Changes in the Contribution of the Rib Cage to Tidal Breathing during Infancy1-3
MARC B. HERSHENSON, ANDREW A. COLIN, MARY EllEN B. WOHl, and ANN R. STARK
Introduction
Because of its shape, high compliance, and deformability, the contribution of the rib cage to tidal breathing may be limited in newborns. First, the inspiratory action of the rib cage muscles depends on elevation of the ribs to a more horizontal position. In the newborn, the ribs are relatively horizontal at rest (1), limiting the potential increasein thoracic crosssectional area. Second, increments in rib cage volume may be limited by the high compliance of the newborn chest wall (2), which predisposes to inward movement of the rib cage during diaphragmatic contraction (3). Third, the deformability of the newborn rib cage may reduce mechanical coupling of the diaphragm and rib cage. Thus, passive outward movement of the lower rib cage by the diaphragm would not result in upper rib cage outward displacement. With growth and maturation, the resting orientation of the rib cage becomes more like that of the adult (1). Similarly, chest wall compliance decreases (4). Thus, one would expect the rib cage contribution to tidal volume to increase with age. To test this hypothesis, we used respiratory inductive plethysmography (RIP) to determine the relative contributions of the rib cage and abdomen to tidal volume in healthy infants and children during quiet sleep. Methods This study was approved by The Children's Hospital Human Subjects Committee. Subjects were studied after informed parental consent.
Subjects Fourteen healthy infants and children 1to 26 months of age were studied. Six children were studied on two occasions. Subjects were studied at home while asleep in the supine position. Recordings were made when the children were sleeping quietly and breathing regularly with no body movements, and therefore likely to be in quiet sleep (5). In the absence of electroencephalographic data, we consid-
922
SUMMARY As the shape, compliance, and deformabillty of the rib cage (RC) change during infanCI/, RC participation in quiet breathing may increase. We used respiratory inductive plethysmography (RIP) to determine the relative contributions of the RC and abdomen (AB) to tidal volume (VT) In 20 studies in 14 healthy infants 1 to 26 months of age during quiet natural sleep. RIP was calibrated with simultaneous flow measurements (anesthesia mask and pneumotachograph) by the least squares method of statistical analysis. We analyzed segments of breathing with and without flow measurement for RIP-derived VT, change in RC volume (Vre) and AB volume (Yab) with each breath and the RC contribution to tidal breathing (%RC = VrelVre + Yab). The %RC increased with age: %RC = 1.4 age (months) + 33 (r = 0.69, P < 0.01). After 9 months of age, %RC resembled that found in qUietly sleeping adolescents. Mask placement increased VT in all but one subject (mean increase,29 ± 23% of baseline ± SO; p < 0.001, paired f test). In infants younger than 10 months of age, mask placement also increased %RC (without mask, 40 ± 9%; With mask, 46 ± 10%; p < 0.02). We conclude that by 1 yr of age, the RC contribution to tidal breathing during quiet sleep is similar to that of the adolescent, suggesting that major developmental changes in RC shape, compliance, and deformabillty take place during infanCl/. AM REV RESPIR DIS 1990; 141:922-925
ered rib cage and abdominal asynchrony suggestive of active sleep, and excluded such periods from analysis. All children had a normal perinatal history and were receiving no medication at the time of examination. In all cases, data were not collected until at least 30 min after feeding.
Flow and Volume Measurements Flow measurements were obtained with an anesthesia mask (estimated dead space, 30 ml), an "0" Fleisch pneumotachograph (Fleisch, Lausanne, Switzerland) (estimated dead space, 3 ml), and a Validyne pressure transducer (Validyne Corp., Northridge, CA). Flow signals were amplified and integrated (Hewlett-Packard, Waltham, MA) to yield tidal volume (VT).
Rib Cage and Abdominal Wall Displacements Rib cage and abdominal wall displacements were measured by RIP (Respitrace", Noninvasive Monitoring Systems, Ardsley, NY). Rib cage bands were placed with the upper end of the band at the level of the axillae. Abdominal bands were placed at the level of the umbilicus, below the costal margin.
