Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals

Background: Recent research indicates that both endocannabinoids (eCB) and heart rate variability (HRV) are associated with stress-induced experiences. However, these underlying mech-anisms are not elucidated. The present study aims to investigate whether exposure to acute and chronic stress conditi...

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Autores:
Mourtakos, Stamatis
Vassiliou, Georgia
Kontoangelos, Konstantinos
Philippou, Anastassios
Tzavellas, Elias
Tornero Aguilera, José Francisco
Clemente-Suárez, Vicente Javier
Papageorgiou, Charalabos
Sidossis, Labros S.
Papageorgiou, Christos
Tipo de recurso:
Article of journal
Fecha de publicación:
2021
Institución:
Corporación Universidad de la Costa
Repositorio:
REDICUC - Repositorio CUC
Idioma:
eng
OAI Identifier:
oai:repositorio.cuc.edu.co:11323/9274
Acceso en línea:
https://hdl.handle.net/11323/9274
https://doi.org/10.3390/ijerph19010028
https://repositorio.cuc.edu.co/
Palabra clave:
Endocannabinoids
Heart rate variability
Acute stress
Physical exercise
Special forces
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openAccess
License
Atribución 4.0 Internacional (CC BY 4.0)
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repository_id_str
dc.title.eng.fl_str_mv Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
title Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
spellingShingle Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
Endocannabinoids
Heart rate variability
Acute stress
Physical exercise
Special forces
title_short Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
title_full Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
title_fullStr Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
title_full_unstemmed Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
title_sort Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy seals
dc.creator.fl_str_mv Mourtakos, Stamatis
Vassiliou, Georgia
Kontoangelos, Konstantinos
Philippou, Anastassios
Tzavellas, Elias
Tornero Aguilera, José Francisco
Clemente-Suárez, Vicente Javier
Papageorgiou, Charalabos
Sidossis, Labros S.
Papageorgiou, Christos
dc.contributor.author.spa.fl_str_mv Mourtakos, Stamatis
Vassiliou, Georgia
Kontoangelos, Konstantinos
Philippou, Anastassios
Tzavellas, Elias
Tornero Aguilera, José Francisco
Clemente-Suárez, Vicente Javier
Papageorgiou, Charalabos
Sidossis, Labros S.
Papageorgiou, Christos
dc.subject.proposal.eng.fl_str_mv Endocannabinoids
Heart rate variability
Acute stress
Physical exercise
Special forces
topic Endocannabinoids
Heart rate variability
Acute stress
Physical exercise
Special forces
description Background: Recent research indicates that both endocannabinoids (eCB) and heart rate variability (HRV) are associated with stress-induced experiences. However, these underlying mech-anisms are not elucidated. The present study aims to investigate whether exposure to acute and chronic stress conditions can give rise to measurable changes, both to the peripheral eCB ligands and HRV. Methods: Thirteen candidates under intense preparation for their enlistment in the Hellenic Navy SEALs (HNS) participated in the study. All subjects underwent mental state examination, while HRV variables in time and frequency domain recordings were acquired. Furthermore, at baseline and 30 days after prolonged and intensive physical exercise, hair was collected to measure eCB ligands, such as anandamide (AEA), 2-arachidonoylglycerol (2-AG), and the N-acyl ethanolamine (NAE) molecules: palmitoylethanolamide (PEA) and oleoylethanolamide (OEA). Results: Comparing basal hair concentrations of eCB ligands before and after intense physical exercise, we found that AEA, PEA, and OEA were notably increased, whereas no differences were observed regarding the ligand 2-AG. Furthermore, there were observed associations between the concentrations of peripheral eCB ligands, both at baseline and after the prolonged physical exercise and the time and frequency domains of HRV. Conclusions: These findings suggest that endocannabinoid–HRV interrelations might share a short-term, and long-term adaptability of the changes in self-regulation associated with stress. Further studies will be required to determine the validity of peripheral eCB signaling and HRV as a biomarker for different aspects of the stress response. © 2021 by the authors. Licensee MDPI, Basel, Switzerland.
