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Cardiac Hypoxic Resistance and Decreasing Lactate During Maximum www.nature.com/scientificreports OPEN Cardiac hypoxic resistance and decreasing lactate during maximum apnea in elite breath hold divers Thomas Kjeld1*, Jakob Møller 1, Kristian Fogh1, Egon Godthaab Hansen2, Henrik Christian Arendrup3, Anders Brenøe Isbrand4, Bo Zerahn4, Jens Højberg5, Ellen Ostenfeld6, Henrik Thomsen1, Lars Christian Gormsen 7 & Marcus Carlsson6 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 15 similar adaptive mechanisms. During maximum apnea O-H2O-PET/CT (n = 6) revealed no myocardial perfusion defcits but increased myocardial blood fow (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 fndings contrast with previous MR studies of BHD, that reported elevated cardiac troponins and decreased myocardial 15 perfusion after 4 min of apnea. In conclusion, we demonstrated for the frst time with O-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. Te physiological adaptions in breath hold divers (BHD) to apnea, includes signifcant diving responses, attenu- ated post-apnea acidosis, reduced sensitivity to oxidative stress and, probably critical to their performances, reduced sensitivity to hypoxia1–6. It has also been demonstrated that similar to adaptions in the northern elephant seal, which can endure apnea for more than 120 min, BHD have a non-coupled maximum respiratory state in their skeletal muscles ~ 22–23% lower than matched aerobic athletes 7. Hence, the skeletal muscles of BHD possess an oxygen conserving adaptation, and this might—at least partly—explain, the extreme performances of BHD holding their breath for more than 11 min and swimming as far as 300 m, or diving beyond 200 m in depth, all on a single breath of air (http://www.freed ive-earth .com/aida-freed iving -world -recor ds). Similarly, 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-specifc 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, but also a high aerobic capacity for lipid metabolism within the heart 8. It could be hypothesized, that the hearts of BHD would possess similar adap- tions. However, two cardiac magnetic resonance imaging (CMR) studies of BHD reported that afer only 4 min of dry apnea concomitant with a reduction in arterial oxygen saturation ~ 23%, cardiac troponins increase, and 1Department of Radiology, Herlev Hospital, University of Copenhagen, Herlev Ringvej 75, 2730 Herlev, Denmark. 2Department of Anesthesiology, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark. 3Department of Cardiothoracic Surgery, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark. 4Department of Clinical Physiology and Nuclear Medicine, Herlev Hospital, University of Copenhagen, Copenhagen, Denmark. 5Department of Cardiothoracic Anesthesiology, Rigshospitalet, University of Copenhagen, Copenhagen, Denmark. 6Department of Clinical Sciences Lund, Lund University, Skåne University Hospital, Lund, Sweden. 7Department of Nuclear Medicine & PET Centre, Aarhus University Hospital, Aarhus, Denmark. *email: [email protected] Scientifc Reports | (2021) 11:2545 | https://doi.org/10.1038/s41598-021-81797-1 1 Vol.:(0123456789) www.nature.com/scientificreports/ CMR epicardial perfusion decreases about 60%9,10. We have reported of elite BHD enduring a reduced arterial oxygen saturation of more than ~ 33%4, and afer competitions with pool static apneas of ~ 5 min (and subsequent 88 ± 21 m underwater swim), where cardiac troponins remains unchanged normal11. Te explanation might be, that BHD who can endure apnea for more than 4 min have a lesser increase in ischemia-modifed albumin (IMA), a marker of the release of reactive oxygen species (ROS) and a measure of resistance to hypoxemia, than compared to BHD who can endure less than 4 min of apnea12. Tis is in accordance with studies of adult seals are demonstrated to have a higher relative capacity for mitochondrial respiration than pups and juvenile seals13, and adult diving mammals also have resistance to release of ROS during dives to tolerate ischemia14,15, indicating that the hypoxic capacity is an adaption. Hence, it is hypothesized that similar adaptive mechanisms to hypoxia as observed in the hearts of adult div- ing mammals could be observed in the hearts of human elite BHD, who can endure apnea for more than 4 min. Tis study aimed to demonstrate this hypothesized adaptation in BHD. As myocardial ischemia is dependent on both blood oxygen