Regulation of glucose turnover and hormonal responses during electrical cycling in tetraplegic humans
Abstract
To examine the importance of blood-borne vs. neural mechanisms for hormonal responses and substrate mobilization during exercise, six spinal cord-injured tetraplegic (C5-T1) males (mean age: 35 yr, range: 24-55 yr) were recruited to perform involuntary, electrically induced cycling [functional electrical stimulation (FES)] to fatigue for 24.6 +/- 2.3 min (mean and SE), and heart rate rose from 67 +/- 7 (rest) to 107 +/- 5 (exercise) beats/min. Voluntary arm cranking in tetraplegics (ARM) and voluntary leg cycling in six matched, long-term immobilized (2-12 mo) males (Vol) served as control experiments. In FES, peripheral glucose uptake increased [12.4 +/- 1.1 (rest) to 19.5 +/- 4.3 (exercise) mumol.min-1.kg-1; P < 0.05], whereas hepatic glucose production did not change from basal values [12.4 +/- 1.4 (rest) vs. 13.0 +/- 3.4 (exercise) mumol.min-1.kg-1]. Accordingly, plasma glucose decreased [from 5.4 +/- 0.3 (rest) to 4.7 +/- 0.3 (exercise) mmol/l; P < 0.05]. Plasma glucose did not change in response to ARM or Vol. Plasma free fatty acids and beta-hydroxybutyrate decreased only in FES experiments (P < 0.05). During FES, increases in growth hormone (GH) and epinephrine and decreases in insulin concentrations were abolished. Although subnormal throughout the exercise period, norepinephrine concentrations increased during FES, and responses of heart rate, adrenocorticotropic hormone, beta-endorphin, renin, lactate, and potassium were marked. In conclusion, during exercise, activity in motor centers and afferent muscle nerves is important for normal responses of GH, catecholamines, insulin, glucose production, and lipolysis. Humoral feedback and spinal or simple autonomic nervous reflex mechanisms are not sufficient. However, such mechanisms are involved in redundant control of heart rate and neuroendocrine activity in exercise.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
This concept was established after a study with electrical stimulation in paralyzed muscles, in which it was verified that the capacity of muscle contractions in modulating other tissues occurs through an independent pathway of activation of the nervous system.
“This concept was established after a study with electrical stimulation in paralyzed muscles, in which it was verified that the capacity of muscle contractions in modulating other tissues occurs through an independent pathway of activation of the nervous system (Kjaer et al., 1996).”
From Physical Exercise-Induced Myokines and Muscle-Adipose Tissue Crosstalk: A Review of Current Knowledge and the Implications for Health and Metabolic Diseases (2018) · cites this paper as Kjaer et al., 1996
Cited by
Sorted by citations
Pedersen, B. K. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.048074 · Cited by 668 · see citing works
“The idea that signalling pathways from contracting muscles to other organs are not solely mediated via the nervous system was supported by findings from electrical stimulation of paralysed muscles in spinal cord-injured patients (Kjaer et al., 1996).”
BackgroundLeal, L. G., Lopes, M. A., & Batista, M. L. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01307 · Cited by 382 · see citing works
“This concept was established after a study with electrical stimulation in paralyzed muscles, in which it was verified that the capacity of muscle contractions in modulating other tissues occurs through an independent pathway of activation of the nervous system (Kjaer et al., 1996).”
BackgroundEdward F. Adolph Distinguished Lecture: Muscle as an endocrine organ: IL-6 and other myokines
Pedersen, B. K. (2009) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00734.2009 · Cited by 214 · see citing works
“The idea that signaling pathways from contracting muscles to other organs were not solely mediated via the nervous system was supported by the findings from electrical stimulation of paralyzed muscles in patients with spinal cord injuries (45).”
