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Effect of sleep efficiency on salivary metabolite profile and cognitive function during exercise in volleyball athletes

  • Nobuhiko Akazawa
  • Naoko Kobayashi
  • Yuki Nakamura
  • Hiroshi Kumagai
  • Youngju Choi
  • Seiji MaedaEmail author
Original Article

Abstract

Purpose

Sleep duration is known to affect physiological and circadian metabolites and human homeostasis. However, little is known about the relationship between sleep quality and metabolite and cognitive function during exercise. Therefore, the aim of the present study was to investigate the impact of sleep quality on metabolite level and cognitive function in female volleyball athletes.

Methods

Twelve female volleyball athletes participated in this study. Sleep efficiency was measured for 1 week using NemuriSCAN (Paramount Bed Co. Ltd., Japan) as an index of sleep quality. The subjects were divided into better (n = 6) and lesser (n = 6) sleep quality groups by the median value of sleep efficiency. Saliva samples were collected using a Salimetric oral swab cotton and salivary metabolites were analysed using capillary electrophoresis and time-of-flight mass spectrometry. The subjects performed Stroop tasks (simple and difficult tasks) at rest and during aerobic exercise in recumbent cycle ergometer at light and heavy intensity.

Results

Increased sleep efficiency was found in the better sleep quality group, whereas total sleep time was similar. There were differences in urea cycle and Krebs cycle metabolites between the two groups; their levels were correlated with sleep efficiency. The difficult-task response time during heavy exercise was faster in the better sleep quality group.

Conclusion

We demonstrated that sleep efficiency was associated with urea cycle and Krebs cycle metabolite levels and response time during heavy exercise in volleyball athletes. These results suggested that sleep quality may affect amino acid and energy metabolism and cognitive function during heavy exercise.

Keywords

Cognitive function Sleep efficiency Metabolome Athlete Exercise intensity 

Abbreviations

CE-TOFMS

Capillary electrophoresis and time-of-flight mass spectrometry

HRR

Heart rate reserve

NO

Nitric oxide

Notes

Author contributions

NA and SM conceived and designed research. NA and NK conducted experiments. NA, NK, YN, HK, and YC collected and analyzed data. NA wrote the manuscript. All authors read and approved the manuscript.