Experimental Protocol RIP data were obtained for an average of 22.8 ± 5.8 min (± SD). Shortly before the end of this period, simultaneous flow measurements were obtained with the mask and pneumotachograph (average duration suitable for analysis, 46 s) (see table 1 for individual data).
Data Collection and Analysis Chest wall displacement and flow signals were recorded on a Hewlett-Packard four-channel FM tape recorder and subsequently displayed on a polygraph. Polygraph records were analyzed for rib cage and abdominal wall displacements (RC and AB, respectively) in units of millimeters of pen displacement, VTin milliliters, and duration of respiratory cycle(not) in seconds. Only data from periods of quiet, regular breathing, presumably quiet sleep, were analyzed. Respiratory inductance plethysmography measurements were calibrated using a variation of the least squares method (figure 1) (6-8). Individual breaths from periods with simultaneous flow measurement were plotted on a coordinate system with the ratio AB/VT on the horizontal axis and RC/VT on the vertical axis. Next, breaths were selected
(Received in original form May 31, 1989 and in revised form September 14, 1989) 1 From the Departments of Anesthesia and Pediatrics, Harvard Medical School, and The Children's Hospital, Boston, Massachusetts. 2 Supported by Grants HL-07633 and HL-34616 from the National Heart, Lung, and Blood Institute and by The Children's Hospital Medical Center Anesthesia Foundation. J Correspondence and requests for reprints should be addressed to Marc B. Hershenson, M.D., The University of Chicago, Wyler Children's Hospital, 5825 S. Maryland Avenue, Box 307, Chicago, IL 60637.
923
RIB CAGE CONTRIBUTION TO BREATHING IN INFANTS
Fig. 1. Least-squares calibration of RIP data. Individual breaths (circles) were plotted on a ABNT, RCNT coordinate system. The closed square represents the calculated "average breath." Predominately rib cage and abdominal breaths selected for least squares analysis (dashed line) are represented by the closed circles (see text for complete selection criteria). Note that in this subject, the breath with the highest RCNT ratio was not selected for least squares analysis because it formed a positively sloped line with the average breath.
,,
0.190 0.185 0.180 0.175
Results
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,
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,
0.160 0.155 U lY
.
-, ,CO 0'
o
0.150
Individual data for OJoRC, VT, and Ttot are shown in table 1.
o
0
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0.170 0.165
o
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0',
,
o
•
0.145 subject J.R. ,, 0.140 +---1------1----+---+-----.:--+--------; 0.085 0.090 0.095 0.100 0.105 0.110 0.115
that were predominately "rib cage" or "abdominal" breaths; the least squares regression line representing these breaths was drawn, and the reciprocals of the x and y intercepts became the abdominal and rib cage calibration factors, respectively. Regression analysis was modified to minimize the perpendicular distance between each point and the regression line, thereby treating rib cage and abdominal displacements equally. Because reliable and unbiased selection of predominately "rib cage" and "abdominal" breaths can be difficult, we developed two criteria for the selection of s~ch breaths (figure 1): First, breaths selected for regression (AB/VT, RC/VT pairs) had to form a negatively sloped line with the calculated "average breath" (mean AB/mean VT, mean RCI mean VT).Individual breaths forming a positively sloped line with the average breath, i.e., breaths with RC/VT and ABD/VT ratios that were either both low or both high, presumably representing those in which the chest wall did not move with only two degrees of freedom, were eliminated from consideration. Second, of those breaths meeting the first criterion, the least squares analysis included only the following breaths: those with the smallest AB/VT, largest AB/VT, smallest RC/VT, and largest RC/VT. Hence, depending on the data, two to four breaths were selected for least squares regression per subject (for example, one breath may have both the-lowest AB/VT and highest RC/VT, decreasing the total number of breaths selected to three). With the calibration factors obtained, mean changes in rib cage (Vrc) and abdominal (Vab) volumes and the percent contribution of the rib cage to total tidal volume (Vrc/Vrc + Vab = OJoRC) were determined. Applying this technique, the average percent deviation between measured and calculated tidal volume was 7.2%, with 9.1% of the calculated breaths having a deviation from measured tidal volume of ~ 15%. The average correlation between measured and calculated tidal volume was 0.81 ± 0.14 (± SD). Using the calibration factors, we then determined Vrc, Vab, VT, and %RC for a section of quiet breathing (average length, 60 s) (see table 1 for individual data). In this way, estimates of %RC were obtained during an
•
ABD (mm)/Vt (ml)
uninstrumented, unstimulated state. In all but four studies, the data were obtained directly prior to application of the mask and pneumotachograph. In the remainder, data just prior to flow measurements were deemed unsuitable for analysis because oftransients such as sighs or body movements; in these instances, a section of data just following the flow measurements was selected. For pooled data, plots of age versus % RC (as determined during periods of RIP alone) and RIP-derived VTwithout mask versus RIPderived VT with mask were constructed. Group mean data were described as the mean ± SD. The effects of mask application on RIP-derived VTand %RC were analyzed with a paired t test. Regression coefficients were calculated as the square root of the ratio of the regression sum of squares to the total sum of squares, and were used to determine statistical significance (9).
