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Serum concentrations of ketones increase after hand-ergometer exercise in persons with cervical spinal cord injuries: a preliminary prospective study

Spinal Cord volume 61, pages 139–144 (2023)Cite this article

Subjects

Abstract

Study design

Experimental study.

Objectives

To compare lipid profiles during moderate-intensity exercise between persons with cervical spinal cord injuries (SCIC) and able-bodied controls (AB).

Setting

Wakayama Medical University, Japan.

Methods

Six participants with SCIC and six AB performed 30-min arm-crank exercise at 50% VO2peak. Blood samples were collected before (PRE), immediately (POST), and 60 min after exercise (REC). Concentrations of serum free fatty acids ([FFA]s), total ketone bodies ([tKB]s), acetoacetic acid ([AcAc]s), insulin ([Ins]s), and plasma catecholamines and glucose ([Glc]p) were assessed.

Results

Catecholamine concentrations in SCIC were lower than AB throughout the experiment (P < 0.001) and remained unchanged, while increased at POST in AB (P < 0.01). [FFA]s remained unchanged in both groups with no differences between groups. [tKB]s in SCIC tended to increase at REC from PRE (P = 0.043), while remaining unchanged in AB (P > 0.42). [AcAc]s in SCIC increased at REC from PRE and POST (P < 0.01) while remaining unchanged in AB (interactions of Group × Time P = 0.014). [Glc]p and [Ins]s were comparable between the groups throughout the study.

Conclusion

Serum ketone bodies in SCIC increased after exercise while remaining unchanged in AB, suggesting that suppressed uptakes of serum ketone bodies from blood to the muscles in SCIC would partially contribute the increased serum ketones.

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Fig. 1: Plasma concentrations of adrenaline and noradrenaline.
Fig. 2: Serum concentrations.
Fig. 3: Plasma concentrations of glucose and serum concentrations of insulin.

Data availability

The dataset generated and analyzed during the current study is available from the corresponding author upon reasonable request.

References

  1. Yekutiel M, Brooks ME, Ohry A, Yarom J, Carel R. The prevalence of hypertension, ischaemic heart disease and diabetes in traumatic spinal cord injured patients and amputees. Paraplegia. 1989;27:58–62.

    CAS  Google Scholar 

  2. Office of Sports Promotion for the Disabled, Health and Sports Division, Japan Sports Agency. Report on "Project for the Promotion of Sports for Persons with Disabilities in Local Communities (Survey and Research on the Promotion of Sports Participation by Persons with Disabilities). Sasakawa Sports Foundation, Tokyo, 2018. (In Japanese).

  3. Guttmann L, Silver J, Wyndham CH. Thermoregulation in spinal man. J Physiol. 1958;142:406–19.

    Article  CAS  Google Scholar 

  4. Kjaer M, Dela F, Sørensen FB, Secher NH, Bangsbo J, Mohr T, et al. Fatty acid kinetics and carbohydrate metabolism during electrical exercise in spinal cord-injured humans. Am J Physiol Regul Integr Comp Physiol. 2001;281:R1492–8.

    Article  CAS  Google Scholar 

  5. Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R. Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord. 1997;35:86–91.

    Article  CAS  Google Scholar 

  6. Gilbert O, Croffoot JR, Taylor AJ, Nash M, Schomer K, Groah S. Serum lipid concentrations among persons with spinal cord injury - a systematic review and meta-analysis of the literature. Atherosclerosis. 2014;232:305–12.

    Article  CAS  Google Scholar 

  7. Puchalska P, Crawford PA. Multi-dimensional roles of ketone bodies in fuel metabolism, signaling, and therapeutics. Cell Metab. 2017;25:262–84.

    Article  CAS  Google Scholar 

  8. Lasko-McCarthey P, Davis JA. Protocol dependency of VO2max during arm cycle ergometry in males with quadriplegia. Med Sci Sports Exerc. 1991;23:1097–101.

    Article  CAS  Google Scholar 

  9. Sato C, Kamijo YI, Sakurai Y, Araki S, Sakata Y, Ishigame A, et al. Three-week exercise and protein intake immediately after exercise increases the 6-min walking distance with simultaneously improved plasma volume in patients with chronic cerebrovascular disease: a preliminary prospective study. BMC Sports Sci Med Rehabil. 2022;14:38.

