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Measurements of chest wall volume variation during tidal breathing in the supine and lateral positions in healthy subjects
Respiratory Physiology & Neurobiology 193 (2014) 38–42
Contents lists available at ScienceDirect
Respiratory Physiology & Neurobiology journal homepage: www.elsevier.com/locate/resphysiol
Measurements of chest wall volume variation during tidal breathing in the supine and lateral positions in healthy subjects Masafumi Nozoe a,∗ , Kyoshi Mase b , Sachie Takashima b , Kazuhiro Matsushita a , Yusuke Kouyama a , Hiromi Hashizume a , Yurina Kawasaki c , Yuki Uchiyama d , Noriyasu Yamamoto e , Yoshihiro Fukuda d , Kazuhisa Domen f a
Department of Rehabilitation, Hyogo College of Medicine Sasayama Medical Center, Kurooka 5, Sasayama, Hyogo, Japan Department of Physical Therapy, Faculty of Nursing and Rehabilitation, Konan Women’s University, Japan c Department of Rehabilitation, Konan Kakogawa Hospital, Japan d Department of General Medicine and Community Health Science, Hyogo College of Medicine, Japan e Department of Functional Regenerative Science, Hyogo College of Medicine, Japan f Department of Rehabilitation Medicine, Hyogo College of Medicine, Japan b
a r t i c l e
i n f o
Article history: Accepted 29 December 2013 Keywords: Chest wall volume Lateral position Optoelectronic plethysmography
a b s t r a c t Purpose: To study the feasibility and the laterality of measurements of chest wall volume variation during tidal breathing in the lateral position in healthy subjects. Methods: Eighteen normal subjects were studied. Chest wall volume changes were measured by optoelectronic plethysmography in the supine and right and left lateral positions during quiet breathing. The accuracy of measuring lung volume was also examined using hot wire spirometry in 10 of the subjects. Results: The measurement errors between lung volume changes and chest wall volume changes were not significantly different in all positions. There was no significant difference between right and left compartmental volume changes in the supine position. However, chest wall volume changes were lower on the dependent side in the lateral position than on the non-dependent side because of the decrease in abdominal rib cage and abdomen volume changes. Conclusion: Chest wall volume measurements during quiet breathing in the lateral position have high measuring accuracy and show laterality. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Turning onto the lateral position from the supine position is known to affect respiratory mechanics, such as the ratio of ventilation to perfusion, hemodynamics, and pulmonary gas exchange (Nelson and Anderson, 1989; Schellongowski et al., 2007; Verbanck et al., 1997; Frerichs et al., 2002). Particularly in regional ventilation, it has been reported that the regional distribution of tidal volume was higher in the dependent lung than in the non-dependent lung (Frerichs et al., 2002). Therefore, the ventilation on the dependent side lung is greater than that on the other side lung in the lateral position; that is, regional ventilation shows “laterality” in that position (Riedel et al., 2005). Optoelectronic plethysmography (OEP) has been used to measure total and compartmental chest wall volume changes during quiet breathing in several positions because it reflects lung volume
∗ Corresponding author. Tel.: +81 79 552 7381; fax: +81 79 552 7382. E-mail addresses: [email protected], [email protected] (M. Nozoe). 1569-9048/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.resp.2013.12.016
changes accurately, and it helps us to understand the chest wall mechanics that consist of the two-compartment rib cage [pulmonary rib cage (RCp), abdominal rib cage (RCa)] and abdomen (AB) model (Cala et al., 1996; Kenyon et al., 1997; Aliverti et al., 1997, 2000, 2001; Wang et al., 2009; Romei et al., 2010). Aliverti et al. (2001) studied the regional chest wall volume changes in the supine and prone positions in normal subjects. They reported that most of the chest wall volume change is distributed in the abdominal compartment both in the supine and prone positions, but it did not show laterality. Romei et al. (2010) studied it in several postures from seated to supine positions, and they reported that the chest wall kinematics were affected by position, with a progressive increase of the abdominal contribution to tidal volume. However, chest wall volume changes in the lateral position have not been reported. In the lateral position, total or compartmental chest wall volume changes during tidal breathing may differ between the two sides because regional ventilation shows laterality in that position. The purpose of this study was to develop and test the feasibility of measurements of chest wall volume variation during tidal breathing in the right and left lateral positions in healthy subjects. The aim was also to compare the laterality of chest wall volume
M. Nozoe et al. / Respiratory Physiology & Neurobiology 193 (2014) 38–42 Table 1 Subjects’ demographics and anthropometric parameters. Male Age (years) Weight (kg) Height (cm) BMI (kg/m2 )
27.3 66.8 176.2 21.5
Female ± ± ± ±
4.8 9.4 7.2 2.6
24.6 51.8 159.3 20.2
± ± ± ±
5.3 9.0** 8.6** 1.5
BMI: body mass index. All data are expressed as means ± SD. ** p < 0.01 vs. male.
