Abstract
While supine, fluid moves from the legs and accumulates in the chest and neck. However, patterns of rostral fluid shift are not clear. Furthermore, real-time measurement of neck fluid volume has not been investigated. The objective of this study was to investigate the dynamics of rostral fluid shift in men and women. We developed a bioelectrical impedance system to measure leg, abdominal, thoracic and neck fluid volumes (LFV, AFV, TFV, NFV) continuously. Forty healthy non-obese adults (20 men) lay supine for 90 min while fluid volumes were measured. After 90 min, a similar volume of fluid shifted out of the legs in both sexes (p = 0.079), but men accumulated more fluid in their thorax (63 ± 6 vs. 44 ± 11 ml, p = 0.016) and neck (17 ± 2 vs. 14 ± 1 ml, p = 0.029) than women. In both sexes, the increase in NFV caused a significant increase in neck circumference, which was greater in men (p = 0.009). Furthermore, 80% of rostral fluid shift would occur in the first 2 h of lying supine. These results suggest that greater fluid shift into the thorax and neck may contribute to the higher prevalence of sleep apnea in men than in women.
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Abbreviations
- AFV:
-
Abdominal fluid volume
- ANCOVA:
-
Analysis of covariance
- BMI:
-
Body mass index
- LFV:
-
Leg fluid volume
- NC:
-
Neck circumference
- NFV:
-
Neck fluid volume
- TFV:
-
Thoracic fluid volume
- UA-XSA:
-
Upper airway cross-sectional area
References
Avasthey, P., and E. H. Wood. Intrathoracic and venous pressure relationships during responses to changes in body position. J. Appl. Physiol. 37:166–175, 1974.
Baccelli, G., P. Pacenti, S. Terrani, M. Checchini, G. Riglietti, F. Prestipino, E. Omboni, F. Sardella, M. Catalano, and Z. Malacarne. Scintigraphic recording of blood volume shifts. J. Nucl. Med. 36:2022–2031, 1995.
Berg, H. E., B. Tedner, and P. A. Tesch. Changes in lower limb muscle cross-sectional area and tissue fluid volume after transition from standing to supine. Acta Physiol. Scand. 148:379–385, 1993.
Bracco, D., D. Thiebaud, R. L. Chiolero, M. Landry, P. Burckhardt, and Y. Schutz. Segmental body composition assessed by bioelectrical impedance analysis and DEXA in humans. J. Appl. Physiol. (1985) 81:2580–2587, 1996.
Chiu, K. L., C. M. Ryan, S. Shiota, P. Ruttanaumpawan, M. Arzt, J. S. Haight, C. T. Chan, J. S. Floras, and T. D. Bradley. Fluid shift by lower body positive pressure increases pharyngeal resistance in healthy subjects. Am. J. Respir. Crit. Care Med. 174:1378–1383, 2006.
De Lorenzo, A., A. Andreoli, J. Matthie, and P. Withers. Predicting body cell mass with bioimpedance by using theoretical methods: a technological review. J. Appl. Physiol. (1985) 82:1542–1558, 1997.
Dempsey, J. A., S. C. Veasey, B. J. Morgan, and C. P. O’Donnell. Pathophysiology of sleep apnea. Physiol. Rev. 90:47–112, 2010.
Demura, S., S. Sato, and T. Kitabayashi. Percentage of total body fat as estimated by three automatic bioelectrical impedance analyzers. J. Physiol. Anthropol. Appl. Hum. Sci. 23:93–99, 2004.
Drazner, M. H., A. Prasad, C. Ayers, D. W. Markham, J. Hastings, P. S. Bhella, S. Shibata, and B. D. Levine. The relationship of right- and left-sided filling pressures in patients with heart failure and a preserved ejection fraction. Circ. Heart Fail 3:202–206, 2010.
Fawcett, J. K., and V. Wynn. Effects of posture on plasma volume and some blood constituents. J. Clin. Pathol. 13:304–310, 1960.
