration checks of the accuracy of the pressure gauge were performed using standard mercury column measurement techniques. Measurements for MIP were taken at least three or more times and until two maximal readings were within <5% difference of each other for all age groups. This measurement was performed from end-exhalation at residual volume using a disposable 1-in diameter cardboard mouthpiece, following the methods of Smyth et al.17 Measurements for MEP were taken at least three or more times until two maximal readings were within <5% difference of each other for all age groups. This measurement was performed at end-inhalation at total lung capacity using a disposable 1-in diameter cardboard mouthpiece. Between each repetition, the subject was given a 1 min rest break. The largest value of MIP and MEP was recorded for analysis.
Statistical Analyses
Linear regression analysis was utilized to determine prediction equations for each of the respiratory pressures (MIP, MEP) from the independent variables for males and females independently. The independent variables included subject age, body mass, standing height, and sitting height, as well as the square, inverse, and natural logarithms of these variables. The 5th percentile was determined to define the lower limit of the normal ranges (LLNs). The coefficients of correlation and determination and the LLNs were used to evaluate prediction accuracy of the derived functions. Analysis of variance with repeated measures [0 between factors, 1 within factor (measured and/or predicted = 4 levels)] was utilized to compare the MIP and MEP predictions using the derived equations to the predictions from previously published equations derived for other youth populations (i.e., predictions from three existing equations were compared to the predictions from the equations derived here), as well as to the actual respiratory pressures measured in the Hopi sample (i.e., predictions from three existing equations were compared to the actual measurements made on the sample). For all analyses, an α=0.05 was chosen a priori. For the analysis of variance, this experimentwise error rate was maintained throughout all post hoc tests for specific differences (post hoc adjusted α=0.0170).
RESULTS
The anthropometric and respiratory pressure data for the male and female subjects from the derivation sample are presented in Table 1. Ten children were tested but not included in the final analysis because they descended from other tribes.
Table 1.
Anthropometry and Respiratory Pressures for Hopi Youth
| Males (n = 125) | Females (n = 163) | |
|---|---|---|
| Age (yr) | 9.2 (1.8) | 9.0 (1.8) |
| 4–5 yr | n = 4 | n = 5 |
| 6–7 yr | n = 19 | n = 31 |
| 8–9 yr | n = 44 | n = 65 |
| 10–11 yr | n = 52 | n = 48 |
| 12–13 yr | n = 6 | n = 14 |
|
| ||
| Anthropometry | ||
| Standing Height (cm) | 134.7 (11.4) | 134.4 (12.4) |
| Sitting Height (cm) | 71.9 (4.7) | 71.2 (5.9) |
| Body Mass (kg) | 37.7 (12.6) | 38.2 (15.1) |
| BMI (kg ⋅ m−2) | 20.3 (4.4) | 20.5 (5.2) |
|
| ||
| Respiratory Pressures | ||
| MIP (cm H2O) | 86.8 (23.0) | 73.7 (22.0) |
| MEP (cm H2O) | 100.2 (34.7) | 75.9 (26.1) |
Values are mean (SD).
The derived sex-specific prediction equations for MIP and MEP appear in Table 2. Age and the inverse of body mass were consistently significant predictors of the respiratory pressures for both sexes. Age squared and standing height were also significant predictors in one or more of the models. From a practical clinical standpoint, it was important to determine a common set of predictor variables across all the respiratory pressures and sexes. Therefore, while the regression functions presented in Table 2 are not necessarily the “best” prediction functions for each of the respiratory pressures, it was determined that the regression functions utilizing age and the inverse of body mass as independent variables resulted in the best predictions on average for MIP and MEP across the sexes. It was desirous to have as few predictor variables as possible to reduce the complexity of the equations in the medical practice setting. While the addition of standing height and/or age squared as predictor variables resulted in increases in the coefficients of multiple determination, their contributions to the accuracy of the regression functions were nominal and their inclusion in the models deemed unnecessary.
Table 2.
Respiratory Pressure Prediction Equations for Hopi Youth
| Prediction Equation | LLN | R 2 | |
|---|---|---|---|
| Males (n = 125) | |||
| MIP (cm H2O) | = 68.150 + (4.354 * AGE) – (718.436 * invBM) | 31.1 | 0.33 |
| MEP (cm H2O) | = 88.315 + (4.870 * AGE) – (1108.804 * invBM) | 49.7 | 0.25 |
|
| |||
| Females (n = 163) | |||
| MIP (cm H2O) | = 61.702 + (2.868 * AGE) – (461.187 * invBM) | 33.1 | 0.17 |
| MEP (cm H2O) | = 33.713 + (5.108 * AGE) – (125.727 * invBM) | 39.8 | 0.15 |
AGE = age (yr); invBM = inverse of body mass (kg); LLN = subtract this value for the lower limit of the normal range (5th percentile).