changes in the supine and lateral positions. We hypothesized that the measuring accuracy is high not only in the supine position but also in the lateral positions, and that laterality of chest wall volume changes is seen in lateral positions but not in the supine position. 2. Methods 2.1. Subjects Eighteen normal subjects with normal pulmonary function (nine males, 27.3 ± 4.8 years old; nine females, 24.6 ± 5.3 years old) were studied. Table 1 shows the age and anthropometric data for all subjects. All subjects gave their written, informed consent in advance. All studies were approved by the Ethics Committee of Hyogo College of Medicine. 2.2. Measuring procedure Chest wall volume was measured by OEP methods using eight infrared cameras (Mac 3D System, Motion Analysis Corporation, San Diego, CA, USA). Passive markers made of thin reflective film on plastic spheres with diameters of 9 mm were used. The markers were fixed to the chest wall surface with each subject lying on the floor. The position of each marker was determined as described in a previous study (Cala et al., 1996) excluding the hidden part of the chest wall: 66 markers in the supine position excluding the back, and 81 markers in both lateral positions excluding the mid-axillary
39
line on the dependent side. In both lateral positions, each subject was asked to place his upper limb on a cushion over the greater trochanter to avoid hiding the markers on the mid-axillary line on the non-dependent side (Fig. 1). Before starting the measurements, all subjects were placed in each position (supine position, right lateral position, left lateral position). Then, measurements were taken for 2 min of quiet breathing in each position. All subjects performed the inspiratory capacity maneuver at the start and at the end during quiet breathing to correct “drift” caused by mechanical error (Johnson et al., 1999). The measurement positions were selected randomly. The coordinate data of all reflective markers were sampled at 100 Hz using analysis software (EVaRT5.04, Motion Analysis Corporation). Chest wall volume (VCW ), pulmonary rib cage volume (VRCp ), abdominal rib cage volume (VRCa ), and abdomen volume (VAB ) were then calculated using the positions of the chest wall markers (Nozoe et al., 2011). In particular, total and compartmental chest wall volumes were obtained by summing the volumes of a set of tetrahedrons using position vectors based on body surface marker coordinates. The present method differs from other methods based on Gauss’ theorem, which have been reported in several papers involving OEP (Cala et al., 1996; Kenyon et al., 1997; Aliverti et al., 1997, 2000, 2001). The method based on the Gauss’ theorem calculates the volume enclosed by a surface by calculating a surface integral and converting it into a volume integral. Therefore our tetrahedrons volume might be differ slightly from the volume calculated by the Gauss’ theorem. The measurements during the last 20 s in each position were analyzed, and total and compartmental tidal volume changes (VCW , VRCp , VRCa , VAB ) were calculated, as well as the volumes of the left and right sides separately. 2.3. Accuracy of volume measurements The accuracy of the lung volume measurements was evaluated using hot wire spirometry (AE300-s, Minato Medical Science, Tokyo, Japan) synchronized with OEP in 10 of the subjects (6 males; 23.8 ± 2.6 years old). Measurements taken during the last 20 s in each position were analyzed, and tidal volume (VSP ) was
Fig. 1. Marker positioning in the supine and right lateral positions (A, B) and computed models of the chest wall (C, D).
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M. Nozoe et al. / Respiratory Physiology & Neurobiology 193 (2014) 38–42
Table 2 Measurement accuracy, expressed as discrepancy.
VSP (ml) VCW (ml) Discrepancy (%)
3. Results
Supine (n = 51)
Right lateral (n = 49)
Left lateral (n = 54)
454 ± 81 457 ± 80 −0.5 ± 6.0
482 ± 88 476 ± 83 1.4 ± 8.1
461 ± 76 459 ± 83 1.0 ± 7.1
SP, spirometer; CW, chest wall; OEP, optoelectronic plethysmography; VSP , volume changes of the spirometery; VCW , volume changes of the total chest wall. All data are expressed as mean values ± SD, and n indicates the number of analyzed breaths.
calculated. The mean discrepancy reported as a percentage of the volume between VCW and VSP was calculated as described by Aliverti et al. (2001): Discrepancy (%) =
VSP − VCW × 100 VSP
2.4. Statistical analysis Data are presented as means ± standard deviation. Agreement between VCW and VSP was analyzed using Bland–Altman analysis in each position. The association between VCW and VSP was evaluated by linear regression. Comparisons of VSP , VCW , VRCp , VRCa , and VAB among all positions were performed using one-way ANOVA, with Bonferroni methods on a post hoc basis. Comparisons between right and left side volume changes were performed using the paired t-test. The level of significance was set at p < 0.05. All statistical procedures were performed using SPSS 15.0J for Windows statistical software (SPSS Inc., Chicago, IL, USA).
3.1. Measuring accuracy Overall, 51 breaths in the supine position, 49 breaths in the right lateral position, and 54 breaths in the left lateral position were analyzed. Table 2 shows VSP , VCW , and the discrepancy in each position. There were no significant differences in VSP , VCW , and discrepancy, and discrepancy was less than 2% in all positions. Fig. 2 shows the association between VCW and VSP and the Bland–Altman analysis results. Strong correlations were found in all positions (R2 = 0.8746, p < 0.01; R2 = 0.8076, p < 0.01; R2 = 0.8631, p < 0.01, respectively), and there were no adding errors and proportional errors in the Bland–Altman analyses. 3.2. Compartmental chest wall volume changes Overall, 86 breaths in the supine position, 89 breaths in the right lateral position, and 92 breaths in the left lateral position were analyzed. Table 3 shows the total and compartmental chest wall volume changes during quiet breathing. VCW , VRCp , and VAB did not differ among the positions, but VRCa was significantly decreased in both lateral positions compared to the supine position (both p < 0.01). 3.3. Laterality of chest wall volume changes There was no laterality in total and compartmental chest wall volume changes in the supine position. However, in the lateral
Fig. 2. Lung gas volume changes from spirometry (VSP ) compared to chest wall volume changes from optoelectronic plethysmography (VCW ). Top: linear regression analysis (A) supine position, (B) right lateral position, and (C) left lateral position. Bottom: Bland–Altman analysis (D) supine position, (E) right lateral position, and (F) left lateral position.
M. Nozoe et al. / Respiratory Physiology & Neurobiology 193 (2014) 38–42 Table 3 Compartmental chest wall volume changes measured by OEP.
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positions, the abdominal rib cage and abdomen volume changes were lower on the dependent side than on the non-dependent side during quiet breathing. As a result, chest wall volume changes in the lateral positions were lower on the dependent side than on the non-dependent side (Table 4). There were no differences in VCW , VRCp , and VAB on the right and left sides among different positions. Abdominal rib cage volume changes on the dependent side were lower in the lateral position than in the supine position (Table 4, both p < 0.01).
measurement accuracy in the supine position was better in the present study than in the previous report (Aliverti et al., 2001). We used many markers because we could measure the chest wall more extensively with a greater number of infrared cameras compared to the previous report (Aliverti et al., 2001, 4 cameras; present study, 8 cameras). On the other hand, chest wall volume changes in the lateral position measured by the OEP method have not been previously reported. It was possible to measure chest wall volume in the lateral position by having more infrared cameras. In the present study, since there were no significant differences in discrepancy among the three positions, the OEP method appears to have high accuracy for measuring chest wall volume in the lateral position. In order to explain the small discrepancies between the lung and the spirometer, other conditions (humidity, pressure, and temperature) must be considered. In order to correct ambient temperature, pressure saturated with water vapor (ATPS, 25 ◦ C) to body temperature, and pressure saturated with water vapor (BTPS) conditions, we should have applied a correction factor of about 1.07. This would have changed the %err from −0.5% to 6.0% in the supine position, 1.4% to 7.6% in the right lateral position, and 1.0% to 7.0% in the left lateral position.
