The Key Roles of Negative Pressure Breathing and Exercise in the Development of Interstitial Pulmonary Edema in Professional Male SCUBA Divers

Abstract

Background: Immersion pulmonary edema is potentially a catastrophic condition; however, the pathophysiological mechanisms are ill-defined. This study assessed the individual and combined effects of exertion and negative pressure breathing on the cardiovascular system during the development of pulmonary edema in SCUBA divers.

Methods: Sixteen male professional SCUBA divers performed four SCUBA dives in a freshwater pool at 1 m depth while breathing air at either a positive or negative pressure both at rest or with exercise. Echocardiography and lung ultrasound were used to assess the cardiovascular changes and lung comet score (a measure of interstitial pulmonary edema).

Results: The ultrasound lung comet score was 0 following both the dives at rest regardless of breathing pressure. Following exercise, the mean comet score rose to 4.2 with positive pressure breathing and increased to 15.1 with negative pressure breathing. The development of interstitial pulmonary edema was significantly related to inferior vena cava diameter, right atrial area, tricuspid annular plane systolic excursion, right ventricular fractional area change, and pulmonary artery pressure. Exercise combined with negative pressure breathing induced the greatest changes in these cardiovascular indices and lung comet score.

Conclusions: A diver using negative pressure breathing while exercising is at greatest risk of developing interstitial pulmonary edema. The development of immersion pulmonary edema is closely related to hemodynamic changes in the right but not the left ventricle. Our findings have important implications for divers and understanding the mechanisms of pulmonary edema in other clinical settings.

Keywords: Atrial natriuretic peptide; Echocardiography; Exercise; Hydrostatic transrespiratory pressure; Immersion pulmonary edema; Inspiratory breathing effort; Lung ultrasonography; Negative pressure breathing; Right heart preload; Work of breathing.

Fig. 1

Tidal volume loop during each dive condition in one diver. A positive transpulmonary pressure gradient (or positive static lung load: SLL+) is set when the rebreather is worn anteriorly (on the abdomen) by the diver in prone position (a). A positive pressure breathing (PPB) condition is created. Conversely, when the rebreather is worn posteriorly (b), the transpulmonary pressure gradient is negative in the prone position (negative static lung load, SLL−), and the diver is in condition of negative pressure breathing (NPB). In each condition, the diver completed two 30-min dives, one simply statically floating (static), and one with continuous fin swimming (exercise). Examples of tidal pressure-volume loops are sketched during both static and exercise in each PPB and NPB condition. The dashed lines indicate the SLL level in each condition. Peak insp. press., peak inspiratory pressure during; peak expir. press., peak expiratory pressure. Of note, in each PPB and NPB, Vt lengthening carried the main rest to exercise change, while pressure ranges were very similar during static and exercise dives

Fig. 2

Percent changes in parameters of right cardiac function after 30-min dive in each combination of pressure breathing and physical activity. StPP, static dive with positive transpulmonary pressure; StNP, static dive with negative transpulmonary pressure; ExPP, continuous finning dive with positive transpulmonary pressure; ExNP, continuous finning dive with negative transpulmonary pressure; IVC diam, diameter of inferior vena cava; RA area, right atrial area; RV/LV, ratio of right to left ventricle end-diastolic area; RVFAC, right ventricle fractional area change; TAPSE tricuspid annular plane systolic excursion; sPAP, systolic pulmonary arterial pressure. *p < 0.05 significant difference between ExPP and StPP or ExNP and StNP; ^#p < 0.05 significant difference between ExPP and StNP or ExNP and StPP; ^$p < 0.05 significant difference between ExNP and ExPP. Two-way analysis of variance (ANOVA) with repeated-measures and the post hoc Holm–Sidak test were used to compare the four conditions in each variable

Fig. 3

ULC score according to a the rise in right atrial area, b the rise in TAPSE, c the plasma concentration of Nt-proANP, d the rise in RV/LV ratio, and e the power of breathing, after the exercise dives. ULC score, extravascular lung water score, according to the number of ultrasound lung comet tails. ∆% RA area, percent change from predive in right atrial area; ∆% TAPSE, percent change from predive in tricuspid annular plane systolic excursion; ANP, Nt-proANP plasma concentration at the end of dive; RV/LV, ratio of right to left ventricle end-diastolic area. Empty circles, ExPPB, i.e., setting of positive transpulmonary pressure breathing; full circles, ExNPB, i.e., setting of negative transpulmonary pressure breathing

Fig. 4

Correlations observed between individual cumulated inspiratory work of breathing and the corresponding percent changes in right atrial volume (a), rise in TAPSE (b), in RV/LV ratio (c), and the final plasma Nt-proANP concentration (d), during the fin exercise dive with negative transpulmonary pressure. cWOB insp, cumulated inspiratory work of breathing; ∆RA area, change in right atrial area; ∆TAPSE, change in tricuspid annular plane systolic excursion; RV/LV, ratio of right to left ventricles end-diastolic area; Nt-proANP, plasma concentration of Nt-proANP