Age-related Changes in %RC In subjects studied within the first 3 months oflife, %RC averaged 34 ± 9%, a percentage similar to that obtained in newborns during quiet sleep (8, 10).The rib cagecontribution to tidal volumethen increased with age: %RC = 1.4 age (months) + 33 (r = 0.69, p < 0.01) (figure 2). In subjects 9 months of age or older, mean %RC equaled 60 ± 17%, resembling that found in quietly sleeping adolescents and adults (II, 12). Mask-related Changes in Tidal Volume Mean RIP-derived VT during mask breathing was 29 ± 23% greater than that during breathing without the mask (p < 0.001,paired t test) (figure 3). These data agree with previous work demonstrating that the application of a face mask and pneumotachograph, or a face mask rim alone, increase VT (13, 14). Mask-related Changes in %RC In studies carried out in infants younger than 10 months of age (n = 14), mask placement was associated with a significant increase in %RC (without mask, 40 ± 9%; with mask, 46 ± 10%; p < 0.02).
TABLE 1 INDIVIDUAL DATA Subject No."
Age (months)
TRIP
Tmask (5)
DfoRCRIP
DfoRCmask
(%)
VTmask (m/)
Ttotmask
(%)
VTRIP (m/)
TtotRIP
(5)
(5)
(5)
1 2 3 4 5 6 7 8 9 1 (#2) 4 (#2) 9 (#2) 10 11 8 (#2) 3 (#2) 11 (#2) 12 13 14
1 1 2 2 3 3 4 4 5 6 7 8 8 9 13 15 16 17 24 26
42 60 62 50 40 44 90 32 42 48 64 80 60 42 80 132 84 56 40 42
38 54 36 34 42 34 36 32 70 44 70 52 36 36 54 70 36 38 52 46
45 30 33 44 20 33 31 50 33 36 40 54 51 45 45 75 35 80 66 61
57 39 39 34 35 32 51 57 36 56 47 56 55 55 47 81 37 76 75 56
33 18 23 31 17 47 40 29 85 25 40 66 50 44 84 101 49 82 84 100
44 24 38 38 20 37 51 43 87 35 69 102 63 53 92 122 76 96 100 103
2.2 1.7 1.2 2.5 2.1 2.3 2.0 1.8 2.2 2.7 1.9 2.8 2.5 2.6 2.9 3.5 2.5 3.0 3.0 3.1
2.0 1.6 1.1
1.7 1.6 1.9 1.8 1.6 1.9 2.6 1.8 .5 2.8 2.3 2.6 3.2 2.4 3.1 2.9 3.1
Definition of abbreviations: TRIP = duration of RIP data collection; Tmask = duration of testing period with mask; %RCRIP = % rib cage contribution during RIP alone; 0AlRDmask = % rib cage contribution during RIP and mask: VTRIP = tidal volume duro ing RIP alone; VTmask = tidal volume during RIP and mask; TtotRIP = duration of respiratory cycle during RIP alone; Ttotmask = duration of respiratory cycle during RIP and mask. • The (#2) notation beside a few subject numbers denotes the subject's second study.