publishDate 2021
dc.date.issued.none.fl_str_mv 2021-12-21
dc.date.accessioned.none.fl_str_mv 2022-06-21T15:38:08Z
dc.date.available.none.fl_str_mv 2022-06-21T15:38:08Z
dc.type.spa.fl_str_mv Artículo de revista
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dc.type.content.spa.fl_str_mv Text
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dc.identifier.issn.spa.fl_str_mv 1661-7827
dc.identifier.uri.spa.fl_str_mv https://hdl.handle.net/11323/9274
dc.identifier.url.spa.fl_str_mv https://doi.org/10.3390/ijerph19010028
dc.identifier.doi.spa.fl_str_mv 10.3390/ijerph19010028
dc.identifier.eissn.spa.fl_str_mv 1660-4601
dc.identifier.instname.spa.fl_str_mv Corporación Universidad de la Costa
dc.identifier.reponame.spa.fl_str_mv REDICUC - Repositorio CUC
dc.identifier.repourl.spa.fl_str_mv https://repositorio.cuc.edu.co/
identifier_str_mv 1661-7827
10.3390/ijerph19010028
1660-4601
Corporación Universidad de la Costa
REDICUC - Repositorio CUC
url https://hdl.handle.net/11323/9274
https://doi.org/10.3390/ijerph19010028
https://repositorio.cuc.edu.co/
dc.language.iso.none.fl_str_mv eng
language eng
dc.relation.ispartofjournal.spa.fl_str_mv International Journal of Environmental Research and Public Health
dc.relation.references.spa.fl_str_mv 1. Galve-Roperh, I.; Chiurchiù, V.; Díaz-Alonso, J.; Bari, M.; Guzmán, M.; Maccarrone, M. Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Prog. Lipid Res. 2013, 52, 633–650. [CrossRef] [PubMed]
2. Wei, D.; Allsop, S.; Tye, K.; Piomelli, D. Endocannabinoid Signaling in the Control of Social Behavior. Trends Neurosci. 2017, 40, 385–396. [CrossRef] [PubMed]
3. Raso, G.M.; Russo, R.; Calignano, A.; Meli, R. Palmitoylethanolamide in CNS health and disease. Pharmacol. Res. 2014, 86, 32–41. [CrossRef] [PubMed]
4. Thabuis, C.; Tissot-Favre, D.; Bezelgues, J.B.; Martin, J.C.; Cruz-Hernandez, C.; Dionisi, F.; Destaillats, F. Biological functions and metabolism of oleoylethanolamide. Lipids 2008, 43, 887. [CrossRef] [PubMed]
5. Ueda, N.; Tsuboi, K.; Uyama, T. Metabolism of endocannabinoids and relatedN-acylethanolamines: Canonical and alternative pathways. FEBS J. 2013, 280, 1874–1894. [CrossRef] [PubMed]
6. Morena, M.; Patel, S.; Bains, J.; Hill, M.N. Neurobiological Interactions Between Stress and the Endocannabinoid System. Neuropsychopharmacology 2015, 41, 80–102. [CrossRef] [PubMed]
7. Wilker, S.; Pfeiffer, A.; Elbert, T.; Ovuga, E.; Karabatsiakis, A.; Krumbholz, A.; Thieme, D.; Schelling, G.; Kolassa, I.-T. Endocannabinoid concentrations in hair are associated with PTSD symptom severity. Psychoneuroendocrinology 2016, 67, 198–206. [CrossRef]
8. Koenig, A.M.; Gao, W.; Umlauft, M.; Schury, K.; Reister, F.; Kirschbaum, C.; Karabatsiakis, A.; Kolassa, I.T. Altered hair endocannabinoid levels in mothers with childhood maltreatment and their newborns. Biol. Psychol. 2018, 135, 93–101. [CrossRef] [PubMed]
9. Krumbholz, A.; Anielski, P.; Reisch, N.; Schelling, G.; Thieme, D. Diagnostic Value of Concentration Profiles of Glucocorticosteroids and Endocannabinoids in Hair. Ther. Drug Monit. 2013, 35, 600–607. [CrossRef] [PubMed]
10. Škopek, M.; Heidler, J.; Hnizdil, J.; Šulc, J. The effect of cannabidiol (CBD) on simple and complex reaction times. Trends Sport Sci. 2021, 28, 147–151.