4. Discussion
4.2. Compartmental and laterality of chest wall volume changes
The present results showed the feasibility of measuring chest wall volume variation during tidal breathing in the lateral position in healthy subjects, as well as the laterality of chest wall volume changes in the lateral position, which was related to the reduction in the abdominal rib cage and abdomen volume changes on the dependent side.
A few studies have examined the laterality or asymmetry of chest wall motion in several diseases or conditions using OEP (Aliverti et al., 2001; Lanini et al., 2003; De Groote et al., 2004; Boudarham et al., 2013). Aliverti et al. (2001) studied the chest wall volume changes in the supine and prone positions. They reported no laterality during quiet and deep breathing in both positions. Lanini et al. (2003) evaluated the differences in volumes between chest wall hemicompartments during quiet breathing, voluntary hyperventilation, and hypercapnic stimulation in patients with hemiparesis due to stroke. They also detected no asymmetry during quiet breathing. De Groote et al. (2004) assessed the expansion of the chest wall after lung transplantation due to emphysema. They found no differences between the native and transplanted sides during breathing. Boudarham et al. (2013) reported that patients with unilateral diaphragmatic weakness showed asymmetric ventilation measured by OEP. The present study is the first that showed laterality of chest wall volume changes in lateral positions. There are several reasons for this phenomenon. First, the chest wall on the dependent side was restricted by a rigid support. It is well known that the lower ribs expand laterally during inspiration even when the upper ribs move cranially (Saumarez, 1986). Therefore, the inspiratory motion of the abdominal rib cage on the dependent side might be restricted. Second, the abdominal pressure has a gradient, and it has been reported that the gradient changes with posture and body region
Supine (n = 86) VCW (ml) VRCp (ml) VRCa (ml) VAB (ml)
470 131 85 255
± ± ± ±
128 68 38 71
Right lateral (n = 89) 466 129 64 273
± ± ± ±
189 114 37** 82
Left lateral (n = 92) 454 125 61 267
± ± ± ±
208 126 34** 97
OEP, optoelectronic plethysmography; VCW , volume changes of the total chest wall; VRCp , volume changes of the pulmonary rib cage; VRCa , volume changes of the abdominal rib cage; VAB , volume changes of abdomen. All data are expressed as means ± SD. ** p < 0.01 vs. supine.
4.1. Measurement accuracy of chest wall volume changes Measurement accuracy of chest wall volume changes in normal subjects using OEP has been reported in several studies (Cala et al., 1996; Aliverti et al., 2000, 2001; Nozoe et al., 2011; Layton et al., 2013). Cala et al. (1996) reported measuring the accuracy in two normal subjects in the standing position. Aliverti et al. (2001) reported measuring the accuracy in the supine and prone positions, and they calculated discrepancy as in the present study. We also studied measurement accuracy in the standing position (Nozoe et al., 2011). Aliverti et al. (2001) found the discrepancy to be −4.2% ± 6.2% in the supine position and −1.7% ± 7.0% in the prone position. Their results were not much different from the present results (supine position −0.5% ± 6.0%, right lateral position 1.4% ± 8.1%, left lateral position 1.0% ± 7.1%). The only difference between the present method and their method is the number of reflective markers placed on the chest wall surface (Aliverti et al., 2001, 45 markers; present study, 66 markers). As a result, Table 4 The volume changes of each compartment (right and left) measured by OEP. Supine
VCW (ml) VRCp (ml) VRCa (ml) VAB (ml)
Right lateral
Left lateral
Right side
Left side
Right side
Left side
234 ± 58 66 ± 33 42 ± 18 126 ± 34
236 ± 72 65 ± 37 42 ± 21 129 ± 40
223 ± 93 66 ± 54 27 ± 16†† 131 ± 47
243 ± 99 64 ± 61 37 ± 24** 142 ± 41** **
Right side
Left side
237 ± 105 62 ± 62 37 ± 22 139 ± 56
216 ± 109** 63 ± 65 25 ± 13** , ‡‡ 129 ± 52*
OEP, optoelectronic plethysmography; VCW , volume changes of the total chest wall; VRCp , volume changes of the pulmonary rib cage; VRCa , volume changes of the abdominal rib cage; VAB , volume changes of abdomen. All data are expressed as means ± SD. * p < 0.05 vs. right side. ** p < 0.01 vs. right side. †† p < 0.01 vs. supine and left lateral. ‡‡ p < 0.01 vs. supine and right lateral.
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M. Nozoe et al. / Respiratory Physiology & Neurobiology 193 (2014) 38–42
(De Waele et al., 2008; De Keulenaer et al., 2009). Particularly in the lateral position, abdominal pressure on the dependent side could be higher than on the nondependent side. As a result, it might decrease the compliance of that region and restrict expansion. However, many studies have reported an increase in regional lung ventilation on the dependent side with various methods (Verbanck et al., 1997; Frerichs et al., 2002; Riedel et al., 2005). Therefore, we considered the possibility that there was a ‘discrepancy’ between regional ventilation and regional chest wall motion in the lateral position. Why does such a paradoxical phenomenon occur? We considered two reasons. First, mediastinal motion could be changed in the lateral position. It has been reported that the mediastinum moves toward the midsagittal plane when it is shifted laterally (De Groote et al., 2004). It is well known that the mediastinum shifts toward the dependent side in the lateral position, so that chest wall expansion on the dependent side did not increase because the mediastinum moved toward the nondependent side during inspiration. Second, the lung is moving freely within the thoracic cavity. When the chest wall compartment is constrained mechanically, the volume changes in that region of the lung will by necessity be reflected in changes in another compartment as the lung expands (Aliverti et al., 2001). Therefore, the present results about chest wall expansion might not be related to lung ventilation. 4.3. Clinical implication Turning into the lateral position from the supine position is often used in critically ill patients. However, the mechanics of the chest wall in the lateral position have not been studied. Combined with pressure measurements, the present results will help us understand these mechanics because the measurement accuracy was shown in lateral positions. Moreover, the present results will also be fundamental data when examining chest wall volumes in such patients in lateral positions. 4.4. Limitations of the study Compartmental chest wall volume changes were examined during quiet breathing in the lateral recumbent position, which have never been reported previously. However, the subjects were instructed to put their non-dependent side arm on a cushion on the greater trochanter to avoid hiding the markers on the mid-axillary line on the non-dependent side. Patients are not likely to ever lie in such a position, as they would usually have their arms in front of their torso. The difference in arm position may have affected the results. Second, measurements were taken with the subjects on the floor, not on a bed, in order to detect chest wall motion accurately in the region near the floor. However, Aliverti et al. (2000, 2001) took their measurements with the subjects on a bed in an ICU setting so as to be able to apply their results to patients, and they also measured the effects of differences in mattress hardness (Aliverti et al., 2001). The methods used in the present study need to be applied to subjects on mattresses to be able to generalize the results to the clinical setting. Third, pleural and abdominal pressure changes and distribution, regional lung volume, and diaphragm movement need to be examined simultaneously to confirm the present results. There are also limitations to the present study because only regional chest wall volume changes were measured during quiet breathing.