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MARC B. HERSHENSON, ANDREW A. COLIN, MARY EllEN B. WOHl, and ANN R. STARK
Introduction
Because of its shape, high compliance, and deformability, the contribution of the rib cage to tidal breathing may be limited in newborns. First, the inspiratory action of the rib cage muscles depends on elevation of the ribs to a more horizontal position. In the newborn, the ribs are relatively horizontal at rest (1), limiting the potential increasein thoracic crosssectional area. Second, increments in rib cage volume may be limited by the high compliance of the newborn chest wall (2), which predisposes to inward movement of the rib cage during diaphragmatic contraction (3). Third, the deformability of the newborn rib cage may reduce mechanical coupling of the diaphragm and rib cage. Thus, passive outward movement of the lower rib cage by the diaphragm would not result in upper rib cage outward displacement. With growth and maturation, the resting orientation of the rib cage becomes more like that of the adult (1). Similarly, chest wall compliance decreases (4). Thus, one would expect the rib cage contribution to tidal volume to increase with age. To test this hypothesis, we used respiratory inductive plethysmography (RIP) to determine the relative contributions of the rib cage and abdomen to tidal volume in healthy infants and children during quiet sleep. Methods This study was approved by The Children's Hospital Human Subjects Committee. Subjects were studied after informed parental consent.
Subjects Fourteen healthy infants and children 1to 26 months of age were studied. Six children were studied on two occasions. Subjects were studied at home while asleep in the supine position. Recordings were made when the children were sleeping quietly and breathing regularly with no body movements, and therefore likely to be in quiet sleep (5). In the absence of electroencephalographic data, we consid-
922
SUMMARY As the shape, compliance, and deformabillty of the rib cage (RC) change during infanCI/, RC participation in quiet breathing may increase. We used respiratory inductive plethysmography (RIP) to determine the relative contributions of the RC and abdomen (AB) to tidal volume (VT) In 20 studies in 14 healthy infants 1 to 26 months of age during quiet natural sleep. RIP was calibrated with simultaneous flow measurements (anesthesia mask and pneumotachograph) by the least squares method of statistical analysis. We analyzed segments of breathing with and without flow measurement for RIP-derived VT, change in RC volume (Vre) and AB volume (Yab) with each breath and the RC contribution to tidal breathing (%RC = VrelVre + Yab). The %RC increased with age: %RC = 1.4 age (months) + 33 (r = 0.69, P < 0.01). After 9 months of age, %RC resembled that found in qUietly sleeping adolescents. Mask placement increased VT in all but one subject (mean increase,29 ± 23% of baseline ± SO; p < 0.001, paired f test). In infants younger than 10 months of age, mask placement also increased %RC (without mask, 40 ± 9%; With mask, 46 ± 10%; p < 0.02). We conclude that by 1 yr of age, the RC contribution to tidal breathing during quiet sleep is similar to that of the adolescent, suggesting that major developmental changes in RC shape, compliance, and deformabillty take place during infanCl/. AM REV RESPIR DIS 1990; 141:922-925
ered rib cage and abdominal asynchrony suggestive of active sleep, and excluded such periods from analysis. All children had a normal perinatal history and were receiving no medication at the time of examination. In all cases, data were not collected until at least 30 min after feeding.
Flow and Volume Measurements Flow measurements were obtained with an anesthesia mask (estimated dead space, 30 ml), an "0" Fleisch pneumotachograph (Fleisch, Lausanne, Switzerland) (estimated dead space, 3 ml), and a Validyne pressure transducer (Validyne Corp., Northridge, CA). Flow signals were amplified and integrated (Hewlett-Packard, Waltham, MA) to yield tidal volume (VT).
Rib Cage and Abdominal Wall Displacements Rib cage and abdominal wall displacements were measured by RIP (Respitrace", Noninvasive Monitoring Systems, Ardsley, NY). Rib cage bands were placed with the upper end of the band at the level of the axillae. Abdominal bands were placed at the level of the umbilicus, below the costal margin.
Experimental Protocol RIP data were obtained for an average of 22.8 ± 5.8 min (± SD). Shortly before the end of this period, simultaneous flow measurements were obtained with the mask and pneumotachograph (average duration suitable for analysis, 46 s) (see table 1 for individual data).