11. Ho, W.S.; Kelly, M.E. Cannabinoids in the cardiovascular system. Adv. Pharmacol. 2017, 80, 329–366.
12. Dugrenot, E.; Balestra, C.; Gouin, E.; L’Her, E.; Guerrero, F. Physiological effects of mixed-gas deep sea dives using a closed-circuit rebreather: A field pilot study. Eur. J. Appl. Physiol. 2021, 121, 3323–3331. [CrossRef] [PubMed]
13. Bustamante-Sánchez, A.; Tornero-Aguilera, J.F.; Fernández-Elías, V.E.; Hormeño-Holgado, A.J.; Dalamitros, A.A.; ClementeSuárez, V.J. Effect of Stress on Autonomic and Cardiovascular Systems in Military Population: A Systematic Review. Cardiol. Res. Pract. 2020, 2020, 7986249. [CrossRef] [PubMed]
14. Lafère, P.; Lambrechts, K.; Germonpré, P.; Balestra, A.; Germonpré, F.L.; Marroni, A.; Cialoni, D.; Bosco, G.; Balestra, C. Heart Rate Variability During a Standard Dive: A Role for Inspired Oxygen Pressure? Front. Physiol. 2021, 12, 1060. [CrossRef] [PubMed]
15. Järvelin-Pasanen, S.; Sinikallio, S.; Tarvainen, M.P. Heart rate variability and occupational stress—Systematic review. Ind. Health 2018, 56, 500–511. [CrossRef] [PubMed]
16. Thayer, J.F.; Åhs, F.; Fredrikson, M.; Sollers, J.J., III; Wager, T.D. A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neurosci. Biobehav. Rev. 2012, 36, 747–756. [CrossRef]
17. Smith, R.; Thayer, J.F.; Khalsa, S.S.; Lane, R.D. The hierarchical basis of neurovisceral integration. Neurosci. Biobehav. Rev. 2017, 75, 274–296. [CrossRef]
18. Donias, S.; Karastergiou, A.; Manos, N. Validation of Symptom Checklist 90 R in the Greek population. Psychiatriki 1991, 2, 42–48.
19. Sauvé, B.; Koren, G.; Walsh, G.; Tokmakejian, S.; van Uum, S.H. Measurement of cortisol in human hair as a biomarker of systemic exposure. Clin. Investig. Med. 2007, 30, E183–E191. [CrossRef] [PubMed]
20. Kirschbaum, C.; Tietze, A.; Skoluda, N.; Dettenborn, L. Hair as a retrospective calendar of cortisol production—Increased cortisol incorporation into hair in the third trimester of pregnancy. Psychoneuroendocrinology 2009, 34, 32–37. [CrossRef]
21. Gao, W.; Stalder, T.; Foley, P.; Rauh, M.; Deng, H.; Kirschbaum, C. Quantitative analysis of steroid hormones in human hair using a column-switching LC–APCI–MS/MS assay. J. Chromatogr. B 2013, 928, 1–8. [CrossRef] [PubMed]
22. Manenschijn, L.; Koper, J.W.; Lamberts, S.W.; van Rossum, E.F. Evaluation of a method to measure long term cortisol levels. Steroids 2011, 76, 1032–1036. [CrossRef]
23. Noppe, G.; De Rijke, Y.B.; Dorst, K.; van den Akker, E.L.T.; Van Rossum, E.F.C. LC-MS/MS-based method for long-term steroid profiling in human scalp hair. Clin. Endocrinol. 2015, 83, 162–166. [CrossRef] [PubMed]
24. Voegel, C.D.; Baumgartner, M.R.; Kraemer, T.; Wüst, S.; Binz, T.M. Simultaneous quantification of steroid hormones and endocannabinoids (ECs) in human hair using an automated supported liquid extraction (SLE) and LC-MS/MS—Insights into EC baseline values and correlation to steroid concentrations. Talanta 2021, 222, 121499. [CrossRef] [PubMed]
25. Hill, M.N.; Miller, G.E.; Carrier, E.J.; Gorzalka, B.B.; Hillard, C.J. Circulating endocannabinoids and N-acyl ethanolamines are differentially regulated in major depression and following exposure to social stress. Psychoneuroendocrinology 2009,