Fenech, M., and M. Y. Jaffrin. Extracellular and intracellular volume variations during postural change measured by segmental and wrist-ankle bioimpedance spectroscopy. IEEE Trans. Biomed. Eng. 51:166–175, 2004.
Fredberg, J. J., M. E. Wohl, G. M. Glass, and H. L. Dorkin. Airway area by acoustic reflections measured at the mouth. J. Appl. Physiol. 48:749–758, 1980.
Friedman, O., T. D. Bradley, C. T. Chan, R. Parkes, and A. G. Logan. Relationship between overnight rostral fluid shift and obstructive sleep apnea in drug-resistant hypertension. Hypertension 56:1077–1082, 2010.
Friedman, O., T. D. Bradley, and A. G. Logan. Influence of lower body positive pressure on upper airway cross-sectional area in drug-resistant hypertension. Hypertension 61:240–245, 2013.
Hildebrandt, W., H. C. Gunga, J. Herrmann, L. Rocker, K. Kirsch, and J. Stegemann. Enhanced slow caudad fluid shifts in orthostatic intolerance after 24-h bed-rest. Eur. J. Appl. Physiol. Occup. Physiol. 69:61–70, 1994.
Jafari, B., and V. Mohsenin. Overnight rostral fluid shift in obstructive sleep apnea: does it affect the severity of sleep-disordered breathing? Chest 140:991–997, 2011.
Jaffrin, M. Y., and H. Morel. Body fluid volumes measurements by impedance: a review of bioimpedance spectroscopy (BIS) and bioimpedance analysis (BIA) methods. Med. Eng. Phys. 30:1257–1269, 2008.
Kachlik, D., V. Pechacek, V. Musil, and V. Baca. The venous system of the pelvis: new nomenclature. Phlebology 25:162–173, 2010.
Kasai, T., J. S. Floras, and T. D. Bradley. Sleep apnea and cardiovascular disease: a bidirectional relationship. Circulation 126:1495–1510, 2012.
Kasai, T., S. S. Motwani, D. Yumino, J. M. Gabriel, L. T. Montemurro, V. Amirthalingam, J. S. Floras, and T. D. Bradley. Contrasting effects of lower body positive pressure on upper airways resistance and partial pressure of carbon dioxide in men with heart failure and obstructive or central sleep apnea. J. Am. Coll. Cardiol. 61:1157–1166, 2013.
Kasai, T., S. S. Motwani, D. Yumino, S. Mak, G. E. Newton, and T. D. Bradley. Differing relationship of nocturnal fluid shifts to sleep apnea in men and women with heart failure. Circ. Heart Fail. 5:467–474, 2012.
Krogh, A., E. M. Landis, and A. H. Turner. The movement of fluid through the human capillary wall in relation to venous pressure and to the colloid osmotic pressure of the blood. J. Clin. Invest. 11:63–95, 1932.
Kyle U. G., I. Bosaeus, A. D. De Lorenzo, P. Deurenberg, M. Elia, J. M. Gomez, B. L. Heitmann, L. Kent-Smith, J. C. Melchior, M. Pirlich, H. Scharfetter, A. M. Schols, C. Pichard and E. W. G. Composition of the. Bioelectrical impedance analysis–part I: review of principles and methods. Clin. Nutr. 23:1226–1243, 2004.
Larsen, F., L. Mogensen, and B. Tedner. Influence of furosemide and body posture on transthoracic electrical impedance in AMI. Chest 90:733–737, 1986.
Levick, J. R., and C. C. Michel. The effects of position and skin temperature on the capillary pressures in the fingers and toes. J. Physiol. 274:97–109, 1978.
Ling, C. H., A. J. de Craen, P. E. Slagboom, D. A. Gunn, M. P. Stokkel, R. G. Westendorp, and A. B. Maier. Accuracy of direct segmental multi-frequency bioimpedance analysis in the assessment of total body and segmental body composition in middle-aged adult population. Clin. Nutr. 30:610–615, 2011.