Data Collection and Analysis Chest wall displacement and flow signals were recorded on a Hewlett-Packard four-channel FM tape recorder and subsequently displayed on a polygraph. Polygraph records were analyzed for rib cage and abdominal wall displacements (RC and AB, respectively) in units of millimeters of pen displacement, VTin milliliters, and duration of respiratory cycle(not) in seconds. Only data from periods of quiet, regular breathing, presumably quiet sleep, were analyzed. Respiratory inductance plethysmography measurements were calibrated using a variation of the least squares method (figure 1) (6-8). Individual breaths from periods with simultaneous flow measurement were plotted on a coordinate system with the ratio AB/VT on the horizontal axis and RC/VT on the vertical axis. Next, breaths were selected
(Received in original form May 31, 1989 and in revised form September 14, 1989) 1 From the Departments of Anesthesia and Pediatrics, Harvard Medical School, and The Children's Hospital, Boston, Massachusetts. 2 Supported by Grants HL-07633 and HL-34616 from the National Heart, Lung, and Blood Institute and by The Children's Hospital Medical Center Anesthesia Foundation. J Correspondence and requests for reprints should be addressed to Marc B. Hershenson, M.D., The University of Chicago, Wyler Children's Hospital, 5825 S. Maryland Avenue, Box 307, Chicago, IL 60637.
923
RIB CAGE CONTRIBUTION TO BREATHING IN INFANTS
Fig. 1. Least-squares calibration of RIP data. Individual breaths (circles) were plotted on a ABNT, RCNT coordinate system. The closed square represents the calculated "average breath." Predominately rib cage and abdominal breaths selected for least squares analysis (dashed line) are represented by the closed circles (see text for complete selection criteria). Note that in this subject, the breath with the highest RCNT ratio was not selected for least squares analysis because it formed a positively sloped line with the average breath.
,,
0.190 0.185 0.180 0.175
Results
,,
,
• ,
,
0.160 0.155 U lY
.
-, ,CO 0'
o
0.150
Individual data for OJoRC, VT, and Ttot are shown in table 1.
o
0
"0
o
0.170 0.165
o
" , ,
o o o " , o 0
0',
,
o
•
0.145 subject J.R. ,, 0.140 +---1------1----+---+-----.:--+--------; 0.085 0.090 0.095 0.100 0.105 0.110 0.115
that were predominately "rib cage" or "abdominal" breaths; the least squares regression line representing these breaths was drawn, and the reciprocals of the x and y intercepts became the abdominal and rib cage calibration factors, respectively. Regression analysis was modified to minimize the perpendicular distance between each point and the regression line, thereby treating rib cage and abdominal displacements equally. Because reliable and unbiased selection of predominately "rib cage" and "abdominal" breaths can be difficult, we developed two criteria for the selection of s~ch breaths (figure 1): First, breaths selected for regression (AB/VT, RC/VT pairs) had to form a negatively sloped line with the calculated "average breath" (mean AB/mean VT, mean RCI mean VT).Individual breaths forming a positively sloped line with the average breath, i.e., breaths with RC/VT and ABD/VT ratios that were either both low or both high, presumably representing those in which the chest wall did not move with only two degrees of freedom, were eliminated from consideration. Second, of those breaths meeting the first criterion, the least squares analysis included only the following breaths: those with the smallest AB/VT, largest AB/VT, smallest RC/VT, and largest RC/VT. Hence, depending on the data, two to four breaths were selected for least squares regression per subject (for example, one breath may have both the-lowest AB/VT and highest RC/VT, decreasing the total number of breaths selected to three). With the calibration factors obtained, mean changes in rib cage (Vrc) and abdominal (Vab) volumes and the percent contribution of the rib cage to total tidal volume (Vrc/Vrc + Vab = OJoRC) were determined. Applying this technique, the average percent deviation between measured and calculated tidal volume was 7.2%, with 9.1% of the calculated breaths having a deviation from measured tidal volume of ~ 15%. The average correlation between measured and calculated tidal volume was 0.81 ± 0.14 (± SD). Using the calibration factors, we then determined Vrc, Vab, VT, and %RC for a section of quiet breathing (average length, 60 s) (see table 1 for individual data). In this way, estimates of %RC were obtained during an
•
ABD (mm)/Vt (ml)
uninstrumented, unstimulated state. In all but four studies, the data were obtained directly prior to application of the mask and pneumotachograph. In the remainder, data just prior to flow measurements were deemed unsuitable for analysis because oftransients such as sighs or body movements; in these instances, a section of data just following the flow measurements was selected. For pooled data, plots of age versus % RC (as determined during periods of RIP alone) and RIP-derived VTwithout mask versus RIPderived VT with mask were constructed. Group mean data were described as the mean ± SD. The effects of mask application on RIP-derived VTand %RC were analyzed with a paired t test. Regression coefficients were calculated as the square root of the ratio of the regression sum of squares to the total sum of squares, and were used to determine statistical significance (9).