Funding

This study was supported by the Japan Society for the Promotion of Science KAKENHI, Grant Number 26282181.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Akazawa N, Hamasaki A, Tanahashi K, Kosaki K, Yoshikawa T, Myoenzono K, Maeda S (2018) Lactotripeptide ingestion increases cerebral blood flow velocity in middle-aged and older adults. Nutr Res 53:61–66CrossRefGoogle Scholar
  2. Axelsson J, Kecklund G, Akerstedt T, Donofrio P, Lekander M, Ingre M (2008) Sleepiness and performance in response to repeated sleep restriction and subsequent recovery during semi-laboratory conditions. Chronobiol Int 25:297–308CrossRefGoogle Scholar
  3. Bahri S, Curis E, El Wafi FZ, Aussel C, Chaumeli JC, Cynober L, Zerrouk N (2008) Mechanisms and kinetics of citrulline uptake in a model of human intestinal epithelial cells. Clin Nutr 27:872–880CrossRefGoogle Scholar
  4. Bailey SJ, Blackwell JR, Lord T, Vanhatalo A, Winyard PG, Jones AM (2015) l-Citrulline supplementation improves O2 uptake kinetics and high-intensity exercise performance in humans. J Appl Physiol 119:385–395CrossRefGoogle Scholar
  5. Bak LK, Schousboe A, Waagepetersen HS (2006) The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer. J Neurochem 98:641–653CrossRefGoogle Scholar
  6. Benedict C, Hallschmid M, Lassen A, Mahnke C, Schultes B, Schiöth HB, Bom J, Lage T (2011) Acute sleep deprivation reduces energy expenditure in healthy men. Am J Clin Nutr 93:1229–1236CrossRefGoogle Scholar
  7. Berton R, Conceição MS, Libardi CA, Canevarolo RR, Gaspari AF, Chacon-Mikahik MP, Zeri AC, Cavaglieri CR (2017) Metabolic time-course response after resistance exercise: a metabolomics approach. J Sports Sci 35:1211–1218CrossRefGoogle Scholar
  8. Borg G (1970) Perceived exertion as an indicator of somatic stress. Scand J Rehabil Med 2:92–98Google Scholar
  9. Bosoi CR, Rose CF (2009) Identifying the direct effects of ammonia on the brain. Metab Brain Dis 24:95–102CrossRefGoogle Scholar
  10. Chang YK, Labban JD, Gapin JI, Etnier JL (2012) The effects of acute exercise on cognitive performance: a meta-analysis. Brain Res 1453:87–101CrossRefGoogle Scholar
  11. Chiu CN, Chen CY, Muggleton NG (2017) Sport, time pressure, and cognitive performance. Prog Brain Res 234:85–99CrossRefGoogle Scholar
  12. Davies SK, Ang JE, Revell VL, Holmes B, Mann A, Robertson FP, Cui N, Middleton B, Ackermann K, Kayser M, Thumser AE, Raynaud FI, Skene DJ (2014) Effect of sleep deprivation on the human metabolome. Proc Natl Acad Sci USA 111:10761–10766CrossRefGoogle Scholar
  13. Drapeau C, Hamel-Hébert I, Robillard R, Selmaoui B, Filipini D, Carrier J (2006) Challenging sleep in aging: the effects of 200 mg of caffeine during the evening in young and middle-aged moderate caffeine consumers. J Sleep Res 15:133–141CrossRefGoogle Scholar
  14. Figueroa A, Alvarez-Alvarado S, Ormsbee MJ, Madzima TA, Campbell JC, Wong A (2015) Impact of l-citrulline supplementation and whole-body vibration training on arterial stiffness and leg muscle function in obese postmenopausal women with high blood pressure. Exp Gerontol 63:35–40CrossRefGoogle Scholar
  15. Fullagar HH, Skorski S, Duffield R, Hammes D, Coutts AJ, Meyer T (2015) Sleep and athletic performance: the effects of sleep loss on exercise performance, and physiological and cognitive responses to exercise. Sports Med 45:161–186CrossRefGoogle Scholar
  16. Glade MJ (2010) Caffeine—not just a stimulant. Nutrition 26:932–938CrossRefGoogle Scholar
  17. Heaney LM, Deighton K, Suzuki T (2019) Non-targeted metabolomics in sport and exercise science. J Sports Sci 37:959–967CrossRefGoogle Scholar
  18. Huang Z, Davis HH, Yue Q, Wiebking C, Duncan NW, Zhang J, Wagner NF, Wolff A, Northoss G (2015) Increase in glutamate/glutamine concentration in the medial prefrontal cortex during mental imagery: a combined functional MRS and fMRI study. Hum Brain Mapp 36:3204–3212CrossRefGoogle Scholar