26. Bluett, R.J.; Gamble-George, J.C.; Hermanson, D.J.; Hartley, N.D.; Marnett, L.J.; Patel, S. Central anandamide deficiency predicts stress-induced anxiety: Behavioral reversal through endocannabinoid augmentation. Transl. Psychiatry 2014, 4, e408. [CrossRef]
27. Patel, S.; Cravatt, B.F.; Hillard, C.J. Synergistic Interactions between Cannabinoids and Environmental Stress in the Activation of the Central Amygdala. Neuropsychopharmacology 2004, 30, 497–507. [CrossRef] [PubMed]
28. Hill, M.N.; Kumar, S.A.; Filipski, S.B.; Iverson, M.; Stuhr, K.L.; Keith, J.M.; Cravatt, B.F.; Hillard, C.J.; Chattarji, S.; McEwen, B.S. Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdala microstructure. Mol. Psychiatry 2013, 18, 1125–1135. [CrossRef] [PubMed]
29. Hohmann, A.G.; Suplita, R.L.; Bolton, N.M.; Neely, M.H.; Fegley, D.; Mangieri, R.; Krey, J.F.; Walker, J.M.; Holmes, P.V.; Crystal, J.D.; et al. An endocannabinoid mechanism for stress-induced analgesia. Nature 2005, 435, 1108–1112. [CrossRef]
30. Morena, M.; Roozendaal, B.; Trezza, V.; Ratano, P.; Peloso, A.; Hauer, D.; Atsak, P.; Trabace, L.; Cuomo, V.; McGaugh, J.L.; et al. Endogenous cannabinoid release within prefrontal-limbic pathways affects memory consolidation of emotional training. Proc. Natl. Acad. Sci. USA 2014, 111, 18333–18338. [CrossRef] [PubMed]
31. Gorzalka, B.B.; Hill, M.N.; Hillard, C.J. Regulation of endocannabinoid signaling by stress: Implications for stress-related affective disorders. Neurosci. Biobehav. Rev. 2008, 32, 1152–1160. [CrossRef] [PubMed]
32. Katona, I.; Freund, T.F. Multiple Functions of Endocannabinoid Signaling in the Brain. Annu. Rev. Neurosci. 2012, 35, 529–558. [CrossRef]
33. Mechoulam, R.; Parker, L.A. The Endocannabinoid System and the Brain. Annu. Rev. Psychol. 2013, 64, 21–47. [CrossRef] [PubMed]
34. Gao, W.; Walther, A.; Wekenborg, M.; Penz, M.; Kirschbaum, C. Determination of endocannabinoids and N-acylethanolamines in human hair with LC-MS/MS and their relation to symptoms of depression, burnout, and anxiety. Talanta 2020, 217, 121006. [CrossRef]
35. Davis, M.P.; Behm, B.; Mehta, Z.; Fernandez, C. The Potential Benefits of Palmitoylethanolamide in Palliation: A Qualitative Systematic Review. Am. J. Hosp. Palliat. Med. 2019, 36, 1134–1154. [CrossRef] [PubMed]
36. Hillard, C.J. Circulating Endocannabinoids: From Whence Do They Come and Where are They Going? Neuropsychopharmacology 2018, 43, 155–172. [CrossRef] [PubMed]
37. Battistini, L.; Maccarrone, M. The Endocannabinoid System in Peripheral Lymphocytes as a Mirror of Neuroinflammatory Diseases. Curr. Pharm. Des. 2008, 14, 2370–2382. [CrossRef]
38. Ori, Z.; Monir, G.; Weiss, J.; Sayhouni, X.; Singer, D.H. Heart rate variability. Frequency domain analysis. Cardiol. Clin. 1992, 10, 499–533. [CrossRef]
39. Tornero-Aguilera, J.F.; Pelarigo, J.G.; Clemente-Suárez, V.J. Psychophysiological Intervention to Improve Preparedness in Military Special Operations Forces. Aerosp. Med. Hum. Perform. 2019, 90, 953–958. [CrossRef]
40. Hormeño-Holgado, A.J.; Nikolaidis, P.T.; Clemente-Suárez, V.J. Psychophysiological Patterns Related to Success in a Special Operation Selection Course. Front. Physiol. 2019, 10, 867. [CrossRef] [PubMed]
