Mechanics of airway and alveolar collapse in human breath-hold diving

https://doi.org/10.1016/j.resp.2007.07.006Get rights and content

Abstract

A computational model of the human respiratory tract was developed to study airway and alveolar compression and re-expansion during deep breath-hold dives. The model incorporates the chest wall, supraglottic airway, trachea, branched airway tree, and elastic alveoli assigned time-dependent surfactant properties. Total lung collapse with degassing of all alveoli is predicted to occur around 235 m, much deeper than estimates for aquatic mammals. Hysteresis of the pressure–volume loop increases with maximum diving depth due to progressive alveolar collapse. Reopening of alveoli occurs stochastically as airway pressure overcomes adhesive and compressive forces on ascent. Surface area for gas exchange vanishes at collapse depth, implying that the risk of decompression sickness should reach a plateau beyond this depth. Pulmonary capillary transmural stresses cannot increase after local alveolar collapse. Consolidation of lung parenchyma might provide protection from capillary injury or leakage caused by vascular engorgement due to outward chest wall recoil at extreme depths.

Introduction

Breath-hold diving became recognized as a competitive sport in 1949 when Raimondo Bucher dove to 30 m on a single breath of air. The depth record has since been advanced over 80 times by various highly trained individuals dedicated to extending human physiological limits underwater. The present depth record for a weight-assisted breath-hold dive on a sled is 214 m achieved by Austrian free diver Herbert Nitsch in 2007. At this depth, where the hydrostatic pressure is 22 times that at the surface, gas enclosed in lungs and conducting airways must compress to less than 5% of initial surface volume. While the physiology of breath-hold diving has been investigated extensively over the past several decades (Lundgren and Ferrigno, 1987, Rahn and Yokoyama, 1965), little attention has been paid to the alterations of pulmonary mechanics that make these dives possible, and the implications of near-total lung compression that human divers experience at extreme depths.

It was once believed that lung compression below residual volume would cause injury (Craig, 1968). Under that assumption, total lung capacity compressing to a typical residual volume of 25% would have limited maximum depth to about 4 atm or 30 m for a subject of average size. Airspace volume reduction at much greater depths is assumed to occur through a combination of airway closure, alveolar compression, and engorgement of the pulmonary capillary network with blood translocated centrally from the peripheral circulation (Schaefer et al., 1968). Airways and alveoli of diving mammals like seals and whales undergo near-total collapse at depth, limiting vascular stresses in the lungs. Human lungs must undergo similar collapse, but the degree to which this occurs is not known since thoracic imaging studies are difficult to conduct underwater. The only images obtained are chest radiographs of breath-hold divers at depths up to 20 m using submerged X-ray equipment (Data et al., 1979). High elevation of the diaphragm and dilatation of the heart were noted at depth, but film quality was less than optimal, and pulmonary atelectasis is difficult to quantify on plain radiographs. No further attempts to image or measure lungs underwater during human breath-hold dives have been reported.

Some breath-hold divers have experienced pulmonary edema, hemoptysis, and chest pain on moderate or deep dives (Boussuges et al., 1999, Kiyan et al., 2001, Fitz-Clarke, 2006), yet many record-setting divers have had no problems at all. It is not clear why certain divers are more susceptible to adverse effects at depth. Only a few symptomatic individuals have been examined immediately after breath-hold diving, and none have undergone direct visualization by bronchoscopy to definitively localize sources of active bleeding. The etiology of these complications remains unclear. Alveolar collapse might protect the lungs from excessive vascular stresses, and might also limit decompression sickness risk by reducing gas exchanging surface area for nitrogen uptake from the lungs (Falke et al., 1985).

There has been no investigation into how human lungs and communicating airspaces compress, collapse, and re-expand during breath-hold dives. This paper describes a computational model of human lungs and airspaces developed to provide insight into obligatory changes in pulmonary mechanics during deep dives. The model confirms that a high degree of airspace collapse, far beyond that occurring at residual volume, is essential on deep dives, and illustrates the role of opening pressures at which alveoli re-expand on ascent. It is hypothesized that parenchymal compression in regions of lung collapse limits pulmonary capillary transmural pressures caused by vascular engorgement at extreme depths.

Section snippets

Methods

The human respiratory tract is represented as a series of elastic conduits illustrated in Fig. 1. Supraglottic segments are numbered from 0 at the nostrils to 20 at the glottis. The nasal cavity has five segments, the paranasal sinuses have four, and the mouth and pharynx have 11. These are linked in series, since the static compliance of the entire system does not depend on geometrical arrangement or cavity shapes. The paranasal sinuses have a total volume of 90 ml (Kawarai et al., 1999) with

Results

Volume distribution along the 42 airway segments and 240 alveoli during descent from the surface to 200 m depth is shown in Fig. 2. The initial airway pressure PA of 60 cm H2O at the surface corresponds with inflation to a pre-dive lung volume of 9.20 l and airway volume of 0.42 l. These represent typical values in a diver after normal inspiration to total lung capacity (TLC) followed by positive pressure hyperinflation using glossopharyngeal lung packing, a technique employed by champion

Discussion

The model predicts the depth-dependent response of human lungs and airways to hydrostatic compression during breath-hold diving, and the lung collapse depth at which all alveoli become degassed. There have been no previous attempts to measure or model pulmonary mechanics under these conditions. Collapse depth cannot be determined by simply applying Boyle's law to the volume of the alveoli at ambient pressure because the stiffer embedded conducting airways account for a progressively greater

Conclusion

The model predicts that human lungs collapse beyond 200 m, based on estimates of the compliance curves of airways and alveoli. This is much deeper than estimates for aquatic mammals. Reopening of closed alveoli occurs on ascent beginning at a depth that depends on the maximum depth reached, and surfactant properties. A practical implication is that pulmonary capillary transmural stresses cannot increase after local alveolar collapse. Consolidation of lung parenchyma might serve as a protective

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