Mean predicted MIP and MEP across the male and female subjects using previously published equations derived for Navajo9 and Caucasian youth4,5 (Table 3) were compared to the actual measurements made on the Hopi sample, and the predicted variables using the Hopi youth equations derived in this study (Table 4). The predictions for both MIP and MEP using the equations derived for Navajo and Caucasian youth were significantly different (p≤0.001) from the actual measurements made on the Hopi sample for both sexes, which support the derivation of Hopi specific prediction equations for MIP and MEP (Table 2). Likewise, the predictions derived from these equations were significantly different (p≤0.001) from the predicted variables derived from the Hopi specific equations across both sexes. Mean measured values for MIP (Table 5) and MEP (Table 6) across age for each sex are displayed with the predictions of the same variables using the Hopi youth equations derived here, the corresponding LLNs, and the previously published equations derived for Navajo and Caucasian youth.
Table 3.
Previously Published Respiratory Pressure Prediction Equations for Youth
| Prediction Equation | |
|---|---|
| Arnall (Navajo)11 | |
| Males | |
| MIP (cm H2O) | = 25.00 + (5.70 * AGE) |
| MEP (cm H2O) | = 23.00 + (5.60 * AGE) |
| Females | |
| MIP (cm H2O) | = 39.00 + (3.10 * AGE) |
| MEP (cm H2O) | = 37.00 + (3.10 * AGE) |
|
| |
| Wilson (Caucasian)5 | |
| Males | |
| MIP (cm H2O) | = 44.50 + (0.75 * BM) |
| MEP (cm H2O) | = 35.00 + (5.50 * AGE) |
| Females | |
| MIP (cm H2O) | = 40.00 + (0.57 * BM) |
| MEP (cm H2O) | = 24.00 + (4.80 * AGE) |
|
| |
| Tomalak (Caucasian)4 | |
| Males | |
| MIP (cm H2O) | = (0.031 + (0.711 * AGE)) * 10.1972 |
| MEP (cm H2O) | = (2.495 + (0.474 * AGE)) * 10.1972 |
| Females | |
| MIP (cm H2O) | = (1.399 + (0.461 * AGE)) * 10.1972 |
| MEP (cm H2O) | = (3.980 + (0.281 * AGE)) * 10.1972 |
AGE = age (yr); BM = body mass (kg)
Table 4.
Comparison of Predicted Respiratory Pressures in Hopi Youth Using the Derived Prediction Equations and Previously Published Equations for Use in Other Youth Populations
| Males (n = 125) | Females (n = 163) | |||
|---|---|---|---|---|
| MIP (cm H2O) | MEP (cm H2O) | MIP (cm H2O) | MEP (cm H2O) | |
| Actual: Hopi | 86.8 (23.0) | 100.2 (34.7) | 73.7 (22.0) | 75.9 (26.1) |
| Predicted: Hopia | 86.8 (13.3) | 100.2 (17.5) | 73.7 (9.1) | 75.9 (10.0) |
| Predicted: Arnall (Navajo)b | 77.2 (10.2)* | 74.3 (10.0)* | 66.9 (5.5)* | 64.9 (5.5)* |
| Predicted: Wilson (Caucasian)c | 72.8 (9.5)* | 85.3 (9.8)* | 61.8 (8.6)* | 67.1 (8.5)* |
| Predicted: Tomalak (Caucasian)d | 66.4 (13.0)* | 69.7 (8.6)* | 56.5 (8.4)* | 66.3 (5.1)* |
Mean (SD) predicted values over all subjects; Predictions using the equations from:
the present study (Table 2)
Values significantly different from the actual values measured in the sample and from the value derived from the Hopi prediction equations (p≤0.001 for all).
Table 5.