    Article  Google Scholar 

  10. Kamijo Y, Takeno Y, Sakai A, Inaki M, Okumoto T, Itoh J, et al. Plasma lactate concentration and muscle blood flow during dynamic exercise with negative-pressure breathing. J Appl Physiol. 2000;89:2196–205.

    Article  CAS  Google Scholar 

  11. Kouda K, Furusawa K, Sugiyama H, Sumiya T, Ito T, Tajima F, et al. Does 20-min arm crank ergometer exercise increase plasma interleukin-6 in individuals with cervical spinal cord injury? Eur J Appl Physiol. 2012;112:597–604.

    Article  Google Scholar 

  12. Han I, Mukaimoto T, Ueda H, Kiyota H, Ohno M. Effects of intermittent bouts of aerobic exercise on oxygen consumption during and after exercise. NSSU J Sport Sci. 2012;1:1–7.

    Google Scholar 

  13. Martin Ginis KA, van der Scheer JW, Latimer-Cheung AE, Barrow A, Bourne C, Carruthers P, et al. Evidence-based scientific exercise guidelines for adults with spinal cord injury: an update and a new guideline. Spinal Cord. 2018;56:308–21.

    Article  Google Scholar 

  14. Karvonen MJ, Kentala E, Mustala O. The effects of training on heart rate: a longitudinal study. Ann Med Exp Biol Fenn. 1957;35:307–15.

    CAS  Google Scholar 

  15. Nishiyama K, Kamijo YI, van der Scheer JW, Kinoshita T, Goosey-Tolfrey VL, Hoekstra SP, et al. Lipid metabolism after mild cold stress in persons with a cervical spinal cord injury. Spinal Cord. 2022. https://doi.org/10.1038/s41393-022-00788-9.

  16. Zimmermann G, Bolter LM, Sluka R, Höller Y, Bathke AC, Thomschewski A, et al. Sample sizes and statistical methods in interventional studies on individuals with spinal cord injury: a systematic review. J Evid Based Med. 2019;12:200–8.

    Article  Google Scholar 

  17. Ranallo RF, Rhodes EC. Lipid metabolism during exercise. Sports Med. 1998;26:29–42.

    Article  CAS  Google Scholar 

  18. Kimber NE, Heigenhauser GJF, Spriet LL, Dyck DJ. Skeletal muscle fat and carbohydrate metabolism during recovery from glycogen-depleting exercise in humans. J Physiol. 2003;548:919–27.

    Article  CAS  Google Scholar 

  19. Gorgey AS, Dudley GA. Skeletal muscle atrophy and increased intramuscular fat after incomplete spinal cord injury. Spinal Cord. 2007;45:304–9.

    Article  CAS  Google Scholar 

  20. Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA. Intramuscular fat and glucose tolerance after spinal cord injury –a cross-sectional study. Spinal Cord. 2004;42:711–6.

    Article  CAS  Google Scholar 

  21. Shah PK, Stevens JE, Gregory CM, Pathare NC, Jayaraman A, Bickel SC, et al. Lower-extremity muscle cross-sectional area after incomplete spinal cord injury. Arch Phys Med Rehabil. 2006;87:772–8.

    Article  Google Scholar 

  22. Grabacka M, Pierzchalska M, Dean M, Reiss K. Regulation of ketone body metabolism and the role of PPARα. Int J Mol Sci. 2016;17:2093.

    Article  Google Scholar 

  23. Bauman WA, Adkins RH, Spungen AM, Waters RL. The effect of residual neurological deficit on oral glucose tolerance in persons with chronic spinal cord injury. Spinal Cord. 1999;37:765–71.

    Article  CAS  Google Scholar 

  24. Karlsson AK. Insulin resistance and sympathetic function in high spinal cord injury. Spinal Cord. 1999;37:494–500.

    Article  CAS  Google Scholar 

  25. Bluvshtein V, Korczyn AD, Pinhas I, Vered Y, Gelernter I, Catz A. Insulin resistance in tetraplegia but not in mid-thoracic paraplegia: is the mid-thoracic spinal cord involved in glucose regulation? Spinal Cord. 2011;49:648–52.