41. Hormeño-Holgado, A.J.; Clemente-Suárez, V.J. Psychophysiological Monitorization in a Special Operation Selection Course. J. Med. Syst. 2019, 43, 47. [CrossRef] [PubMed]
42. Sánchez-Molina, J.; Robles-Pérez, J.J.; Clemente-Suárez, V.J. Assessment of Psychophysiological Response and Specific Fine Motor Skills in Combat Units. J. Med. Syst. 2018, 42, 67. [CrossRef] [PubMed]
43. Sánchez-Molina, J.; Pérez, J.J.R.; Clemente-Suárez, V.J. Effect of Parachute Jump in the Psychophysiological Response of Soldiers in Urban Combat. J. Med. Syst. 2017, 41, 99. [CrossRef] [PubMed]
44. Aguilera, J.F.T.; Gil-Cabrera, J.; Clemente-Suárez, V.J. Determining the psychophysiological responses of military aircrew when exposed to acute disorientation stimuli. BMJ Mil. Health 2020. [CrossRef]
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spelling Mourtakos, StamatisVassiliou, GeorgiaKontoangelos, KonstantinosPhilippou, AnastassiosTzavellas, EliasTornero Aguilera, José FranciscoClemente-Suárez, Vicente JavierPapageorgiou, CharalabosSidossis, Labros S.Papageorgiou, Christos2022-06-21T15:38:08Z2022-06-21T15:38:08Z2021-12-211661-7827https://hdl.handle.net/11323/9274https://doi.org/10.3390/ijerph1901002810.3390/ijerph190100281660-4601Corporación Universidad de la CostaREDICUC - Repositorio CUChttps://repositorio.cuc.edu.co/Background: Recent research indicates that both endocannabinoids (eCB) and heart rate variability (HRV) are associated with stress-induced experiences. However, these underlying mech-anisms are not elucidated. The present study aims to investigate whether exposure to acute and chronic stress conditions can give rise to measurable changes, both to the peripheral eCB ligands and HRV. Methods: Thirteen candidates under intense preparation for their enlistment in the Hellenic Navy SEALs (HNS) participated in the study. All subjects underwent mental state examination, while HRV variables in time and frequency domain recordings were acquired. Furthermore, at baseline and 30 days after prolonged and intensive physical exercise, hair was collected to measure eCB ligands, such as anandamide (AEA), 2-arachidonoylglycerol (2-AG), and the N-acyl ethanolamine (NAE) molecules: palmitoylethanolamide (PEA) and oleoylethanolamide (OEA). Results: Comparing basal hair concentrations of eCB ligands before and after intense physical exercise, we found that AEA, PEA, and OEA were notably increased, whereas no differences were observed regarding the ligand 2-AG. Furthermore, there were observed associations between the concentrations of peripheral eCB ligands, both at baseline and after the prolonged physical exercise and the time and frequency domains of HRV. Conclusions: These findings suggest that endocannabinoid–HRV interrelations might share a short-term, and long-term adaptability of the changes in self-regulation associated with stress. Further studies will be required to determine the validity of peripheral eCB signaling and HRV as a biomarker for different aspects of the stress response. © 2021 by the authors. Licensee MDPI, Basel, Switzerland.10 páginasapplication/pdfengFrontiers Media S.A.SwitzerlandAtribución 4.0 Internacional (CC BY 4.0)© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccesshttp://purl.org/coar/access_right/c_abf2Endocannabinoids and heart rate