Hamada, T., Sasaki, H., Hayashi, T., Moritani, T., & Nakao, K. (2003) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00486.2002 · Cited by 96 · see citing works
Exercise effects on postprandial glucose metabolism in type 1 diabetes: a triple-tracer approach
Mallad, A., Hinshaw, L., Schiavon, M., Dalla Man, C., Dadlani, V., Basu, R., Lingineni, R., Cobelli, C., Johnson, M. L., Carter, R., et al. (2015) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00014.2015 · Cited by 94 · see citing works
“, lactate, free fatty acids), or potential blood-borne feedback and afferent mechanisms that have been shown more recently to modulate glucose Ra (6, 18, 19).”
BackgroundMethodJeon, J. Y., Weiss, C., Steadward, R., Ryan, E. A., Burnham, R., Bell, G. J., Chilibeck, P. D., & Wheeler, G. (2002) · Spinal Cord · doi:10.1038/sj.sc.3101260 · Cited by 86 · see citing works
Role of the sympathoadrenergic system in adipose tissue metabolism during exercise in humans
Stallknecht, B. M., Lorentsen, J., Enevoldsen, L. H., Bülow, J., Biering‐Sørensen, F., Galbo, H., & Kjær, M. (2001) · The Journal of Physiology · doi:10.1111/j.1469-7793.2001.00283.x · Cited by 83 · see citing works
“Journal of Physiology (2001), 536.1, pp.283–29412631 283 (Krum et al. 1990), as well as impaired release of adrenaline from the adrenal medulla (Schmid et al. 1998).”
BackgroundInfluentialSelf-citationKjær, M., Hanel, B., Worm, L., Perko, G., Lewis, S. F., Sahlin, K., Galbo, H., & Secher, N. H. (1999) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1999.277.1.r76 · Cited by 80 · see citing works
Self-citationCaffeine ingestion and metabolic responses of tetraplegic humans during electrical cycling
Mohr, T. T., van Soeren, M., Graham, T. E., & Kjær, M. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.85.3.979 · Cited by 76 · see citing works
“In the present study the plasma catecholamine concentrations were subnormal, in agreement with previous reports (1, 18, 25, 34).”
BackgroundResultSelf-citationGrowth hormone responses to sub-maximal and sprint exercise
Stokes, K. (2003) · Growth Hormone & IGF Research · doi:10.1016/s1096-6374(03)00016-9 · Cited by 67 · see citing works
Spinal cord injury and physical activity: preservation of the body
Galea, M. P. (2011) · Spinal Cord · doi:10.1038/sc.2011.149 · Cited by 63 · see citing works
Glucoregulation During Exercise: The Role of the Neuroendocrine System
Coker, R. H., & Kjaer, M. (2005) · Sports Medicine · doi:10.2165/00007256-200535070-00003 · Cited by 60 · see citing works
Self-citationIrisin and Autophagy: First Update
Pesce, M., Ballerini, P., Paolucci, T., Puca, I., Farzaei, M. H., & Patruno, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207587 · Cited by 59 · see citing works
“It was supported by previous study with electrical stimulation in paralyzed muscles, in which Kjaer and coworkers verified that the ability of muscle contractions in regulating other tissues occurs through an independent pathway of activation of the nervous system [35].”
ResultWaldauf, P., Hrušková, N., Blahutová, B., et al. (2021) · Thorax · doi:10.1136/thoraxjnl-2020-215755 · Cited by 54 · see citing works
“29 30 In a pilot study, FESCE seems to be safe and feasible in the critically ill. 31 In the light of this we aimed to test early FESCE-based proto-colised rehabilitation in a randomised controlled trial powered to test treatment effects on patient-centred outcomes.”
Droujinine, I. A., & Perrimon, N. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00082 · Cited by 46 · see citing works
“Importantly, blood-borne signals mediate critical systemic homeostatic adjustments from local perturbations, illustrated by control of systemic physiology by electrical cycling of paralyzed muscles in spinal-cord injured tetraplegic humans (Kjaer et al., 1996; Pedersen, 2011).”