levels, perfusion and the need of oxygen based on cardiac contraction, these parameters were 15 quantifed using arterial samples, cine CMR and O-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. Methods Tis study included eight Danish healthy male non-smoking subjects and was approved by the Regional Ethics Committee of Copenhagen (H-1-2013-060). All clinical investigations were conducted according to the principles expressed in the Declaration of Helsinki. Informed consent, written and oral, were obtained from the participants. All subjects were elite BHD (age 42 ± 8 years) able to hold their breath for more than 5 min and ranked among the national top 10. Tree ranked among the World top 10, one was a 2016 outdoor free-diving World champion, one reached third place at the same championship (no limit depth competition), and one was a World record holder. VO2 max measurement and dual-energy X-ray absorptiometry scan. Subjects completed a stand- ardized warm-up followed by an incremental cycling test starting at a workload of 150 W and increasing 25 W every minute until voluntary exhaustion. Pulmonary O2 and CO2 concentrations in the expired gas were con- tinuously measured breath-by-breath (Quark, Cosmed, Rome, Italy) during the test. Te highest recorded 30 s average oxygen uptake (VO 2) during the test was defned as VO 2max. For recognition of true VO 2max three of fve criteria had to be met: individual perception of exhaustion, respiratory exchange ratio > 1.15, plateau of VO 2 curve, heart rate approaching age-predicted maximum and inability to maintain a pedaling frequency above 70 rpm. A dual-energy X-ray absorptiometry scan (Lunar iDXA; Lunar, Madison, WI, USA) was performed to assess body composition. Cardiac magnetic resonance imaging (CMR). Image acquisition. For one day prior to the study, the subjects refrained from physical exercise and consumption of alcohol or cafeine. Imaging was performed in a 1.5 T MR imaging system (Achieva, Philips Medical System, Te Netherlands) afer a warm-up of three consecu- tive apnea to maximize the diving response 4. Cine images were acquired at (1) rest during a short (< 20 s) apnea at end-expiration with open pharynx, (2) end of a apnea with max expiration and (3) the end of dry static apnea afer glossopharyngeal insufation (GPI)16. Images were collected shortly before end of apnea before breath- ing, and subjects were instructed to stay as calm as possible during imaging to avoid imaging artefacts. Cardiac chamber volumes and function were collected in the transversal and double-oblique short axis stacks with 8 mm thick slices and 25% gap. Cine imaging were performed with retrospectively ECG-gated steady-state free preces- sion sequences (SSFP) reconstructed to 25 phases covering the entire cardiac cycle using the following settings: TR/TE 3.3/1.6 ms, fip angle 60°; and spatial resolution 1.3 × 1.3 × 8 mm3. For blood oxygen level dependence (BOLD) imaging a fast gradient-echo multi-echo black blood T2* sequence was used in the short axis plane17,18. Te BOLD sequences were acquired at rest and afer 240 s of apnea, to ensure image collection on all subjects, as the duration of this could be up to 20 s. BOLD had the following settings: TR 25.8 ms with efective repeti- tion time 1600 ms and collecting 14 images with TE from 3.2 to 24.1 ms, fip angle 20°; and spatial resolution 1 × 2 × 1.2 × 8 mm3. Image analysis. Lef and right ventricular (LV and RV) and atrial (LA and RA) volumes were determined in end-diastole (ED) and end-systole (ES) and used to determine the infuence of apnea on cardiac volumes, func- tion, flling and individual chamber outfow. Data were analyzed by one experienced level three CMR reader and one level one CMR cardiologist using dedicated sofware (Segment version 2.1) carefully avoiding image artefacts and imaging especially during involuntary breathing movements19. LV wall thickness (LVWT) was determined from a midventricular short-axis slice from the epicardial and endocardial borders delineations of the lef ventricle at end-diastole. Stroke volume (SV) was computed as the diference between end diastolic volume (EDV) and end systolic volume (ESV). Ejection fractions were computed as SV divided by EDV. T2* was determined from the BOLD images using a LV septal midwall region of interest carefully avoiding image artefacts and using a ftting algorithm in the Segment sofware as previously described20.
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