    Article  CAS  Google Scholar 

  26. Rodwell VW, Bender DA, Botham KM, et al. Overview of metabolism & the provision of metabolic fuels. In: Harper’s illustrated biochemistry. New York: McGraw-Hill Medical; 2015. p. 139–51.

  27. Dionyssiotis Y. Malnutrition in spinal cord injury: more than nutritional deficiency. J Clin Med Res. 2012;4:227–36.

    CAS  Google Scholar 

  28. Macdonald IA, Bennett T, Fellows IW. Catecholamines and the control of metabolism in man. Clin Sci. 1985;68:613–9.

    Article  CAS  Google Scholar 

  29. Arner P, Kriegholm E, Engfeldt P, Bolinder J. Adrenergic regulation of lipolysis in situ at rest and during exercise. J Clin Investig. 1990;85:893–8.

    Article  CAS  Google Scholar 

  30. Palmisano BT, Zhu L, Eckel RH, Stafford JM. Sex differences in lipid and lipoprotein metabolism. Mol Metab. 2018;15:45–55.

    Article  CAS  Google Scholar 

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Acknowledgements

We thank all participants for their cooperation in our study. We also appreciate the service of Dr. Sven Hoekstra, Ph.D. from Loughborough University for kindly editing this manuscript. Grants: Mitacs-Japan Society for the Promotion of Science (JSPS) Internship program in 2017 (FT as host supervisor to JA).

Funding

This study was supported by grants from Nachikatsuura Research Foundation (L1221) to FT and also supported by funding from the Japan Society for the Promotion of Science through JSPS Postdoctoral Fellowships for Research in Japan (Summer Program; ID# SP17401; 2017).

Author information

Authors and Affiliations

  1. Department of Rehabilitation Medicine, Wakayama Medical University, Wakayama, 641-8509, Japan

    Kazunari Nishiyama, Yukihide Nishimuara, Yoshi-ichiro Kamijo, Takashi Moriki, Yuki Mukai, Yasunori Umemoto, Ken Kouda, Takahiro Ogawa & Fumihiro Tajima

  2. Department of Rehabilitation Medicine, Iwate Medical University, Yahaba-cho, 028-3695, Japan

    Kazunari Nishiyama & Yukihide Nishimuara

  3. Medical Center for Health Promotion and Sports Science, Wakayama Medical University, Wakayama, 640-8033, Japan

    Yukihide Nishimuara, Jason S Au, Yoshi-ichiro Kamijo, Yuki Mukai, Yasunori Umemoto & Fumihiro Tajima

  4. Department of Kinesiology and Health Sciences, University of Waterloo, Waterloo, ON, N2L 3G1, Canada

    Jason S Au

  5. Department of Rehabilitation Medicine, Dokkyo Medical University Saitama Medical Center, Koshigaya, 343-8555, Japan

    Yoshi-ichiro Kamijo

  6. Chuzan Hospital Clinical Education and Research Center, Okinawa, 904-2151, Japan

    Takahiro Ogawa

  7. Department of Rehabilitation Medicine, Aichi Medical University, Aichi, 480-1195, Japan

    Takahiro Ogawa

Authors
  1. Kazunari Nishiyama
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Contributions

KN, Y-iK, YN, and FT conceived and designed research; KN, Y-iK, JSA, TM, YM, YU, KK, and TO performed the experiments; KN and Y-iK analyzed the data; KN, Y-iK, JSA, YN, and FT interpreted the results; KN prepared the figures; KN and Y-iK drafted the manuscript; all authors edited and revised the manuscript; all authors approved the final version of the manuscript.

Corresponding author

Correspondence to Yukihide Nishimuara.

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Competing interests

The authors declare no competing interests.

Ethics

The study protocol and the methods applied in this study conformed to the guidelines of the Declaration of Helsinki and were approved by the Review Board on Human Experiments, Wakayama Medical University.

Informed consent

Informed consent for inclusion in this study was obtained from the participants.

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Nishiyama, K., Nishimuara, Y., Au, J.S. et al. Serum concentrations of ketones increase after hand-ergometer exercise in persons with cervical spinal cord injuries: a preliminary prospective study. Spinal Cord 61, 139–144 (2023). https://doi.org/10.1038/s41393-022-00859-x

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