5. Conclusion The feasibility and the laterality of measurements of chest wall volume variation during tidal breathing were studied in the lateral position in healthy subjects. The findings demonstrated high measurement accuracy and the laterality of chest wall volume changes, which was related to the reduction in abdominal rib cage and abdomen volume changes on the dependent side in the lateral position. References Aliverti, A., Cala, S.J., Duranti, R., Ferrigno, G., Kenyon, C.M., Pedotti, A., Scano, G., Sliwinski, P., Macklem, P.T., Yan, S., 1997. Human respiratory muscle actions and control during exercise. J. Appl. Physiol. 83, 1256–1269. Aliverti, A., Dellacá, R., Pelosi, P., Chiumello, D., Pedotti, A., Gattinoni, L., 2000. Optoelectronic plethysmography in intensive care patients. Am. J. Respir. Crit. Care Med. 161, 1546–1552. Aliverti, A., Dellacà, R., Pelosi, P., Chiumello, D., Gatihnoni, L., Pedoti, A., 2001. Compartmental analysis of breathing in the supine and prone positions by optoelectronic plethysmography. Ann. Biomed. Eng. 29, 60–70. Boudarham, J., Pradon, D., Prigent, H., Falaize, L., Durand, M.C., Meric, H., Petitjean, M., Lofaso, F., 2013. Optoelectronic plethysmography as an alternative method for the diagnosis of unilateral diaphragmatic weakness. Chest 144, 887–895. Cala, S.J., Kenyon, C.M., Ferrigno, G., Carnevali, P., Aliverti, A., Pedotti, A., Macklem, P.T., Rochester, D.F., 1996. Chest wall and lung volume estimation by optical reflectance motion analysis. J. Appl. Physiol. 81, 2680–2689. De Groote, A., Van Muylem, A., Scillia, P., Cheron, G., Verleden, G., Paiva, M., Estenne, M., 2004. Ventilation asymmetry after transplantation for emphysema: role of chest wall and mediastinum. Am. J. Respir. Crit. Care Med. 170, 1233–1238. De Keulenaer, B.L., De Waele, J.J., Powell, B., Malbrain, M.L., 2009. What is normal intra-abdominal pressure and how is it affected by positioning, body mass and positive end-expiratory pressure? Intensive Care Med. 35, 969–976. De Waele, J.J., De Laet, I., De Keulenaer, B., Widder, S., Kirkpatrick, A.W., Cresswell, A.B., Malbrain, M., Bodnar, Z., Mejia-Mantilla, J.H., Reis, R., Parr, M., Schulze, R., Compano, S., Cheatham, M., 2008. The effect of different reference transducer positions on intra-abdominal pressure measurement: a multicenter analysis. Intensive Care Med. 34, 1299–1303. Frerichs, I., Hinz, J., Herrmann, P., Weisser, G., Hahn, G., Dudykevych, T., Quintel, M., Hellige, G., 2002. Detection of local lung air content by electrical impedance tomography compared with electron beam CT. J. Appl. Physiol. 93, 660–666. Johnson, B.D., Weisman, I.M., Zeballos, R.J., Beck, K.C., 1999. Emerging concepts in the evaluation of ventilatory limitation during exercise: the exercise tidal flowvolume loop. Chest 116, 488–503. Kenyon, C.M., Cala, S.J., Yan, S., Aliverti, A., Scano, G., Duranti, R., Pedotti, A., Macklem, P.T., 1997. Rib cage mechanics during quiet breathing and exercise in humans. J. Appl. Physiol. 83, 1242–1255. Lanini, B., Bianchi, R., Romagnoli, I., Coli, C., Binazzi, B., Gigliotti, F., Pizzi, A., Grippo, A., Scano, G., 2003. Chest wall kinematics in patients with hemiplegia. Am. J. Respir. Crit. Care Med. 168, 109–113. Layton, A.M., Moran, S.L., Garber, C.E., Armstrong, H.F., Basner, R.C., Thomashow, B.M., Bartels, M.N., 2013. Optoelectronic plethysmography compared to spirometry during maximal exercise. Respir. Physiol. Neurobiol. 185, 362–368. Nelson, L.D., Anderson, H.B., 1989. Physiologic effects of steep positioning in the surgical intensive care unit. Arch. Surg. 124, 352–355. Nozoe, M., Mase, K., Tsutou, A., 2011. Regional chest wall volume changes during various breathing maneuvers. J. Jpn. Phys. Ther. Assoc. 14, 12–18. Riedel, T., Richards, T., Schibler, A., 2005. The value of electrical impedance tomography in assessing the effect of body position and positive airway pressures on regional lung ventilation in spontaneously breathing subjects. Intensive Care Med. 31, 1522–1528. Romei, M., Mauro, A.L., D’Angelo, M.G., Turconi, A.C., Bresolin, N., Pedotti, A., Aliverti, A., 2010. Effects of gender and posture on thoraco-abdominal kinematics during quiet breathing in healthy adults. Respir. Physiol. Neurobiol. 172, 184–191. Saumarez, R.C., 1986. An analysis of possible movements of human upper rib cage. J Appl Physiol. 60, 678–689. Schellongowski, P., Losert, H., Locker, G.J., Laczika, K., Frass, M., Holzinger, U., Bojic, A., Staudinger, T., 2007. Prolonged lateral steep position impairs respiratory mechanics during continuous lateral rotation therapy in respiratory failure. Intensive Care Med. 33, 625–631. Verbanck, S., Schuermans, D., Van Muylem, A., Paiva, M., Noppen, M., Vincken, W., 1997. Ventilation distribution during histamine provocation. J. Appl. Physiol. 83, 1907–1916. Wang, H.K., Lu, T.W., Liing, R.J., Shih, T.T., Chen, S.C., Lin, K.H., 2009. Relationship between chest wall motion and diaphragmatic excursion in healthy adults in supine position. J. Formos. Med. Assoc. 108, 577–586.