  19. Hursel R, Rutters F, Gonnissen HK, Martens EA, Westerterp-Plantenga MS (2011) Effects of sleep fragmentation in healthy men on energy expenditure, substrate oxidation, physical activity, and exhaustion measured over 48 h in a respiratory chamber. Am J Clin Nutr 94:804–808CrossRefGoogle Scholar
  20. Jarraya S, Jarraya M, Chtourou H, Souissi N (2014) Effect of time of day and partial sleep deprivation on the reaction time and the attentional capacities of the handball goalkeeper. Biol Rhythm Res 45:183–191CrossRefGoogle Scholar
  21. Kant AK, Graubard BI (2014) Association of self-reported sleep duration with eating behaviors of American adults: NHANES 2005–2010. Am J Clin Nutr 100:938–947CrossRefGoogle Scholar
  22. Kayaba M, Park I, Iwayama K, Seya Y, Ogata H, Yajima K, Satoh M, Tokuyama K (2017) Energy metabolism differs between sleep stages and begins to increase prior to awakening. Metabolism 69:14–23CrossRefGoogle Scholar
  23. Kogure T, Shirakawa S, Shimokawa M, Hosokawa Y (2011) Automatic sleep/wake scoring from body motion in bed: validation of a newly developed sensor placed under a mattress. J Physiol Anthropol 30:103–109CrossRefGoogle Scholar
  24. Kurata K, Nagasawa M, Tomonaga S, Aoki M, Akiduki S, Morishita K, Denbow DM, Furuse M (2012) Orally administered l-ornithine reduces restraint stress-induced activation of the hypothalamic-pituitary-adrenal axis in mice. Neurosci Lett 506:287–291CrossRefGoogle Scholar
  25. Leeder J, Glaister M, Pizzoferro K, Dawson J, Pedlar C (2012) Sleep duration and quality in elite athletes measured using wristwatch actigraphy. J Sports Sci 30:541–545CrossRefGoogle Scholar
  26. Levine J, Barak Y, Gonzalves M, Szor H, Elizur A, Kofman O, Beimaker RF (1995) Double-blind, controlled trial of inositol treatment of depression. Am J Psychiatry 152:792–794CrossRefGoogle Scholar
  27. Lucas SJ, Ainslie PN, Murrell CJ, Thomas KN, Franz EA, Cotter JD (2012) Effect of age on exercise-induced alterations in cognitive executive function: relationship to cerebral perfusion. Exp Gerontol 47:541–551CrossRefGoogle Scholar
  28. Mah CD, Mah KE, Kezirian EJ, Dement WC (2011) The effect of sleep extension on the athletic performance of collegiate basketball players. Sleep 34(7):943–950CrossRefGoogle Scholar
  29. Mann DT, Williams AM, Ward P, Janelle CM (2007) Perceptual-cognitive expertise in sport: a meta-analysis. J Sport Exerc Psychol 29:457–478CrossRefGoogle Scholar
  30. Miyake M, Kirisako T, Kokubo T, Miura Y, Morishita K, Okamura H, Tsuda A (2014) Randomised controlled trial of the effects of l-ornithine on stress markers and sleep quality in healthy workers. Nutr J 13:53CrossRefGoogle Scholar
  31. Nakamura Y, Choi Y, Akazawa N, Park I, Kawana F, Satoh M, Tokuyama K, Maeda S (2019) Effect of bright-light exposure before sleep on human urine metabolite. J Phys Fit Sport Med 8:89–96CrossRefGoogle Scholar
  32. Ra SG, Maeda S, Higashino R, Imai T, Miyakawa S (2014) Metabolomics of salivary fatigue markers in soccer players after consecutive games. Appl Physiol Nutr Metab 39:1120–1126CrossRefGoogle Scholar
  33. Reilly T, Piercy M (1994) The effect of partial sleep deprivation on weight-lifting performance. Ergonomics 37:107–115CrossRefGoogle Scholar
  34. Romero MJ, Platt DH, Caldwell RB, Caldwell RW (2006) Therapeutic use of citrulline in cardiovascular disease. Cardiovasc Drug Rev 24(3–4):275–290CrossRefGoogle Scholar
  35. Sanchez-Ortuno M, Moore N, Taillard J, Valtat C, Leger D, Bioulac B, Philip P (2005) Sleep duration and caffeine consumption in a French middle-aged working population. Sleep Med 6:247–251CrossRefGoogle Scholar
  36. Santone C, Dinallo V, Paci M, D’Ottavio Barbato G, Bernardini S (2014) Saliva metabolomics by NMR for the evaluation of sport performance. J Pharm Biomed Anal 88:441–446CrossRefGoogle Scholar
  37. Soga T, Ueno Y, Naraoka H, Ohashi Y, Tomita M, Nishioka T (2002) Simultaneous determination of anionic intermediates for Bacillus subtilis metabolic pathways by capillary electrophoresis electrospray ionization mass spectrometry. Anal Chem 74:2233–2239CrossRefGoogle Scholar