Maximal Inspiratory Pressure Predictions within Sex and across Age Groups in Hopi Youth Using the Derived Prediction Equations and Previously Published Equations for Use in Other Youth Populations
| Measured MIP (cm H2O) | Hopi Predicteda MIP (cm H2O) | LLN (cm H2O) | Arnall Predictedb MIP (cm H2O) | Wilson Predictedc MIP (cm H2O) | Tomalak Predictedd MIP (cm H2O) | |
|---|---|---|---|---|---|---|
| Males | ||||||
| 4–5 yr (n = 4) | 46.0 (14.1) | 53.4 (5.6) | 22.3 | 52.1 (2.9) | 60.2 (3.4) | 34.5 (3.6) |
| 6–7 yr (n = 19) | 72.8 (16.7) | 70.4 (6.1) | 39.3 | 63.4 (2.6) | 65.3 (4.8) | 48.9 (3.3) |
| 8–9 yr (n = 44) | 82.5 (22.1) | 83.1 (6.6) | 52.05 | 73.6 (2.9) | 70.5 (7.1) | 61.8 (3.7) |
| 10–11 yr (n = 52) | 97.7 (19.7) | 96.0 (5.7) | 64.9 | 85.1 (2.9) | 76.4 (8.4) | 76.4 (3.7) |
| 12–13 yr (n = 6) | 96.3 (15.6) | 109.0 (5.4) | 78.0 | 95.3 (2.9) | 89.6 (11.6) | 89.5 (3.7) |
|
| ||||||
| Females | ||||||
| 4–5 yr (n = 5) | 50.0 (13.5) | 52.4 (1.4) | 19.3 | 54.5 (0.0) | 51.2 (0.7) | 37.8 (0.0) |
| 6–7 yr (n = 31) | 66.6 (15.1) | 62.3 (5.0) | 29.5 | 59.8 (1.4) | 55.4 (4.6) | 45.8 (2.2) |
| 8–9 yr (n = 65) | 69.8 (19.5) | 72.8 (4.1) | 39.7 | 65.8 (1.5) | 60.8 (7.2) | 54.9 (2.3) |
| 10–11 yr (n = 48) | 81.0 (23.2) | 80.3 (3.4) | 47.2 | 71.4 (1.6) | 65.1 (8.0) | 63.4 (2.4) |
| 12–13 yr (n = 14) | 91.3 (25.7) | 87.5 (2.2) | 54.4 | 76.2 (0.0) | 72.4 (9.4) | 70.7 (0.0) |
Actual and predicted values are mean (SD); Predictions using the equations from:
the present study (Table 2)
LLN = lower limit of the normal range (5th percentile).
Table 6.
Maximal Expiratory Pressure Predictions within Sex and across Age Groups in Hopi Youth Using the Derived Prediction Equations and Previously Published Equations for Use in Other Youth Populations
| Measured MEP (cm H2O) | Hopi Predicteda MEP (cm H2O) | LLN (cm H2O) | Arnall Predictedb MEP (cm H2O) | Wilson Predictedc MEP (cm H2O) | Tomalak Predictedd MEP (cm H2O) | |
|---|---|---|---|---|---|---|
| Males | ||||||
| 4–5 yr (n = 4) | 56.5 (8.7) | 56.8 (9.3) | 7.1 | 49.6 (2.8) | 61.1 (2.8) | 48.4 (2.4) |
| 6–7 yr (n = 19) | 81.6 (30.7) | 79.4 (9.1) | 29.7 | 60.1 (2.5) | 72.1 (2.5) | 58.0 (2.2) |
| 8–9 yr (n = 44) | 95.4 (31.1) | 95.7 (9.6) | 46.0 | 70.7 (2.8) | 81.9 (2.8) | 66.6 (2.4) |
| 10–11 yr (n = 52) | 114.4 (34.9) | 111.8 (8.3) | 62.1 | 82.0 (2.8) | 93.0 (2.8) | 76.4 (2.4) |
| 12–13 yr (n = 6) | 100.8 (23.8) | 128.6 (7.7) | 78.9 | 92.1 (2.9) | 102.8 (2.8) | 85.1 (2.5) |
|
| ||||||
| Females | ||||||
| 4–5 yr (n = 5) | 46.0 (10.2) | 52.8 (0.4) | 13.0 | 52.5 (0.0) | 48.0 (0.0) | 54.9 (0.0) |
| 6–7 yr (n = 31) | 66.7 (16.9) | 63.0 (2.8) | 23.2 | 57.8 (1.4) | 56.2 (2.2) | 59.8 (1.3) |
| 8–9 yr (n = 65) | 73.1 (23.0) | 74.1 (2.8) | 34.3 | 63.8 (1.5) | 65.5 (2.3) | 65.4 (1.4) |
| 10–11 yr (n = 48) | 82.9 (29.7) | 84.0 (2.7) | 44.2 | 69.4 (1.6) | 74.2 (2.4) | 70.6 (1.4) |
| 12–13 yr (n = 14) | 95.6 (28.5) | 92.7 (0.6) | 52.9 | 74.2 (0.0) | 81.6 (0.0) | 75.0 (0.0) |
Actual and predicted values are mean (SD); Predictions using the equations from:
the present study (Table 2)
LLN = lower limit of the normal range (5th percentile).