Contents lists available at ScienceDirect
Respiratory Physiology & Neurobiology journal homepage: www.elsevier.com/locate/resphysiol
Measurements of chest wall volume variation during tidal breathing in the supine and lateral positions in healthy subjects Masafumi Nozoe a,∗ , Kyoshi Mase b , Sachie Takashima b , Kazuhiro Matsushita a , Yusuke Kouyama a , Hiromi Hashizume a , Yurina Kawasaki c , Yuki Uchiyama d , Noriyasu Yamamoto e , Yoshihiro Fukuda d , Kazuhisa Domen f a
Department of Rehabilitation, Hyogo College of Medicine Sasayama Medical Center, Kurooka 5, Sasayama, Hyogo, Japan Department of Physical Therapy, Faculty of Nursing and Rehabilitation, Konan Women’s University, Japan c Department of Rehabilitation, Konan Kakogawa Hospital, Japan d Department of General Medicine and Community Health Science, Hyogo College of Medicine, Japan e Department of Functional Regenerative Science, Hyogo College of Medicine, Japan f Department of Rehabilitation Medicine, Hyogo College of Medicine, Japan b
a r t i c l e
i n f o
Article history: Accepted 29 December 2013 Keywords: Chest wall volume Lateral position Optoelectronic plethysmography
a b s t r a c t Purpose: To study the feasibility and the laterality of measurements of chest wall volume variation during tidal breathing in the lateral position in healthy subjects. Methods: Eighteen normal subjects were studied. Chest wall volume changes were measured by optoelectronic plethysmography in the supine and right and left lateral positions during quiet breathing. The accuracy of measuring lung volume was also examined using hot wire spirometry in 10 of the subjects. Results: The measurement errors between lung volume changes and chest wall volume changes were not significantly different in all positions. There was no significant difference between right and left compartmental volume changes in the supine position. However, chest wall volume changes were lower on the dependent side in the lateral position than on the non-dependent side because of the decrease in abdominal rib cage and abdomen volume changes. Conclusion: Chest wall volume measurements during quiet breathing in the lateral position have high measuring accuracy and show laterality. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Turning onto the lateral position from the supine position is known to affect respiratory mechanics, such as the ratio of ventilation to perfusion, hemodynamics, and pulmonary gas exchange (Nelson and Anderson, 1989; Schellongowski et al., 2007; Verbanck et al., 1997; Frerichs et al., 2002). Particularly in regional ventilation, it has been reported that the regional distribution of tidal volume was higher in the dependent lung than in the non-dependent lung (Frerichs et al., 2002). Therefore, the ventilation on the dependent side lung is greater than that on the other side lung in the lateral position; that is, regional ventilation shows “laterality” in that position (Riedel et al., 2005). Optoelectronic plethysmography (OEP) has been used to measure total and compartmental chest wall volume changes during quiet breathing in several positions because it reflects lung volume
∗ Corresponding author. Tel.: +81 79 552 7381; fax: +81 79 552 7382. E-mail addresses: [email protected], [email protected] (M. Nozoe). 1569-9048/$ – see front matter © 2014 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.resp.2013.12.016
changes accurately, and it helps us to understand the chest wall mechanics that consist of the two-compartment rib cage [pulmonary rib cage (RCp), abdominal rib cage (RCa)] and abdomen (AB) model (Cala et al., 1996; Kenyon et al., 1997; Aliverti et al., 1997, 2000, 2001; Wang et al., 2009; Romei et al., 2010). Aliverti et al. (2001) studied the regional chest wall volume changes in the supine and prone positions in normal subjects. They reported that most of the chest wall volume change is distributed in the abdominal compartment both in the supine and prone positions, but it did not show laterality. Romei et al. (2010) studied it in several postures from seated to supine positions, and they reported that the chest wall kinematics were affected by position, with a progressive increase of the abdominal contribution to tidal volume. However, chest wall volume changes in the lateral position have not been reported. In the lateral position, total or compartmental chest wall volume changes during tidal breathing may differ between the two sides because regional ventilation shows laterality in that position. The purpose of this study was to develop and test the feasibility of measurements of chest wall volume variation during tidal breathing in the right and left lateral positions in healthy subjects. The aim was also to compare the laterality of chest wall volume
M. Nozoe et al. / Respiratory Physiology & Neurobiology 193 (2014) 38–42 Table 1 Subjects’ demographics and anthropometric parameters. Male Age (years) Weight (kg) Height (cm) BMI (kg/m2 )
27.3 66.8 176.2 21.5
Female ± ± ± ±
4.8 9.4 7.2 2.6
24.6 51.8 159.3 20.2
± ± ± ±
5.3 9.0** 8.6** 1.5
BMI: body mass index. All data are expressed as means ± SD. ** p < 0.01 vs. male.