BackgroundFunctional electrical stimulation in neurological disorders
Sujith, O. K. (2008) · European Journal of Neurology · doi:10.1111/j.1468-1331.2008.02127.x · Cited by 46 · see citing works
“Mean serum testosterone levels significantly increased with FES-assisted resistance training in SCI and no significant changes were noted in hematocrit, sex hormone binding globulin, Prolactin, epinephrine, and cortisol levels [48,49].”
BackgroundBresnahan, J. J., Farkas, G. J., Clasey, J. L., Yates, J. W., & Gater, D. R. (2018) · Journal of Spinal Cord Medicine · doi:10.1080/10790268.2017.1412562 · Cited by 45 · see citing works
Kjaer, M., Dela, F., Sørensen, F. B., Secher, N., Bangsbo, J., Mohr, T., & Galbo, H. (2001) · American Journal of Physiology. Regulatory Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.281.5.r1492 · Cited by 48 · see citing works
Self-citationSkeletal muscle of trained and untrained paraplegics and tetraplegics
Schantz, P., SJÖBERG, B., WIDEBECK, A. ‐., et al. (1997) · Acta Physiologica Scandinavica · doi:10.1046/j.1365-201x.1997.201371000.x · Cited by 44 · see citing works
“The results focus attention on the considerably lower levels of adrenaline and noradrenaline in tetraplegics at rest and during physical exercise (Bloomfield et al. 1994, Kjaer et al. 1996).”
BackgroundGrowth hormone responses to repeated maximal cycle ergometer exercise at different pedaling rates
Stokes, K., Nevill, M. E., Hall, G. M., & Lakomy, H. K. A. (2002) · Journal of Applied Physiology · doi:10.1152/jappl.2002.92.2.602 · Cited by 41 · see citing works
“(20) suggested that humoral feedback mechanisms and autonomic nervous reflexes, without efferent motor center activity, may exert redundant control of pituitary hormonal responses.”
BackgroundHeart rate during exercise with leg vascular occlusion in spinal cord-injured humans
Kjær, M., Pott, F. C., Mohr, T. T., et al. (1999) · Journal of Applied Physiology · doi:10.1152/jappl.1999.86.3.806 · Cited by 41 · see citing works
Self-citationKouda, K., Furusawa, K., Sugiyama, H., Sumiya, T., Ito, T., Tajima, F., & Shimizu, K. (2011) · European Journal of Applied Physiology · doi:10.1007/s00421-011-2004-2 · Cited by 40 · see citing works
“Patients with high CSCI have impaired sympathetic nervous system and thus reduced catecholamine response to exercise, compared with both normal healthy subjects and to some extent subjects with low-thoracic level SCI (Kjaer et al. 1996).”
BackgroundLow-Grade Inflammation and Spinal Cord Injury: Exercise as Therapy?
Alves, E. D. S., Lemos, V. D. A., Ruiz, F. S., Lira, F. S., dos Santos, R. V. T., Rosa, J. P. P., Caperuto, É. C., Tufik, S., & de Mello, M. T. (2013) · Mediators of Inflammation · doi:10.1155/2013/971841 · Cited by 37 · see citing works
“Lower plasma catecholamine responses to arm exercise have been found in individuals with spinal cord injury compared with healthy subjects [39].”
BackgroundHeesterbeek, P. J. C., Berkelmans, H. W. A., Thijssen, D. H. J., van Kuppevelt, H. J. M., Hopman, M. T. E., & Duysens, J. (2005) · Technology and Disability · doi:10.3233/tad-2005-17207 · Cited by 35 · see citing works
Effect of increased blood glucose availability on glucose kinetics during exercise
Howlett, K. F., Angus, D. J., Proietto, J., & Hargreaves, M. (1998) · Journal of Applied Physiology · doi:10.1152/jappl.1998.84.4.1413 · Cited by 34 · see citing works
“In addition, neural feedback from working muscle may play a role in regulating the hormonal and metabolic response to exercise (13).”