variability alterations after exposure to prolonged intensive physical exercise of the hellenic navy sealsArtículo de revistahttp://purl.org/coar/resource_type/c_6501http://purl.org/coar/resource_type/c_2df8fbb1Textinfo:eu-repo/semantics/articlehttp://purl.org/redcol/resource_type/ARThttp://purl.org/coar/version/c_970fb48d4fbd8a85https://www.mdpi.com/1660-4601/19/1/28International Journal of Environmental Research and Public Health1. Galve-Roperh, I.; Chiurchiù, V.; Díaz-Alonso, J.; Bari, M.; Guzmán, M.; Maccarrone, M. Cannabinoid receptor signaling in progenitor/stem cell proliferation and differentiation. Prog. Lipid Res. 2013, 52, 633–650. [CrossRef] [PubMed]2. Wei, D.; Allsop, S.; Tye, K.; Piomelli, D. Endocannabinoid Signaling in the Control of Social Behavior. Trends Neurosci. 2017, 40, 385–396. [CrossRef] [PubMed]3. Raso, G.M.; Russo, R.; Calignano, A.; Meli, R. Palmitoylethanolamide in CNS health and disease. Pharmacol. Res. 2014, 86, 32–41. [CrossRef] [PubMed]4. Thabuis, C.; Tissot-Favre, D.; Bezelgues, J.B.; Martin, J.C.; Cruz-Hernandez, C.; Dionisi, F.; Destaillats, F. Biological functions and metabolism of oleoylethanolamide. Lipids 2008, 43, 887. [CrossRef] [PubMed]5. Ueda, N.; Tsuboi, K.; Uyama, T. Metabolism of endocannabinoids and relatedN-acylethanolamines: Canonical and alternative pathways. FEBS J. 2013, 280, 1874–1894. [CrossRef] [PubMed]6. Morena, M.; Patel, S.; Bains, J.; Hill, M.N. Neurobiological Interactions Between Stress and the Endocannabinoid System. Neuropsychopharmacology 2015, 41, 80–102. [CrossRef] [PubMed]7. Wilker, S.; Pfeiffer, A.; Elbert, T.; Ovuga, E.; Karabatsiakis, A.; Krumbholz, A.; Thieme, D.; Schelling, G.; Kolassa, I.-T. Endocannabinoid concentrations in hair are associated with PTSD symptom severity. Psychoneuroendocrinology 2016, 67, 198–206. [CrossRef]8. Koenig, A.M.; Gao, W.; Umlauft, M.; Schury, K.; Reister, F.; Kirschbaum, C.; Karabatsiakis, A.; Kolassa, I.T. Altered hair endocannabinoid levels in mothers with childhood maltreatment and their newborns. Biol. Psychol. 2018, 135, 93–101. [CrossRef] [PubMed]9. Krumbholz, A.; Anielski, P.; Reisch, N.; Schelling, G.; Thieme, D. Diagnostic Value of Concentration Profiles of Glucocorticosteroids and Endocannabinoids in Hair. Ther. Drug Monit. 2013, 35, 600–607. [CrossRef] [PubMed]10. Škopek, M.; Heidler, J.; Hnizdil, J.; Šulc, J. The effect of cannabidiol (CBD) on simple and complex reaction times. Trends Sport Sci. 2021, 28, 147–151.11. Ho, W.S.; Kelly, M.E. Cannabinoids in the cardiovascular system. Adv. Pharmacol. 2017, 80, 329–366.12. Dugrenot, E.; Balestra, C.; Gouin, E.; L’Her, E.; Guerrero, F. Physiological effects of mixed-gas deep sea dives using a closed-circuit rebreather: A field pilot study. Eur. J. Appl. Physiol. 2021, 121, 3323–3331. [CrossRef] [PubMed]13. Bustamante-Sánchez, A.; Tornero-Aguilera, J.F.; Fernández-Elías, V.E.; Hormeño-Holgado, A.J.; Dalamitros, A.A.; ClementeSuárez, V.J. Effect of Stress on Autonomic and Cardiovascular Systems in Military Population: A Systematic Review. Cardiol. Res. Pract. 2020, 2020, 7986249. [CrossRef] [PubMed]14. Lafère, P.; Lambrechts, K.; Germonpré, P.; Balestra, A.; Germonpré, F.L.; Marroni, A.; Cialoni, D.; Bosco, G.; Balestra, C. Heart Rate Variability During a Standard Dive: A Role for Inspired Oxygen Pressure? Front. Physiol. 