changes in the supine and lateral positions. We hypothesized that the measuring accuracy is high not only in the supine position but also in the lateral positions, and that laterality of chest wall volume changes is seen in lateral positions but not in the supine position. 2. Methods 2.1. Subjects Eighteen normal subjects with normal pulmonary function (nine males, 27.3 ± 4.8 years old; nine females, 24.6 ± 5.3 years old) were studied. Table 1 shows the age and anthropometric data for all subjects. All subjects gave their written, informed consent in advance. All studies were approved by the Ethics Committee of Hyogo College of Medicine. 2.2. Measuring procedure Chest wall volume was measured by OEP methods using eight infrared cameras (Mac 3D System, Motion Analysis Corporation, San Diego, CA, USA). Passive markers made of thin reflective film on plastic spheres with diameters of 9 mm were used. The markers were fixed to the chest wall surface with each subject lying on the floor. The position of each marker was determined as described in a previous study (Cala et al., 1996) excluding the hidden part of the chest wall: 66 markers in the supine position excluding the back, and 81 markers in both lateral positions excluding the mid-axillary
39
line on the dependent side. In both lateral positions, each subject was asked to place his upper limb on a cushion over the greater trochanter to avoid hiding the markers on the mid-axillary line on the non-dependent side (Fig. 1). Before starting the measurements, all subjects were placed in each position (supine position, right lateral position, left lateral position). Then, measurements were taken for 2 min of quiet breathing in each position. All subjects performed the inspiratory capacity maneuver at the start and at the end during quiet breathing to correct “drift” caused by mechanical error (Johnson et al., 1999). The measurement positions were selected randomly. The coordinate data of all reflective markers were sampled at 100 Hz using analysis software (EVaRT5.04, Motion Analysis Corporation). Chest wall volume (VCW ), pulmonary rib cage volume (VRCp ), abdominal rib cage volume (VRCa ), and abdomen volume (VAB ) were then calculated using the positions of the chest wall markers (Nozoe et al., 2011). In particular, total and compartmental chest wall volumes were obtained by summing the volumes of a set of tetrahedrons using position vectors based on body surface marker coordinates. The present method differs from other methods based on Gauss’ theorem, which have been reported in several papers involving OEP (Cala et al., 1996; Kenyon et al., 1997; Aliverti et al., 1997, 2000, 2001). The method based on the Gauss’ theorem calculates the volume enclosed by a surface by calculating a surface integral and converting it into a volume integral. Therefore our tetrahedrons volume might be differ slightly from the volume calculated by the Gauss’ theorem. The measurements during the last 20 s in each position were analyzed, and total and compartmental tidal volume changes (VCW , VRCp , VRCa , VAB ) were calculated, as well as the volumes of the left and right sides separately. 2.3. Accuracy of volume measurements The accuracy of the lung volume measurements was evaluated using hot wire spirometry (AE300-s, Minato Medical Science, Tokyo, Japan) synchronized with OEP in 10 of the subjects (6 males; 23.8 ± 2.6 years old). Measurements taken during the last 20 s in each position were analyzed, and tidal volume (VSP ) was
Fig. 1. Marker positioning in the supine and right lateral positions (A, B) and computed models of the chest wall (C, D).
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Table 2 Measurement accuracy, expressed as discrepancy.
VSP (ml) VCW (ml) Discrepancy (%)
3. Results
Supine (n = 51)
Right lateral (n = 49)
Left lateral (n = 54)
454 ± 81 457 ± 80 −0.5 ± 6.0
482 ± 88 476 ± 83 1.4 ± 8.1
461 ± 76 459 ± 83 1.0 ± 7.1
SP, spirometer; CW, chest wall; OEP, optoelectronic plethysmography; VSP , volume changes of the spirometery; VCW , volume changes of the total chest wall. All data are expressed as mean values ± SD, and n indicates the number of analyzed breaths.
calculated. The mean discrepancy reported as a percentage of the volume between VCW and VSP was calculated as described by Aliverti et al. (2001): Discrepancy (%) =
VSP − VCW × 100 VSP
2.4. Statistical analysis Data are presented as means ± standard deviation. Agreement between VCW and VSP was analyzed using Bland–Altman analysis in each position. The association between VCW and VSP was evaluated by linear regression. Comparisons of VSP , VCW , VRCp , VRCa , and VAB among all positions were performed using one-way ANOVA, with Bonferroni methods on a post hoc basis. Comparisons between right and left side volume changes were performed using the paired t-test. The level of significance was set at p < 0.05. All statistical procedures were performed using SPSS 15.0J for Windows statistical software (SPSS Inc., Chicago, IL, USA).
3.1. Measuring accuracy Overall, 51 breaths in the supine position, 49 breaths in the right lateral position, and 54 breaths in the left lateral position were analyzed. Table 2 shows VSP , VCW , and the discrepancy in each position. There were no significant differences in VSP , VCW , and discrepancy, and discrepancy was less than 2% in all positions. Fig. 2 shows the association between VCW and VSP and the Bland–Altman analysis results. Strong correlations were found in all positions (R2 = 0.8746, p < 0.01; R2 = 0.8076, p < 0.01; R2 = 0.8631, p < 0.01, respectively), and there were no adding errors and proportional errors in the Bland–Altman analyses. 3.2. Compartmental chest wall volume changes Overall, 86 breaths in the supine position, 89 breaths in the right lateral position, and 92 breaths in the left lateral position were analyzed. Table 3 shows the total and compartmental chest wall volume changes during quiet breathing. VCW , VRCp , and VAB did not differ among the positions, but VRCa was significantly decreased in both lateral positions compared to the supine position (both p < 0.01). 3.3. Laterality of chest wall volume changes There was no laterality in total and compartmental chest wall volume changes in the supine position. However, in the lateral
Fig. 2. Lung gas volume changes from spirometry (VSP ) compared to chest wall volume changes from optoelectronic plethysmography (VCW ). Top: linear regression analysis (A) supine position, (B) right lateral position, and (C) left lateral position. Bottom: Bland–Altman analysis (D) supine position, (E) right lateral position, and (F) left lateral position.
M. Nozoe et al. / Respiratory Physiology & Neurobiology 193 (2014) 38–42 Table 3 Compartmental chest wall volume changes measured by OEP.
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positions, the abdominal rib cage and abdomen volume changes were lower on the dependent side than on the non-dependent side during quiet breathing. As a result, chest wall volume changes in the lateral positions were lower on the dependent side than on the non-dependent side (Table 4). There were no differences in VCW , VRCp , and VAB on the right and left sides among different positions. Abdominal rib cage volume changes on the dependent side were lower in the lateral position than in the supine position (Table 4, both p < 0.01).
measurement accuracy in the supine position was better in the present study than in the previous report (Aliverti et al., 2001). We used many markers because we could measure the chest wall more extensively with a greater number of infrared cameras compared to the previous report (Aliverti et al., 2001, 4 cameras; present study, 8 cameras). On the other hand, chest wall volume changes in the lateral position measured by the OEP method have not been previously reported. It was possible to measure chest wall volume in the lateral position by having more infrared cameras. In the present study, since there were no significant differences in discrepancy among the three positions, the OEP method appears to have high accuracy for measuring chest wall volume in the lateral position. In order to explain the small discrepancies between the lung and the spirometer, other conditions (humidity, pressure, and temperature) must be considered. In order to correct ambient temperature, pressure saturated with water vapor (ATPS, 25 ◦ C) to body temperature, and pressure saturated with water vapor (BTPS) conditions, we should have applied a correction factor of about 1.07. This would have changed the %err from −0.5% to 6.0% in the supine position, 1.4% to 7.6% in the right lateral position, and 1.0% to 7.0% in the left lateral position.
