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European Journal of Applied Physiology

, Volume 116, Issue 10, pp 1889–1897 | Cite as

Low-volume high-intensity swim training is superior to high-volume low-intensity training in relation to insulin sensitivity and glucose control in inactive middle-aged women

  • Luke J. Connolly
  • Nikolai B. Nordsborg
  • Michael Nyberg
  • Pál Weihe
  • Peter Krustrup
  • Magni Mohr
Original Article

Abstract

Purpose

We tested the hypothesis that low-volume high-intensity swimming has a larger impact on insulin sensitivity and glucose control than high-volume low-intensity swimming in inactive premenopausal women with mild hypertension.

Methods

Sixty-two untrained premenopausal women were randomised to an inactive control (n = 20; CON), a high-intensity low-volume (n = 21; HIT) or a low-intensity high-volume (n = 21; LIT) training group. During the 15-week intervention period, HIT performed 3 weekly 6–10 × 30-s all-out swimming intervals (average heart rate (HR) = 86 ± 3 % HRmax) interspersed by 2-min recovery periods and LIT swam continuously for 1 h at low intensity (average HR = 73 ± 3 % HRmax). Fasting blood samples were taken and an oral glucose tolerance test (OGTT) was conducted pre- and post-intervention.

Results

After HIT, resting plasma [insulin] was lowered (17 ± 34 %; P < 0.05) but remained similar after LIT and CON. Following HIT, 60-min OGTT plasma [insulin] and [glucose] was lowered (24 ± 30 % and 10 ± 16 %; P < 0.05) but remained similar after LIT and CON. Total area under the curve for plasma [glucose] was lower (P < 0.05) after HIT than LIT (660 ± 141 vs. 860 ± 325 mmol min L−1). Insulin sensitivity (HOMA-IR) had increased (P < 0.05) by 22 ± 34 % after HIT, with no significant change after LIT or CON, respectively. Plasma soluble intracellular cell adhesion molecule 1 was lowered (P < 0.05) by 4 ± 8 and 3 ± 9 % after HIT and CON, respectively, while plasma soluble vascular cell adhesion molecule 1 had decreased (P < 0.05) by 8 ± 23 % after HIT only.

Conclusions

These findings suggest that low-volume high-intensity intermittent swimming is an effective and time-efficient training strategy for improving insulin sensitivity, glucose control and biomarkers of vascular function in inactive, middle-aged mildly hypertensive women.

Keywords

Blood glucose Type 2 diabetes Body composition Upper body exercise Metabolic health 

Abbreviations

ANOVA

Analysis of variance

CON

Control

HIT

High-intensity training

HOMA-IR

Homeostatic model assessment of insulin resistance

HR

Heart rate

OGTT

Oral glucose tolerance test

LIT

Low-intensity training

SEM

Standard error of the mean

sICAM-1

Soluble intracellular cell adhesion molecule 1

sVCAM-1

Soluble vascular cell adhesion molecule 1

T2DM

Type 2 diabetes mellitus

tAUC

Total area under the curve

Notes

Acknowledgments

The authors would like to express their appreciation for the outstanding efforts and positive attitude of the participants. In addition, they are extremely grateful for the professional assistance given by swimming coaches Remi Lamhauge, Brynhild Klein, Pauli Øssursson Mohr, Heini Rasmussen, Oluffa á Høvdanum, and the late Jákup Mohr, and for the technical support provided by Ivy Hansen, Gunnrið Jóannesarson, Guðrið Andórsdóttir, Hergerð Joensen, Ann Østerø, Ebba Andreassen, Maud av Fløtum, Liljan av Fløtum Petersen, Marjun Thomsen, Annika Lindenskov, Jann Mortensen, David Childs, Sarah R. Jackman and Jens Jung Nielsen. The study was supported by a Grant from the Faroese Research Council, as well as by The Faroese Confederation of Sports and Olympic Committee (Ítróttarsamband Føroya), and the Danish Sports Confederation (Danmarks Idrætsforbund). In addition, financial support was obtained from Eik Bank.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interests