2021, 12, 1060. [CrossRef] [PubMed]15. Järvelin-Pasanen, S.; Sinikallio, S.; Tarvainen, M.P. Heart rate variability and occupational stress—Systematic review. Ind. Health 2018, 56, 500–511. [CrossRef] [PubMed]16. Thayer, J.F.; Åhs, F.; Fredrikson, M.; Sollers, J.J., III; Wager, T.D. A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neurosci. Biobehav. Rev. 2012, 36, 747–756. [CrossRef]17. Smith, R.; Thayer, J.F.; Khalsa, S.S.; Lane, R.D. The hierarchical basis of neurovisceral integration. Neurosci. Biobehav. Rev. 2017, 75, 274–296. [CrossRef]18. Donias, S.; Karastergiou, A.; Manos, N. Validation of Symptom Checklist 90 R in the Greek population. Psychiatriki 1991, 2, 42–48.19. Sauvé, B.; Koren, G.; Walsh, G.; Tokmakejian, S.; van Uum, S.H. Measurement of cortisol in human hair as a biomarker of systemic exposure. Clin. Investig. Med. 2007, 30, E183–E191. [CrossRef] [PubMed]20. Kirschbaum, C.; Tietze, A.; Skoluda, N.; Dettenborn, L. Hair as a retrospective calendar of cortisol production—Increased cortisol incorporation into hair in the third trimester of pregnancy. Psychoneuroendocrinology 2009, 34, 32–37. [CrossRef]21. Gao, W.; Stalder, T.; Foley, P.; Rauh, M.; Deng, H.; Kirschbaum, C. Quantitative analysis of steroid hormones in human hair using a column-switching LC–APCI–MS/MS assay. J. Chromatogr. B 2013, 928, 1–8. [CrossRef] [PubMed]22. Manenschijn, L.; Koper, J.W.; Lamberts, S.W.; van Rossum, E.F. Evaluation of a method to measure long term cortisol levels. Steroids 2011, 76, 1032–1036. [CrossRef]23. Noppe, G.; De Rijke, Y.B.; Dorst, K.; van den Akker, E.L.T.; Van Rossum, E.F.C. LC-MS/MS-based method for long-term steroid profiling in human scalp hair. Clin. Endocrinol. 2015, 83, 162–166. [CrossRef] [PubMed]24. Voegel, C.D.; Baumgartner, M.R.; Kraemer, T.; Wüst, S.; Binz, T.M. Simultaneous quantification of steroid hormones and endocannabinoids (ECs) in human hair using an automated supported liquid extraction (SLE) and LC-MS/MS—Insights into EC baseline values and correlation to steroid concentrations. Talanta 2021, 222, 121499. [CrossRef] [PubMed]25. Hill, M.N.; Miller, G.E.; Carrier, E.J.; Gorzalka, B.B.; Hillard, C.J. Circulating endocannabinoids and N-acyl ethanolamines are differentially regulated in major depression and following exposure to social stress. Psychoneuroendocrinology 2009,26. Bluett, R.J.; Gamble-George, J.C.; Hermanson, D.J.; Hartley, N.D.; Marnett, L.J.; Patel, S. Central anandamide deficiency predicts stress-induced anxiety: Behavioral reversal through endocannabinoid augmentation. Transl. Psychiatry 2014, 4, e408. [CrossRef]27. Patel, S.; Cravatt, B.F.; Hillard, C.J. Synergistic Interactions between Cannabinoids and Environmental Stress in the Activation of the Central Amygdala. Neuropsychopharmacology 2004, 30, 497–507. [CrossRef] [PubMed]28. Hill, M.N.; Kumar, S.A.; Filipski, S.B.; Iverson, M.; Stuhr, K.L.; Keith, J.M.; Cravatt, B.F.; Hillard, C.J.; Chattarji, S.; McEwen, B.S. Disruption of fatty acid amide hydrolase activity prevents the effects of chronic stress on anxiety and amygdala microstructure. Mol. Psychiatry 2013, 18, 