  38. Spielmann N, Wong DT (2011) Saliva: diagnostics and therapeutic perspectives. Oral Dis 17:345–354CrossRefGoogle Scholar
  39. Taheri M, Arabameri E (2012) The effect of sleep deprivation on choice reaction time and anaerobic power of college student athletes. Asian J Sports Med 3:15–20CrossRefGoogle Scholar
  40. Takeda I, Stretch C, Barnaby P, Bhatnager K, Rankin K, Fu H, Weljie A, Jha N, Slupsky C (2009) Understanding the human salivary metabolome. NMR Biomed 22:577–584CrossRefGoogle Scholar
  41. Thun E, Bjorvatn B, Flo E, Harris A, Pallesen S (2015) Sleep, circadian rhythms, and athletic performance. Sleep Med Rev 23:1–9CrossRefGoogle Scholar
  42. Tsukamoto H, Takenaka S, Suga T, Tanaka D, Takeuchi T, Hamaoka T, Isaka T, Hashimoto T (2017) Effect of exercise intensity and duration on postexercise executive function. Med Sci Sport Exerc 49:774–784CrossRefGoogle Scholar
  43. van der Lee SJ, Teunissen CE, Pool R, Shipley MJ, Teumer A, Chouraki V, Melo van Lent D, Tynkkynen J, Fischer K, Hernesniemi J, Haller T, Singh-Manoux A, Verhoeven A, Willemsen G, de Leeuw FA, Wagner H, van Dongen J, Hertel J, Budde K, Willems van Dijk K, Weinhold L, Ikram MA, Pietzner M, Perola M, Wagner M, Friedrich N, Slagboom PE, Scheltens P, Yang Q, Gertzen RE, Egert S, Li S, Hankemeier T, van Beijsterveldt CEM, Vasan RS, Maier W, Peeters CFW, Jörgen Grabe H, Ramirez A, Seshadri S, Metspalu A, Kivimäki M, Salomaa V, Demirkan A, Boomsma DI, van der Flier WM, Amin N, van Duijn CM (2018) Circulating metabolites and general cognitive ability and dementia: evidence from 11 cohort studies. Alzheimers Dement 14:707–722CrossRefGoogle Scholar
  44. Walsh JK, Muehlbach MJ, Humm TM, Dickins QS, Sugerman JL, Schweitzer PK (1990) Effect of caffeine on physiological sleep tendency and ability to sustain wakefulness at night. Psychopharmacology 101:271–273CrossRefGoogle Scholar
  45. Watson EJ, Coates AM, Kohler M, Banks S (2016) Caffeine consumption and sleep quality in Australian adults. Nutrients 8:479CrossRefGoogle Scholar
  46. Xie L, Kang H, Xu Q, Chen MJ, Liao Y, Thiyagarajan M, O'Donnell J, Christensen DJ, Nicholson C, Iliff JJ, Takano T, Deane R, Nedergaard M (2013) Sleep derives metabolite clearance from the adult brain. Science 8(342):353–357Google Scholar
  47. Yabuki Y, Shioda N, Yamamoto Y, Shigano M, Kumagai K, Morita M, Fukunaga K (2013) Oral l-citrulline administration improves memory deficits following transient brain ischemia through cerebrovascular protection. Brain Res 1520:157–167CrossRefGoogle Scholar
  48. Yamano E, Sugimoto M, Hirayama A, Kume S, Yamato M, Jin G, Tajima S, Goda N, Iwai K, Yamaguti K, Kuratsune H, Soga T, Watanabe Y, Kataoka Y (2016) Index markers of chronic fatigue syndrome with dysfunction of TCA and urea cycles. Sci Rep 6:34990CrossRefGoogle Scholar
  49. Zaccagni L, Onisto N, Gualdi-Russo E (2009) Biological characteristics and ageing in former elite volleyball players. J Sci Med Sport 12:667–672CrossRefGoogle Scholar
  50. Zhang A, Sun H, Wang X (2012) Saliva metabolomics opens door to biomarker discovery, disease diagnosis, and treatment. Appl Biochem Biotechnol 168:1718–1727CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Nobuhiko Akazawa
    • 1
    • 2
  • Naoko Kobayashi
    • 3
  • Yuki Nakamura
    • 3
  • Hiroshi Kumagai
    • 2
    • 4
    • 5
  • Youngju Choi
    • 2
  • Seiji Maeda
    • 2
    Email author
  1. 1.Department of Sport SciencesJapan Institute of Sport SciencesTokyoJapan
  2. 2.Faculty of Health and Sport SciencesUniversity of TsukubaTsukubaJapan
  3. 3.Graduate School of Comprehensive Human SciencesUniversity of TsukubaTsukubaJapan
  4. 4.Graduate School of Health and Sports ScienceJuntendo UniversityInzaiJapan
  5. 5.Japan Society for the Promotion of ScienceTokyoJapan

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