Abstract
Breath-hold divers (BHD) enduring apnea for more than 4 min are characterized by resistance to release of reactive oxygen species, reduced sensitivity to hypoxia, and low mitochondrial oxygen consumption in their skeletal muscles similar to northern elephant seals. The muscles and myocardium of harbor seals also exhibit metabolic adaptations including increased cardiac lactate-dehydrogenase-activity, exceeding their hypoxic limit. We hypothesized that the myocardium of BHD possesses similar adaptive mechanisms. During maximum apnea 15O-H2O-PET/CT (n = 6) revealed no myocardial perfusion deficits but increased myocardial blood flow (MBF). Cardiac MRI determined blood oxygen level dependence oxygenation (n = 8) after 4 min of apnea was unaltered compared to rest, whereas cine-MRI demonstrated increased left ventricular wall thickness (LVWT). Arterial blood gases were collected after warm-up and maximum apnea in a pool. At the end of the maximum pool apnea (5 min), arterial saturation decreased to 52%, and lactate decreased 20%. Our findings contrast with previous MR studies of BHD, that reported elevated cardiac troponins and decreased myocardial perfusion after 4 min of apnea. In conclusion, we demonstrated for the first time with 15O-H2O-PET/CT and MRI in elite BHD during maximum apnea, that MBF and LVWT increases while lactate decreases, indicating anaerobic/fat-based cardiac-metabolism similar to diving mammals.
Highlights
Breath-hold divers (BHD) enduring apnea for more than 4 min are characterized by resistance to release of reactive oxygen species, reduced sensitivity to hypoxia, and low mitochondrial oxygen consumption in their skeletal muscles similar to northern elephant seals
The main and novel findings of our study are: After a warm-up of three consecutive apneas and 1) during 4 min of apnea, the hearts of BHD in this study were without signs of concomitant T2* blood oxygen level dependence (BOLD) assessed myocardial ischemia on cardiac magnetic resonance imaging (CMR), 2) after 4 min of apnea 15O-H2O-PET/CT revealed increased myocardial blood flow to levels approaching theoretical maximum hyperemia[23,24,25,26] without signs of regional myocardial perfusion deficits, and 3) at end of max pool apnea, systemic oxygenation decreased to 4.3 kPa ± 0.4 and pH decreases concomitant with a decrease in lactate in BHD
We demonstrated for the first time that BHD, similar to adult diving mammals, possess cardiac hypoxic resistance and increased myocardial blood flow with CMR and 15O-H2O-PET/CT during apnea ~ 6 min, and lactate metabolization during max pool apnea
Summary
Breath-hold divers (BHD) enduring apnea for more than 4 min are characterized by resistance to release of reactive oxygen species, reduced sensitivity to hypoxia, and low mitochondrial oxygen consumption in their skeletal muscles similar to northern elephant seals. Samples of the skeletal muscles and the heart from adult harbor seals (Phoca Vitulina) shows up to sixfold higher β-hydroxyacyl-CoA dehydrogenase activities normalized to tissue-specific resting metabolic rate, and the heart of the seals possess the highest lactate dehydrogenase activity, compared to dog and rat, suggesting both a reliance on anaerobic metabolism during dives exceeding the animal’s aerobic limit, and a high aerobic capacity for lipid metabolism within the h eart[8]. It could be hypothesized, that the hearts of BHD would possess similar adaptions. As myocardial ischemia is dependent on both blood oxygen levels, perfusion and the need of oxygen based on cardiac contraction, these parameters were quantified using arterial samples, cine CMR and 15O-H2O-PET/CT and the resulting myocardial oxygenation as a sign of ischemia measured using BOLD CMR at rest and during a maximal voluntary apnea in elite BHD with a self-reported maximum static apnea of more than 5 min
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