Malhotra, A., Y. Huang, R. B. Fogel, G. Pillar, J. K. Edwards, R. Kikinis, S. H. Loring, and D. P. White. The male predisposition to pharyngeal collapse: importance of airway length. Am. J. Respir. Crit. Care Med. 166:1388–1395, 2002.
Marin, J. M., S. J. Carrizo, E. Vicente, and A. G. Agusti. Long-term cardiovascular outcomes in men with obstructive sleep apnoea-hypopnoea with or without treatment with continuous positive airway pressure: an observational study. Lancet 365:1046–1053, 2005.
Mohapatra, S. N., and D. W. Hill. The changes in blood resistivity with haematocrit and temperature. Eur. J. Intensive Care Med. 1:153–162, 1975.
Mohsenin, V. Gender differences in the expression of sleep-disordered breathing : role of upper airway dimensions. Chest 120:1442–1447, 2001.
Punjabi, N. M., B. S. Caffo, J. L. Goodwin, D. J. Gottlieb, A. B. Newman, G. T. O’Connor, D. M. Rapoport, S. Redline, H. E. Resnick, J. A. Robbins, E. Shahar, M. L. Unruh, and J. M. Samet. Sleep-disordered breathing and mortality: a prospective cohort study. PLoS Med. 6:e1000132, 2009.
Redolfi, S., I. Arnulf, M. Pottier, T. D. Bradley, and T. Similowski. Effects of venous compression of the legs on overnight rostral fluid shift and obstructive sleep apnea. Respir. Physiol. Neurobiol. 175:390–393, 2011.
Redolfi, S., I. Arnulf, M. Pottier, J. Lajou, I. Koskas, T. D. Bradley, and T. Similowski. Attenuation of obstructive sleep apnea by compression stockings in subjects with venous insufficiency. Am. J. Respir. Crit. Care Med. 184:1062–1066, 2011.
Redolfi, S., D. Yumino, P. Ruttanaumpawan, B. Yau, M. C. Su, J. Lam, and T. D. Bradley. Relationship between overnight rostral fluid shift and Obstructive Sleep Apnea in nonobese men. Am. J. Respir. Crit. Care Med. 179:241–246, 2009.
Rowley, J. A., X. Zhou, I. Vergine, M. A. Shkoukani, and M. S. Badr. Influence of gender on upper airway mechanics: upper airway resistance and Pcrit. J. Appl. Physiol. 91(2248–2254):2001, 1985.
Ryan, C. M., and T. D. Bradley. Pathogenesis of obstructive sleep apnea. J. Appl. Physiol. 99:2440–2450, 2005.
Shepard, Jr, J. W., D. A. Pevernagie, A. W. Stanson, B. K. Daniels, and P. F. Sheedy. Effects of changes in central venous pressure on upper airway size in patients with obstructive sleep apnea. Am. J. Respir Crit. Care. Med. 153:250–254, 1996.
Shiota, S., C. M. Ryan, K. L. Chiu, P. Ruttanaumpawan, J. Haight, M. Arzt, J. S. Floras, C. Chan, and T. D. Bradley. Alterations in upper airway cross-sectional area in response to lower body positive pressure in healthy subjects. Thorax 62:868–872, 2007.
Singh B., A. Yadollahi, O. D. Lyons, H. Alshaer and T. D. Bradley. Measurement of leg fluid volume using bioelectrical impedance [abstract]. In: American Physiology Society Experimental Biology Conference. San Diego, CA, pp. 1156–1114, 2014.
Starling, E. H. On the absorption of fluids from the connective tissue spaces. J. Physiol. 19:312–326, 1896.
Su, M. C., K. L. Chiu, P. Ruttanaumpawan, S. Shiota, D. Yumino, S. Redolfi, J. S. Haight, and T. D. Bradley. Lower body positive pressure increases upper airway collapsibility in healthy subjects. Respir. Physiol. Neurobiol. 161:306–312, 2008.