BackgroundPlasma IL-6 levels during arm exercise in persons with spinal cord injury
Umemoto, Y., Furusawa, K., Kouda, K., Sasaki, Y., Kanno, N., Kojima, D., & Tajima, F. (2011) · Spinal Cord · doi:10.1038/sc.2011.74 · Cited by 31 · see citing works
Regulation of UCP2 and UCP3 by muscle disuse and physical activity in tetraplegic subjects
Hjeltnes, N., Fernström, M., Zierath, J. R., & Krook, A. (1999) · Diabetologia · doi:10.1007/s001250051233 · Cited by 29 · see citing works
“Interestingly, ESLC exercise training in tetraplegic subjects leads to greater reductions of blood glucose and non-esterified fatty acid concentrations compared with similar levels of exercise in able-bodied subjects [31].”
BackgroundOgawa, T., Nakamura, T., Banno, M., Sasaki, Y., Umemoto, Y., Kouda, K., Kawasaki, T., & Tajima, F. (2014) · Spinal Cord · doi:10.1038/sc.2014.88 · Cited by 27 · see citing works
Poole, R., Harrold, C. P., Burridge, J. H., Byrne, C. D., & Holt, R. I. G. (2004) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2004.00400.x · Cited by 25 · see citing works
Murphy, R. J. L., Hartkopp, A., Gardiner, P. F., Kjær, M., & Béliveau, L. (1999) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/s0003-9993(99)90027-8 · Cited by 23 · see citing works
Self-citationHashizaki, T., Nishimura, Y., 寺村, 健., Umemoto, Y., Shibasaki, M., Leicht, C. A., Kouda, K., & Tajima, F. (2018) · International Journal of Hyperthermia · doi:10.1080/02656736.2018.1511838 · Cited by 22 · see citing works
“All patients with CSCI have sympathetic nervous system impairment and thereby reduced circulating adrenaline concentrations, compared with AB subjects [36].”
Gorgey, A. S., & Lawrence, J. (2015) · PM&R · doi:10.1016/j.pmrj.2015.10.006 · Cited by 22 · see citing works
“This was supported by previous work that demonstrated larger reliance on carbohydrate as exercise intensity increased [7,8].”
BackgroundMethodResultInfluentialStatic exercise—induced increase in blood pressure in individuals with cervical spinal cord injury
Yamamoto, M., Tajima, F., Okawa, H., et al. (1999) · Archives of Physical Medicine and Rehabilitation · doi:10.1016/s0003-9993(99)90139-9 · Cited by 19 · see citing works
Yamanaka, M., Furusawa, K., Sugiyama, H., Goto, M., Kinoshita, T., Kanno, N., Takaoka, K., & Tajima, F. (2010) · Spinal Cord · doi:10.1038/sc.2010.13 · Cited by 17 · see citing works
Waldauf, P., Gojda, J., Urban, T., et al. (2019) · Trials · doi:10.1186/s13063-019-3745-1 · Cited by 13 · see citing works
“bolic resistance and insulin sensitivity in quadriplegic patients [42, 43].”
BackgroundBanno, M., Nakamura, T., Furusawa, K., et al. (2012) · Spinal Cord · doi:10.1038/sc.2011.188 · Cited by 12 · see citing works
Temperature responses to electrically induced cycling in spinal cord injured persons
HOLME, E., Mohr, T. T., r, M. K., & Nielsen, B. (2001) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-200103000-00015 · Cited by 12 · see citing works
Self-citationLow-frequency electrical stimulation with variable intensity preserves torque
Mettler, J. A., Magee, D. M., & Doucet, B. M. M. (2018) · Journal of Electromyography and Kinesiology · doi:10.1016/j.jelekin.2018.06.007 · Cited by 11 · see citing works
Renewed Avenues through Exercise Muscle Contractility and Inflammatory Status
Zanchi, N. E., Almeida, F. N., Lira, F. S., Neto, J. C. R., Nicastro, H., da Luz, C. R., Filho, M. A. D. S., Felitti, V., Vainzof, M., Seelaender, M. C. L., et al. (2012) · The Scientific World JOURNAL · doi:10.1100/2012/584205 · Cited by 10 · see citing works
“The idea that signalling pathways from contracting muscles to other organs that were not only mediated by nervous system was supported by the findings from electrical stimulation of paralyzed muscles in patients with spinal cord injuries [18].”