4. Discussion
4.2. Compartmental and laterality of chest wall volume changes
The present results showed the feasibility of measuring chest wall volume variation during tidal breathing in the lateral position in healthy subjects, as well as the laterality of chest wall volume changes in the lateral position, which was related to the reduction in the abdominal rib cage and abdomen volume changes on the dependent side.
A few studies have examined the laterality or asymmetry of chest wall motion in several diseases or conditions using OEP (Aliverti et al., 2001; Lanini et al., 2003; De Groote et al., 2004; Boudarham et al., 2013). Aliverti et al. (2001) studied the chest wall volume changes in the supine and prone positions. They reported no laterality during quiet and deep breathing in both positions. Lanini et al. (2003) evaluated the differences in volumes between chest wall hemicompartments during quiet breathing, voluntary hyperventilation, and hypercapnic stimulation in patients with hemiparesis due to stroke. They also detected no asymmetry during quiet breathing. De Groote et al. (2004) assessed the expansion of the chest wall after lung transplantation due to emphysema. They found no differences between the native and transplanted sides during breathing. Boudarham et al. (2013) reported that patients with unilateral diaphragmatic weakness showed asymmetric ventilation measured by OEP. The present study is the first that showed laterality of chest wall volume changes in lateral positions. There are several reasons for this phenomenon. First, the chest wall on the dependent side was restricted by a rigid support. It is well known that the lower ribs expand laterally during inspiration even when the upper ribs move cranially (Saumarez, 1986). Therefore, the inspiratory motion of the abdominal rib cage on the dependent side might be restricted. Second, the abdominal pressure has a gradient, and it has been reported that the gradient changes with posture and body region
Supine (n = 86) VCW (ml) VRCp (ml) VRCa (ml) VAB (ml)
470 131 85 255
± ± ± ±
128 68 38 71
Right lateral (n = 89) 466 129 64 273
± ± ± ±
189 114 37** 82
Left lateral (n = 92) 454 125 61 267
± ± ± ±
208 126 34** 97
OEP, optoelectronic plethysmography; VCW , volume changes of the total chest wall; VRCp , volume changes of the pulmonary rib cage; VRCa , volume changes of the abdominal rib cage; VAB , volume changes of abdomen. All data are expressed as means ± SD. ** p < 0.01 vs. supine.
4.1. Measurement accuracy of chest wall volume changes Measurement accuracy of chest wall volume changes in normal subjects using OEP has been reported in several studies (Cala et al., 1996; Aliverti et al., 2000, 2001; Nozoe et al., 2011; Layton et al., 2013). Cala et al. (1996) reported measuring the accuracy in two normal subjects in the standing position. Aliverti et al. (2001) reported measuring the accuracy in the supine and prone positions, and they calculated discrepancy as in the present study. We also studied measurement accuracy in the standing position (Nozoe et al., 2011). Aliverti et al. (2001) found the discrepancy to be −4.2% ± 6.2% in the supine position and −1.7% ± 7.0% in the prone position. Their results were not much different from the present results (supine position −0.5% ± 6.0%, right lateral position 1.4% ± 8.1%, left lateral position 1.0% ± 7.1%). The only difference between the present method and their method is the number of reflective markers placed on the chest wall surface (Aliverti et al., 2001, 45 markers; present study, 66 markers). As a result, Table 4 The volume changes of each compartment (right and left) measured by OEP. Supine
VCW (ml) VRCp (ml) VRCa (ml) VAB (ml)
Right lateral
Left lateral
Right side
Left side
Right side
Left side
234 ± 58 66 ± 33 42 ± 18 126 ± 34
236 ± 72 65 ± 37 42 ± 21 129 ± 40
223 ± 93 66 ± 54 27 ± 16†† 131 ± 47
243 ± 99 64 ± 61 37 ± 24** 142 ± 41** **
Right side
Left side
237 ± 105 62 ± 62 37 ± 22 139 ± 56
216 ± 109** 63 ± 65 25 ± 13** , ‡‡ 129 ± 52*
OEP, optoelectronic plethysmography; VCW , volume changes of the total chest wall; VRCp , volume changes of the pulmonary rib cage; VRCa , volume changes of the abdominal rib cage; VAB , volume changes of abdomen. All data are expressed as means ± SD. * p < 0.05 vs. right side. ** p < 0.01 vs. right side. †† p < 0.01 vs. supine and left lateral. ‡‡ p < 0.01 vs. supine and right lateral.
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(De Waele et al., 2008; De Keulenaer et al., 2009). Particularly in the lateral position, abdominal pressure on the dependent side could be higher than on the nondependent side. As a result, it might decrease the compliance of that region and restrict expansion. However, many studies have reported an increase in regional lung ventilation on the dependent side with various methods (Verbanck et al., 1997; Frerichs et al., 2002; Riedel et al., 2005). Therefore, we considered the possibility that there was a ‘discrepancy’ between regional ventilation and regional chest wall motion in the lateral position. Why does such a paradoxical phenomenon occur? We considered two reasons. First, mediastinal motion could be changed in the lateral position. It has been reported that the mediastinum moves toward the midsagittal plane when it is shifted laterally (De Groote et al., 2004). It is well known that the mediastinum shifts toward the dependent side in the lateral position, so that chest wall expansion on the dependent side did not increase because the mediastinum moved toward the nondependent side during inspiration. Second, the lung is moving freely within the thoracic cavity. When the chest wall compartment is constrained mechanically, the volume changes in that region of the lung will by necessity be reflected in changes in another compartment as the lung expands (Aliverti et al., 2001). Therefore, the present results about chest wall expansion might not be related to lung ventilation. 4.3. Clinical implication Turning into the lateral position from the supine position is often used in critically ill patients. However, the mechanics of the chest wall in the lateral position have not been studied. Combined with pressure measurements, the present results will help us understand these mechanics because the measurement accuracy was shown in lateral positions. Moreover, the present results will also be fundamental data when examining chest wall volumes in such patients in lateral positions. 4.4. Limitations of the study Compartmental chest wall volume changes were examined during quiet breathing in the lateral recumbent position, which have never been reported previously. However, the subjects were instructed to put their non-dependent side arm on a cushion on the greater trochanter to avoid hiding the markers on the mid-axillary line on the non-dependent side. Patients are not likely to ever lie in such a position, as they would usually have their arms in front of their torso. The difference in arm position may have affected the results. Second, measurements were taken with the subjects on the floor, not on a bed, in order to detect chest wall motion accurately in the region near the floor. However, Aliverti et al. (2000, 2001) took their measurements with the subjects on a bed in an ICU setting so as to be able to apply their results to patients, and they also measured the effects of differences in mattress hardness (Aliverti et al., 2001). The methods used in the present study need to be applied to subjects on mattresses to be able to generalize the results to the clinical setting. Third, pleural and abdominal pressure changes and distribution, regional lung volume, and diaphragm movement need to be examined simultaneously to confirm the present results. There are also limitations to the present study because only regional chest wall volume changes were measured during quiet breathing.