1125–1135. [CrossRef] [PubMed]29. Hohmann, A.G.; Suplita, R.L.; Bolton, N.M.; Neely, M.H.; Fegley, D.; Mangieri, R.; Krey, J.F.; Walker, J.M.; Holmes, P.V.; Crystal, J.D.; et al. An endocannabinoid mechanism for stress-induced analgesia. Nature 2005, 435, 1108–1112. [CrossRef]30. Morena, M.; Roozendaal, B.; Trezza, V.; Ratano, P.; Peloso, A.; Hauer, D.; Atsak, P.; Trabace, L.; Cuomo, V.; McGaugh, J.L.; et al. Endogenous cannabinoid release within prefrontal-limbic pathways affects memory consolidation of emotional training. Proc. Natl. Acad. Sci. USA 2014, 111, 18333–18338. [CrossRef] [PubMed]31. Gorzalka, B.B.; Hill, M.N.; Hillard, C.J. Regulation of endocannabinoid signaling by stress: Implications for stress-related affective disorders. Neurosci. Biobehav. Rev. 2008, 32, 1152–1160. [CrossRef] [PubMed]32. Katona, I.; Freund, T.F. Multiple Functions of Endocannabinoid Signaling in the Brain. Annu. Rev. Neurosci. 2012, 35, 529–558. [CrossRef]33. Mechoulam, R.; Parker, L.A. The Endocannabinoid System and the Brain. Annu. Rev. Psychol. 2013, 64, 21–47. [CrossRef] [PubMed]34. Gao, W.; Walther, A.; Wekenborg, M.; Penz, M.; Kirschbaum, C. Determination of endocannabinoids and N-acylethanolamines in human hair with LC-MS/MS and their relation to symptoms of depression, burnout, and anxiety. Talanta 2020, 217, 121006. [CrossRef]35. Davis, M.P.; Behm, B.; Mehta, Z.; Fernandez, C. The Potential Benefits of Palmitoylethanolamide in Palliation: A Qualitative Systematic Review. Am. J. Hosp. Palliat. Med. 2019, 36, 1134–1154. [CrossRef] [PubMed]36. Hillard, C.J. Circulating Endocannabinoids: From Whence Do They Come and Where are They Going? Neuropsychopharmacology 2018, 43, 155–172. [CrossRef] [PubMed]37. Battistini, L.; Maccarrone, M. The Endocannabinoid System in Peripheral Lymphocytes as a Mirror of Neuroinflammatory Diseases. Curr. Pharm. Des. 2008, 14, 2370–2382. [CrossRef]38. Ori, Z.; Monir, G.; Weiss, J.; Sayhouni, X.; Singer, D.H. Heart rate variability. Frequency domain analysis. Cardiol. Clin. 1992, 10, 499–533. [CrossRef]39. Tornero-Aguilera, J.F.; Pelarigo, J.G.; Clemente-Suárez, V.J. Psychophysiological Intervention to Improve Preparedness in Military Special Operations Forces. Aerosp. Med. Hum. Perform. 2019, 90, 953–958. [CrossRef]40. Hormeño-Holgado, A.J.; Nikolaidis, P.T.; Clemente-Suárez, V.J. Psychophysiological Patterns Related to Success in a Special Operation Selection Course. Front. Physiol. 2019, 10, 867. [CrossRef] [PubMed]41. Hormeño-Holgado, A.J.; Clemente-Suárez, V.J. Psychophysiological Monitorization in a Special Operation Selection Course. J. Med. Syst. 2019, 43, 47. [CrossRef] [PubMed]42. Sánchez-Molina, J.; Robles-Pérez, J.J.; Clemente-Suárez, V.J. Assessment of Psychophysiological Response and Specific Fine Motor Skills in Combat Units. J. Med. Syst. 2018, 42, 67. [CrossRef] [PubMed]43. Sánchez-Molina, J.; Pérez, J.J.R.; Clemente-Suárez, V.J. Effect of Parachute Jump in the Psychophysiological Response of Soldiers in Urban Combat. J. Med. Syst. 2017, 41, 99. [CrossRef] [PubMed]44. Aguilera, J.F.T.; Gil-Cabrera, J.; Clemente-Suárez, V.J. Determining the psychophysiological responses of military aircrew when exposed to acute disorientation stimuli. BMJ Mil. Health 2020. 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