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Transient transcapillary exchange of water driven by osmotic forces in the heart

Department of Bioengineering, University of Washington, Seattle, Washington 98195

Submitted 11 July 2002 ; accepted in final form 5 May 2003

Osmotic transient responses in organ weight after changes in perfusate osmolarity have implied steric hindrance to small-molecule transcapillary exchange, but tracer methods do not. We obtained osmotic weight transient data in isolated, Ringer-perfused rabbit hearts with NaCl, urea, glucose, sucrose, raffinose, inulin, and albumin and analyzed the data with a new anatomically and physicochemically based model accounting for 1) transendothelial water flux, 2) two sizes of porous passages across the capillary wall, 3) axial intracapillary concentration gradients, and 4) water fluxes between myocytes and interstitium. During steady-state conditions 28% of the transcapillary water flux going to form lymph was through the endothelial cell membranes [capillary hydraulic conductivity (L_p) = 1.8 ± 0.6 x 10^–8 cm · s^–1 · mmHg^–1], presumably mainly through aquaporin channels. The interendothelial clefts (with L_p = 4.4 ± 1.3 x 10^–8 cm · s^–1 · mmHg^–1) account for 67% of the water flux; clefts are so wide (equivalent pore radius was 7 ± 0.2 nm, covering 0.02% of the capillary surface area) that there is no apparent hindrance for molecules as large as raffinose. Infrequent large pores account for the remaining 5% of the flux. During osmotic transients due to 30 mM increases in concentrations of small solutes, the transendothelial water flux was in the opposite direction and almost 800 times as large and was entirely transendothelial because no solute gradient forms across the pores. During albumin transients, gradients persisted for long times because albumin does not permeate small pores; the water fluxes per milliosmolar osmolarity change were 200 times larger than steady-state water flux. The analysis completely reconciles data from osmotic transient, tracer dilution, and lymph sampling techniques.

capillary permeability; reflection coefficient; transport modeling; microcirculation; isolated rabbit heart; porous transport

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