5. Conclusion The feasibility and the laterality of measurements of chest wall volume variation during tidal breathing were studied in the lateral position in healthy subjects. The findings demonstrated high measurement accuracy and the laterality of chest wall volume changes, which was related to the reduction in abdominal rib cage and abdomen volume changes on the dependent side in the lateral position. References Aliverti, A., Cala, S.J., Duranti, R., Ferrigno, G., Kenyon, C.M., Pedotti, A., Scano, G., Sliwinski, P., Macklem, P.T., Yan, S., 1997. Human respiratory muscle actions and control during exercise. J. Appl. Physiol. 83, 1256–1269. Aliverti, A., Dellacá, R., Pelosi, P., Chiumello, D., Pedotti, A., Gattinoni, L., 2000. Optoelectronic plethysmography in intensive care patients. Am. J. Respir. Crit. Care Med. 161, 1546–1552. Aliverti, A., Dellacà, R., Pelosi, P., Chiumello, D., Gatihnoni, L., Pedoti, A., 2001. Compartmental analysis of breathing in the supine and prone positions by optoelectronic plethysmography. Ann. Biomed. Eng. 29, 60–70. Boudarham, J., Pradon, D., Prigent, H., Falaize, L., Durand, M.C., Meric, H., Petitjean, M., Lofaso, F., 2013. Optoelectronic plethysmography as an alternative method for the diagnosis of unilateral diaphragmatic weakness. Chest 144, 887–895. Cala, S.J., Kenyon, C.M., Ferrigno, G., Carnevali, P., Aliverti, A., Pedotti, A., Macklem, P.T., Rochester, D.F., 1996. Chest wall and lung volume estimation by optical reflectance motion analysis. J. Appl. Physiol. 81, 2680–2689. De Groote, A., Van Muylem, A., Scillia, P., Cheron, G., Verleden, G., Paiva, M., Estenne, M., 2004. Ventilation asymmetry after transplantation for emphysema: role of chest wall and mediastinum. Am. J. Respir. Crit. Care Med. 170, 1233–1238. De Keulenaer, B.L., De Waele, J.J., Powell, B., Malbrain, M.L., 2009. What is normal intra-abdominal pressure and how is it affected by positioning, body mass and positive end-expiratory pressure? Intensive Care Med. 35, 969–976. De Waele, J.J., De Laet, I., De Keulenaer, B., Widder, S., Kirkpatrick, A.W., Cresswell, A.B., Malbrain, M., Bodnar, Z., Mejia-Mantilla, J.H., Reis, R., Parr, M., Schulze, R., Compano, S., Cheatham, M., 2008. The effect of different reference transducer positions on intra-abdominal pressure measurement: a multicenter analysis. Intensive Care Med. 34, 1299–1303. Frerichs, I., Hinz, J., Herrmann, P., Weisser, G., Hahn, G., Dudykevych, T., Quintel, M., Hellige, G., 2002. Detection of local lung air content by electrical impedance tomography compared with electron beam CT. J. Appl. Physiol. 93, 660–666. Johnson, B.D., Weisman, I.M., Zeballos, R.J., Beck, K.C., 1999. Emerging concepts in the evaluation of ventilatory limitation during exercise: the exercise tidal flowvolume loop. Chest 116, 488–503. Kenyon, C.M., Cala, S.J., Yan, S., Aliverti, A., Scano, G., Duranti, R., Pedotti, A., Macklem, P.T., 1997. Rib cage mechanics during quiet breathing and exercise in humans. J. Appl. Physiol. 83, 1242–1255. Lanini, B., Bianchi, R., Romagnoli, I., Coli, C., Binazzi, B., Gigliotti, F., Pizzi, A., Grippo, A., Scano, G., 2003. Chest wall kinematics in patients with hemiplegia. Am. J. Respir. Crit. Care Med. 168, 109–113. Layton, A.M., Moran, S.L., Garber, C.E., Armstrong, H.F., Basner, R.C., Thomashow, B.M., Bartels, M.N., 2013. Optoelectronic plethysmography compared to spirometry during maximal exercise. Respir. Physiol. Neurobiol. 185, 362–368. Nelson, L.D., Anderson, H.B., 1989. Physiologic effects of steep positioning in the surgical intensive care unit. Arch. Surg. 124, 352–355. Nozoe, M., Mase, K., Tsutou, A., 2011. Regional chest wall volume changes during various breathing maneuvers. J. Jpn. Phys. Ther. Assoc. 14, 12–18. Riedel, T., Richards, T., Schibler, A., 2005. The value of electrical impedance tomography in assessing the effect of body position and positive airway pressures on regional lung ventilation in spontaneously breathing subjects. Intensive Care Med. 31, 1522–1528. Romei, M., Mauro, A.L., D’Angelo, M.G., Turconi, A.C., Bresolin, N., Pedotti, A., Aliverti, A., 2010. Effects of gender and posture on thoraco-abdominal kinematics during quiet breathing in healthy adults. Respir. Physiol. Neurobiol. 172, 184–191. Saumarez, R.C., 1986. An analysis of possible movements of human upper rib cage. J Appl Physiol. 60, 678–689. Schellongowski, P., Losert, H., Locker, G.J., Laczika, K., Frass, M., Holzinger, U., Bojic, A., Staudinger, T., 2007. Prolonged lateral steep position impairs respiratory mechanics during continuous lateral rotation therapy in respiratory failure. Intensive Care Med. 33, 625–631. Verbanck, S., Schuermans, D., Van Muylem, A., Paiva, M., Noppen, M., Vincken, W., 1997. Ventilation distribution during histamine provocation. J. Appl. Physiol. 83, 1907–1916. Wang, H.K., Lu, T.W., Liing, R.J., Shih, T.T., Chen, S.C., Lin, K.H., 2009. Relationship between chest wall motion and diaphragmatic excursion in healthy adults in supine position. J. Formos. Med. Assoc. 108, 577–586.