The Key Roles of Negative Pressure Breathing and Exercise in the Development of Interstitial Pulmonary Edema in Professional Male SCUBA Divers
Castagna et al. Sports Medicine - Open
The Key Roles of Negative Pressure Breathing and Exercise in the Development of Interstitial Pulmonary Edema in Professional Male SCUBA Divers
Olivier Castagna 3 4
Jacques Regnard 2
Emmanuel Gempp 7
Pierre Louge 8
François Xavier Brocq 6
Bruno Schmid 4
Anne-Virginie Desruelle 4
Valentin Crunel 4
Adrien Maurin 4
Romain Chopard 5
David Hunter MacIver 0 1
0 Musgrove Park, Taunton & Somerset Hospital , Taunton , UK
1 Biological Physics Group, University of Manchester , Manchester , UK
2 EA3920, University Bourgogne Franche-Comté and University Hospitals , Besançon , France
3 Laboratory of Human Motricity, Education Sport and Health , LAMHESS (EA 6312), Toulon , France
4 Underwater Research Team (ERRSO) from the Military Biomedical Research Institute (IRBA) , Toulon , France
5 Department of Cardiology EA3920, Franche Comté University and University Hospital , Besançon , France
6 Department of Cardiology, HIA St Anne Military Hospital , Toulon , France
7 French Navy Diving School , Toulon , France
8 Department of Hyperbaric Medicine, HIA St Anne Military Hospital , Toulon , France
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.
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
Key points
The exercise-induced increase in tidal volume
during immersion elevates right heart preload,
triggering a right to left ventricular imbalance and
lung congestion.
Exercising with negative pressure breathing further
increases the inspiratory work of breathing, right
ventricle loading, right to left heart imbalance, and
rate of interstitial lung water accumulation.
Positive pressure breathing decreases cardiovascular
changes and pulmonary edema during immersion
with exercise.
Plasma levels of atrial natriuretic peptide increase
with inspiratory work and correlates with lung
comet scores.
An altered right to left heart imbalance provokes the
development of immersion pulmonary edema when
inspiratory work is high, e.g., during swimming at
high intensity level or SCUBA diving with negative
pressure breathing setting.
Background
Immersion pulmonary edema (IPE) is accompanied by
the onset of dyspnea while diving or swimming. IPE may
be accompanied by cough, hemoptysis, and severe
hypoxemia and can result in death [
1–3
]. Resting and
normobaric oxygen therapy usually results in rapid relief of
symptoms without sequelae. IPE can occur in both
young athletes as well as older subjects especially if
cardiovascular co-morbidities are present [
4
].
In healthy subjects, the main predisposing factors to
IPE [
5
] are cold water [
3, 6
] and exertion [
7, 8
]. Other
predisposing factors are age > 50 years, hypertension,
and left heart disease [
4
]. The condition has also been
reported in highly fit subjects such as military swimmers
and triathletes [
1–3, 9
]. IPE symptoms can vary in
severity [10], and the accumulation of interstitial pulmonary
edema without overt symptoms is common after normal
diving without significant exertional effort [
11
].
Moderate fin swimming exercise leads to increasing interstitial
pulmonary edema [
12
]. The rise in transmural
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