Cardiac hypoxic resistance and decreasing lactate during maximum apnea in elite breath hold divers

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.

Extreme Hypoxia Causing Brady-Arrythmias During Apnea in Elite Breath-Hold Divers

“…These Sherpas demonstrate decreasing lactate levels during maximum exercise, indicative of lactate metabolization ( Ge et al, 1994 ). Similarly, we have demonstrated that elite BHD decrease circulating lactate levels during maximum apnea ( Kjeld et al, 2021 ), indicative of a similar cardiac metabolism as found in adult harbor seals (Phoca Vitulina), who possess the highest cardiac lactate dehydrogenase activity, compared to terrestrial animals ( Fuson et al, 2003 ). In the present study, we demonstrate stable blood glucose during maximum apnea in the same population of elite BHD (+1) as described in our previous study ( Kjeld et al, 2021 ).…”

“…Similarly, we have demonstrated that elite BHD decrease circulating lactate levels during maximum apnea ( Kjeld et al, 2021 ), indicative of a similar cardiac metabolism as found in adult harbor seals (Phoca Vitulina), who possess the highest cardiac lactate dehydrogenase activity, compared to terrestrial animals ( Fuson et al, 2003 ). In the present study, we demonstrate stable blood glucose during maximum apnea in the same population of elite BHD (+1) as described in our previous study ( Kjeld et al, 2021 ). The stable blood glucose in our study during maximum apnea with PaO 2 of ∼ 4.8 kPa may underline that lactate is metabolized, when compared to the similar findings of Miller et al (2002) demonstrating lactate metabolization during exercise, following decreasing blood glucose metabolization: the pancreatic insulin producing beta-cells are sensitive to moderate hypoxia, causing decreasing insulin production ( Sato et al, 2014 ), and because pancreatic blood supply (from the splenic artery) has been demonstrated to remain stable during apnea ( Bakovíc et al, 2003 ), hypoxia seems to be the main factor affecting the stalled pancreatic insulin production, and hence increasing or more likely stabilizing blood glucose (may be secondarily to peripheral vasoconstriction) during apnea as in our study.…”

“…A 1.1 mm, 20-gauge catheter was inserted in the radial artery of the non-dominant arm connected to a transducer for continuous flow of saline (3 ml/h; Baxter, Uden, Netherlands) for blood pressure monitoring and for collection of blood glucose. Blood glucose analyses were performed immediately after sampling, using an automated self-calibrating blood gas machine (ABL 725, Radiometer, Copenhagen, Denmark) and evaluated for blood gases as well as described previously ( Kjeld et al, 2021 ).…”

“…In contrast, blackouts or even death may be the consequence of maximum apneas in elite breath-hold divers (BHD), despite a pronounced diving reflex ( Foster and Sheel, 2005 ; Kjeld et al, 2009 ; Buzzacott and Denoble, 2018 ) and also metabolic adaptions to hypoxia and hypercapnia similar to diving mammals ( Kjeld et al, 2009 , 2018 ). During maximum apneas of elite BHD, we have previously demonstrated that PET-CT-assessed myocardial blood flow increases markedly (by a factor of 2), whereas both PaO 2 decrease (to 4.3 kPa) and concomitantly circulating lactate levels decrease, indicating lactate metabolism ( Kjeld et al, 2021 ). Lactate metabolism during maximum exercise and apnea can also be demonstrated in high-altitude miners and Sherpas ( Ge et al, 1994 ; Moraga et al, 2019 ), dwelling at 3,440 to 4,243 m altitudes and having SaO 2 between 88 and 93% ( Jansen et al, 2007 ).…”

“… Miller et al (2002) demonstrated during aerobic exercise and lactate infusion that glucose was stable due to decreased metabolism. Therefore, assuming that the decreasing lactate during maximum apnea is indicative of lactate metabolization ( Kjeld et al, 2021 ), and if glucose is stable in elite BHD during maximum apnea, then hypoxia may be the key factor causing bradycardia, as the His bundle conduction system of the heart is very sensitive to both hypoxia and hypoglycemia ( James et al, 1966 ; Senges et al, 1980 ).…”