Su, M. C., K. L. Chiu, P. Ruttanaumpawan, S. Shiota, D. Yumino, S. Redolfi, J. S. Haight, B. Yau, J. Lam, and T. D. Bradley. Difference in upper airway collapsibility during wakefulness between men and women in response to lower-body positive pressure. Clin. Sci. (Lond.) 116:713–720, 2009.
Tagliabue, A., A. Andreoli, M. Comelli, S. Bertoli, G. Testolin, G. Oriani, and A. De Lorenzo. Prediction of lean body mass from multifrequency segmental impedance: influence of adiposity. Acta Diabetol. 38:93–97, 2001.
Terada, N., and T. Takeuchi. Postural changes in venous pressure gradients in anesthetized monkeys. Am. J. Physiol. 264:H21–H25, 1993.
Thompson, W. O., P. K. Thompson, and M. E. Dailey. The effect of posture upon the composition and volume of the blood in man. J. Clin. Invest. 5:573–604, 1928.
van Lieshout, J. J., M. P. Harms, F. Pott, M. Jenstrup, and N. H. Secher. Stroke volume of the heart and thoracic fluid content during head-up and head-down tilt in humans. Acta Anaesthesiol. Scand. 49:1287–1292, 2005.
Waterfield, R. L. The effect of posture on the volume of the leg. J. Physiol. 72:121–131, 1931.
Waterfield, R. L. The effects of posture on the circulating blood volume. J. Physiol. 72:110–120, 1931.
White, L. H., and T. D. Bradley. Role of nocturnal rostral fluid shift in the pathogenesis of obstructive and central sleep apnoea. J. Physiol. 591:1179–1193, 2013.
XITRON. HYDRA ECF/ICF (Model 4200), Bio-impedance spectrum analyzer, for measuring intracellular and extracellular fluid volumes. Operating manual San Diego, CA, USA: XITRON Technologies Inc, 2007.
Youmans, J. B., H. S. Wells, D. Donley, D. G. Miller, and H. Frank. The effect of posture (standing) on the serum protein concentration and colloid osmotic pressure of blood from the foot in relation to the formation of edema. J. Clin. Invest. 13:447–459, 1934.
Young, T., M. Palta, J. Dempsey, J. Skatrud, S. Weber, and S. Badr. The occurrence of sleep-disordered breathing among middle-aged adults. N. Engl. J. Med. 328:1230–1235, 1993.
Yumino, D., S. Redolfi, P. Ruttanaumpawan, M. C. Su, S. Smith, G. E. Newton, S. Mak, and T. D. Bradley. Nocturnal rostral fluid shift: a unifying concept for the pathogenesis of obstructive and central sleep apnea in men with heart failure. Circulation 121:1598–1605, 2010.
Yumino, D., H. Wang, J. S. Floras, G. E. Newton, S. Mak, P. Ruttanaumpawan, J. D. Parker, and T. D. Bradley. Prevalence and physiological predictors of sleep apnea in patients with heart failure and systolic dysfunction. J. Card. Fail. 15:279–285, 2009.
Zhu, F., M. K. Kuhlmann, P. Kotanko, E. Seibert, E. F. Leonard, and N. W. Levin. A method for the estimation of hydration state during hemodialysis using a calf bioimpedance technique. Physiol. Meas. 29:S503–S516, 2008.
Zhu, F., D. Schneditz, E. Wang, and N. W. Levin. Dynamics of segmental extracellular volumes during changes in body position by bioimpedance analysis. J. Appl. Physiol. 85(497–504):1998, 1985.
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Yadollahi, A., Singh, B. & Bradley, T.D. Investigating the Dynamics of Supine Fluid Redistribution Within Multiple Body Segments Between Men and Women. Ann Biomed Eng 43, 2131–2142 (2015). https://doi.org/10.1007/s10439-015-1264-0
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DOI: https://doi.org/10.1007/s10439-015-1264-0