Age-related Changes in %RC In subjects studied within the first 3 months oflife, %RC averaged 34 ± 9%, a percentage similar to that obtained in newborns during quiet sleep (8, 10).The rib cagecontribution to tidal volumethen increased with age: %RC = 1.4 age (months) + 33 (r = 0.69, p < 0.01) (figure 2). In subjects 9 months of age or older, mean %RC equaled 60 ± 17%, resembling that found in quietly sleeping adolescents and adults (II, 12). Mask-related Changes in Tidal Volume Mean RIP-derived VT during mask breathing was 29 ± 23% greater than that during breathing without the mask (p < 0.001,paired t test) (figure 3). These data agree with previous work demonstrating that the application of a face mask and pneumotachograph, or a face mask rim alone, increase VT (13, 14). Mask-related Changes in %RC In studies carried out in infants younger than 10 months of age (n = 14), mask placement was associated with a significant increase in %RC (without mask, 40 ± 9%; with mask, 46 ± 10%; p < 0.02).
TABLE 1 INDIVIDUAL DATA Subject No."
Age (months)
TRIP
Tmask (5)
DfoRCRIP
DfoRCmask
(%)
VTmask (m/)
Ttotmask
(%)
VTRIP (m/)
TtotRIP
(5)
(5)
(5)
1 2 3 4 5 6 7 8 9 1 (#2) 4 (#2) 9 (#2) 10 11 8 (#2) 3 (#2) 11 (#2) 12 13 14
1 1 2 2 3 3 4 4 5 6 7 8 8 9 13 15 16 17 24 26
42 60 62 50 40 44 90 32 42 48 64 80 60 42 80 132 84 56 40 42
38 54 36 34 42 34 36 32 70 44 70 52 36 36 54 70 36 38 52 46
45 30 33 44 20 33 31 50 33 36 40 54 51 45 45 75 35 80 66 61
57 39 39 34 35 32 51 57 36 56 47 56 55 55 47 81 37 76 75 56
33 18 23 31 17 47 40 29 85 25 40 66 50 44 84 101 49 82 84 100
44 24 38 38 20 37 51 43 87 35 69 102 63 53 92 122 76 96 100 103
2.2 1.7 1.2 2.5 2.1 2.3 2.0 1.8 2.2 2.7 1.9 2.8 2.5 2.6 2.9 3.5 2.5 3.0 3.0 3.1
2.0 1.6 1.1
1.7 1.6 1.9 1.8 1.6 1.9 2.6 1.8 .5 2.8 2.3 2.6 3.2 2.4 3.1 2.9 3.1
Definition of abbreviations: TRIP = duration of RIP data collection; Tmask = duration of testing period with mask; %RCRIP = % rib cage contribution during RIP alone; 0AlRDmask = % rib cage contribution during RIP and mask: VTRIP = tidal volume duro ing RIP alone; VTmask = tidal volume during RIP and mask; TtotRIP = duration of respiratory cycle during RIP alone; Ttotmask = duration of respiratory cycle during RIP and mask. • The (#2) notation beside a few subject numbers denotes the subject's second study.
924 z
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HERSHENSON. COLIN, WOHL. AND STARK
100
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C2 f-
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75
Z
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C2 f-
8
0 00
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