Temesi, J., Rooney, K. B., Raymond, J., & O'Connor, H. T. (2009) · European Journal of Applied Physiology · doi:10.1007/s00421-009-1185-4 · Cited by 9 · see citing works
Myokines related to leukocyte recruitment are down-regulated in osteosarcoma
Yu, M., Hu, B., Wang, Q., Yang, Q., & Zhou, S. (2018) · International Journal of Medical Sciences · doi:10.7150/ijms.24928 · Cited by 4 · see citing works
“Recent studies showed that a few individual myokine could mediate metabolic changes, regulate tumorigenesis and tumor invasion to other remote organs such as liver and breast [18, 19].”
BackgroundAstorino, T. A., & McMillan, D. W. (2021) · Journal of Spinal Cord Medicine · doi:10.1080/10790268.2021.1952385 · Cited by 1 · see citing works
Hamada, T., Sasaki, H., Hayashi, T., Moritani, T., Kimura, T., & Nakao, K. (2006)
ergometer exercise at different pedaling rates Growth hormone responses to repeated maximal cycle
Nevill, M. E., Hall, G. M., Barnett, M., et al. (2015)
Effects of Exercise on Incretin Hormones
Toghi-Eshghi, S. R. (2018) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r30g3hd88
From brain to muscle and back : novel approaches to harness the benefits of exercise
Kelahmetoglu, Y. (2020) · Figshare
Effectiveness of electrical muscle stimulation in controlling blood glucose level
Trivedi, V., Goyal, D., & Mahajan, R. (2022) · International Journal of Health Sciences · doi:10.53730/ijhs.v6ns3.7120
- Authors
- Kjaer, M., Pollack, S. F., Mohr, T., Weiss, H., Gleim, G. W., Bach, F. W., Nicolaisen, T., Galbo, H., & Ragnarsson, K. T.
- Affiliations
- Department of Rehabilitation Medicine, Mount Sinai Medical Center, New York, New York 10029, USA.
- Mount Sinai Health System (US)
- Venue
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology
- Publisher
- American Physiological Society
- Published
- 1996-07-01
- Volume
- 271
- Issue
- 1
- Pages
- R191-R199
- ISSN
- 0363-6119 (ISSN-L)
- 1522-1490
- OpenAlex
- W2365720431
- Cited by
- 47
- References
- 0
- Citations by year
- 2022: 1 · 2021: 2 · 2020: 2 · 2019: 1 · 2018: 6 · 2015: 3 · 2014: 1 · 2013: 2 · 2012: 2
- FWCI
- 2.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Regulatory, Integrative and Comparative Physiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Spinal Cord Injury Research
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Management and Research
- Keywords
- tetraplegia, spinal cord injury, functional electrical stimulation, glucose turnover, hepatic glucose production, substrate mobilization, growth hormone, insulin, epinephrine, norepinephrine, catecholamines, beta-endorphin, ACTH, renin, free fatty acids, beta-hydroxybutyrate, heart rate, neuroendocrine regulation, long-term immobilization
- MeSH terms
- Adult, Bicycling, Electric Stimulation, Glucose, Glycerol, Heart Rate, Hematocrit, Hormones, Humans, Insulin, Male, Middle Aged, Norepinephrine, Quadriplegia, Renin, Growth Hormone, Exercise
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
