Surface biophysics of the surface monolayer theory is incompatible with regional lung function

Abstract

The surface monolayer theory of Clements was tested on open surface films of calf lung surfactant extract in a leak-free vertical film surface balance in which alveolar area (A) changes in each lung zone were simulated in accordance with the theory. We found that: 1) physiologically necessary low surface tension (gamma), < 4 dyn/cm, was sustained only by continuous film compression ("expiration"); 2) compression from A equivalent to total lung capacity to functional residual capacity produced fleeting gamma reduction in all zones and quick reversal to high gamma with A changes that simulated tidal volume (VT) breathing at both 14 (adult) and 40 (neonatal) cpm; 3) phase differences between gamma and A axes of VT loops that indicate mixed surface film composition may be attributable to film inertia and viscoelasticity; 4) estimated alveolar retraction pressure due to gamma (P gamma) exceeds "net" transpulmonary pressure, i.e., favors alveolar collapse, under virtually all conditions of the theory in all zones; 5) return to transient, fleeting low gamma in successive VT cycles was determined by the inherent difference in compression and decompression rates, which results in exhaustion of available A in very few cycles; 6) the "sigh", which restores stable low gamma according to the theory, actually produced unstable high gamma during virtually all phases of the maneuver. In contrast, closed bubble films of the surfactant were structurally stable and produce stable near 0 gamma and P gamma.

Intraalveolar bubbles and bubble films: II. Formation in vivo through adulthood

“…Assuming that bubbles are spherical at these volumes (Appendix A), we have calculated from our data an increase of common bubble film area of about 32-38%. Studies of surfactant films in a surface balance show that film surface tension may increase from near zero to relatively high equilibrium values of 25-30 dydcm during an equivalent expansion in vitro (Scarpelli and Mautone, 1994). The possibility that expanded bubble films at high lung volumes result in an increase of surface tension fits Pattle's observations (1960) on surfactant bubbles expanded in vitro, the studies of Schurch et al (1992) on in vitro bubbles expanded from the compressed state (including "film collapse"), and the measurements of surface tension in excised rabbit lungs by Bachofen et al (1987).…”

“…Surfactant films compressed to and beyond "film collapse" (see Bubble Contraction During Deflation, above) tend to decompress spontaneously to an equilibrium, relatively low surface concentration with high surface tension in the open film (Colacicco and Scarpelli, 1973;Scarpelli and Mautone, 1994). In contrast, surfactant films are compressed spontaneously to maximal surface concentration in the closed film of a bubble and, when compressed by external forces beyond "film collapse," they tend to expand spontaneously to the previous state of maximal surface concentration (Pattle, 1958(Pattle, , 1960: In both states, surface tension is near zero.…”

Intraalveolar bubbles and bubble films I. Formation and development during the first 48 hours of extrauterine life in rabbits

“…We note, however, that "menisci" spanning the gas phase of wettable surfaces must be continuous with interfacial films that line these surfaces (Bikerman, 1973); since the terminal unit is closed peripherally, the "meniscus" and interfacial film are in fact a bubble (Scarpelli, 1988). Our concept of the molecular configuration of the film has been presented schematically in its simplest form (Scarpelli and Mautone, 1994). Figure 9 shows this configuration in an alveolus, the shape and relative dimensions of which correspond to alveoli at resting volume as reconstructed by Mercer et al (1987).…”

Analysis of Lung Surfactant Model Systems with Time-of-Flight Secondary Ion Mass Spectrometry

“…According to the surfactant monolayer theory (Clements, 1962) this is attained by almost pure monolayers of dipalmitoylphosphatidylcholine (DPPC) (Bangham, 1979), where non-DPPC components are supposed to be squeezed out from the monolayer at compression/exhalation and respread into the monolayer at expansion/inhalation. This theory, however, is questioned by Scarpelli and Mautone (1994), stating that it is incompatible with regional lung function.…”