DISCUSSION
These results complement our previous studies of pulmonary function in healthy Navajo adolescents10, Navajo children9, Hopi children8 and maximal respiratory pressures in Navajo children.11 The current study of 288 Hopi children adds additional reference values for maximal respiratory pressures for Hopi children ages 4–13 years. Additionally, this sample size represents 36% of the Hopi children attending elementary school, and, therefore, represents a very large percentage of the total elementary school Hopi child population. Our sample size of Native Hopi children 4–13 years of age is significantly larger than the sample that Wilson et al.5 reported of a similar age range and very nearly equal to the sample size in the study by Tomalak et al.4 for that same age range. Thus, our sample is large enough to represent accurately a stable reference set of values for MRPs in Native Hopi children. Moreover, these equations for MIP and MEP are more accurate for the Hopi children than the equations published by either Wilson et al.5 or Tomalak et al.4 Thus, our findings suggest that these equations should be used instead of any other previously published equations for other groups of children since our equations are derived from the population of interest.
It should be noted that our findings are limited in that we did not use a large rubber mouthpiece pressed against the lips and teeth to achieve a better seal for MEP measurements as recommended by Black and Hyatt.15 Thus, we may have lower MEP values from our children when compared with studies using the Black and Hyatt15 technique. In addition, it should be noted that pressure is a surrogate for the determination of respiratory muscle force. As shown by Gaultier and Zinman18, force is the product of pressure and surface area over which the pressure is applied, hence, with a larger thoracic cage the pressure may be less while respiratory force is the same. Unfortunately, we did not measure chest size in this population, and we do not know if chest sizes differ between Caucasian, Navajo, and Hopi children. However, if the sitting/standing height ratios were smaller in Hopi children than in Caucasian and Navajo children, Hopi children would have a smaller thoracic cage. Therefore, if the Hopi children exerted equal muscle force, the pressures they generated would be lower when compared to the values in Caucasian and Navajo children. Differences in chest size may explain why the mean pressures for the Hopi children are higher than the pressures predicted by the prediction equations for Caucasian and Navajo children.
Our findings agree with those of Tomalak et al.4, and Gaultier and Zinman18 who all showed MRPs increased with age, and the males’ values were greater than the females’ values. Wilson et al.5 similarly found that increasing MEP values were greater in males than females with increasing age, but the MIP values for both males and females to be more closely related to body mass. Nevertheless, having the predictors of MRP differ amongst British Caucasian children5, Polish Caucasian children4, and Navajo children11 suggests that children’s pulmonary functions are influence by either geographic location, genetic heritage or a combination of the two. We propose that closely conserved genetic heritage plays an important factor. The Navajo and Hopi live in close proximity to each other, but they are genetically different. The Navajo are part of the Athabaskan group of native peoples, whilst the Hopi are part of the Puebloan (non-Athabaskan) group of native peoples. Moreover, these two groups have not significantly intermingled. Hence, it would appear that the MRP differences are genetic rather than geographic. Therefore, population specific reference equations are important because using reference values derived from other groups would be inaccurate.
In summary, we obtained demographic data as well as MIP and MEP values from a large number of Hopi Native American children attending elementary schools. Along with previous studies, our findings suggest that children’s pulmonary functions are population specific. Thus, the resultant prediction equations are new MRP references that should be used when testing Hopi children ages 4–13 years.
ACKNOWLEDGEMENTS
The authors wish to thank the Hopi Tribal Council, the Hopi Institutional Review Board, the Hopi Health Department, the Hopi Parent-Teacher groups at the elementary schools, the Principals of the Hopi Elementary Schools, and the Hopi parents and/or guardians for their willingness to allow us to conduct this study. We also want to thank all of the children who participated with such great enthusiasm in this study. Their excitement was contagious. We also wish to humbly thank our Native American Research Assistants, Verdell Kanuho of the Navajo Nation and Christina Interpreter of the Hopi Nation, for their tireless devotion to the gathering of this very important data set.
Funding Sources :
NIH, Numbers: R25-GM-56931, 3 SO6 GM-08215-12S1, Institute for Native Americans (INA) at Northern Arizona University, Flagstaff, AZ
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