Ethical approval

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

References

  1. Adams OP (2013) The impact of brief high-intensity exercise on blood glucose levels. Diabetes Metab Syndr Obes 6:113–122. doi: 10.2147/DMSO.S29222 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Al Tunaiji H, Davis JC, Mackey DC, Khan KM (2014) Population attributable fraction of type 2 diabetes due to physical inactivity in adults: a systematic review. BMC Public Health 14:469. doi: 10.1186/1471-2458-14-469 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Appelman Y, van Rijn BB, Ten Haaf ME, Boersma E, Peters SA (2015) Sex differences in cardiovascular risk factors and disease prevention. Atherosclerosis 241:211–218. doi: 10.1016/j.atherosclerosis.2015.01.027 CrossRefPubMedGoogle Scholar
  4. Arad AD, DiMenna FJ, Thomas N, Tamis-Holland J, Weil R, Geliebter A, Albu JB (2015) High-intensity interval training without weight loss improves exercise but not basal or insulin-induced metabolism in overweight/obese African American women. J Appl Physiol 119:352–362. doi: 10.1152/japplphysiol.00306.2015 CrossRefPubMedGoogle Scholar
  5. Burgomaster KA, Cermak NM, Phillips SM, Benton CR, Bonen A, Gibala MJ (2007) Divergent response of metabolite transport proteins in human skeletal muscle after sprint interval training and detraining. Am J Physiol Regul Integr Comp Physiol 292:R1970–R1976. doi: 10.1152/ajpregu.00503.2006 CrossRefPubMedGoogle Scholar
  6. Chedraui P, Perez-Lopez FR (2013) Nutrition and health during mid-life: searching for solutions and meeting challenges for the aging population. Climacteric 16(Suppl 1):85–95. doi: 10.3109/13697137.2013.802884 CrossRefPubMedGoogle Scholar
  7. Chen NG, Azhar S, Abbasi F, Carantoni M, Reaven GM (2000) The relationship between plasma glucose and insulin responses to oral glucose, LDL oxidation, and soluble intercellular adhesion molecule-1 in healthy volunteers. Atherosclerosis 152:203–208. doi: 10.1016/S0021-9150(99)00460-8 CrossRefPubMedGoogle Scholar
  8. Chen HH, Chen YL, Huang CY, Lee SD, Chen SC, Kuo CH (2010) Effects of one-year swimming training on blood pressure and insulin sensitivity in mild hypertensive young patients. Chin J Physiol 53:185–189. doi: 10.4077/cjp.2010.amk042 CrossRefPubMedGoogle Scholar
  9. Ciolac EG, Bocchi EA, Bortolotto LA, Carvalho VO, Greve JM, Guimaraes GV (2010) Effects of high-intensity aerobic interval training vs. moderate exercise on hemodynamic, metabolic and neuro-humoral abnormalities of young normotensive women at high familial risk for hypertension. Hypertens Res 33:836–843. doi: 10.1038/hr.2010.72 CrossRefPubMedGoogle Scholar
  10. Cox KL, Burke V, Beilin LJ, Puddey IB (2010) A comparison of the effects of swimming and walking on body weight, fat distribution, lipids, glucose, and insulin in older women-the Sedentary Women Exercise Adherence Trial 2. Metabolism 59:1562–1573. doi: 10.1016/j.metabol.2010.02.001 CrossRefPubMedGoogle Scholar
  11. Daugaard JR, Richter EA (2001) Relationship between muscle fibre composition, glucose transporter protein 4 and exercise training: possible consequences in non-insulin-dependent diabetes mellitus. Acta Physiol Scand 171:267–276. doi: 10.1046/j.1365-201x.2001.00829.x CrossRefPubMedGoogle Scholar
  12. Durrer C et al (2015) Differential impact of acute high-intensity exercise on circulating endothelial microparticles and insulin resistance between overweight/obese males and females. PLoS ONE 10:e0115860. doi: 10.1371/journal.pone.0115860 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ferrannini E, Camastra S, Coppack SW, Fliser D, Golay A, Mitrakou A (1997) Insulin action and non-esterified fatty acids. The European Group for the Study of Insulin Resistance (EGIR). Proc Nutr Soc 56:753–761CrossRefPubMedGoogle Scholar
  14. Fujimoto E, Machida S, Higuchi M, Tabata I (2010) Effects of nonexhaustive bouts of high-intensity intermittent swimming training on GLUT-4 expression in rat skeletal muscle. J Physiol Sci 60:95–101. doi: 10.1007/s12576-009-0072-4 CrossRefPubMedGoogle Scholar
  15. Gillen JB, Percival ME, Ludzki A, Tarnopolsky MA, Gibala MJ (2013) Interval training in the fed or fasted state improves body composition and muscle oxidative capacity in overweight women. Obesity 21:2249–2255. doi: 10.1002/oby.20379 CrossRefPubMedGoogle Scholar
  16. Glowinska B, Urban M, Peczynska J, Florys B (2005) Soluble adhesion molecules (sICAM-1, sVCAM-1) and selectins (sE selectin, sP selectin, sL selectin) levels in children and adolescents with obesity, hypertension, and diabetes. Metabolism 54:1020–1026. doi: 10.1016/j.metabol.2005.03.004 CrossRefPubMedGoogle Scholar
  17. Goodpaster BH, Katsiaras A, Kelley DE (2003) Enhanced fat oxidation through physical activity is associated with improvements in insulin sensitivity in obesity. Diabetes 52:2191–2197. doi: 10.2337/diabetes.52.9.2191 CrossRefPubMedGoogle Scholar
  18. Holloszy JO, Booth FW (1976) Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol 38:273–291. doi: 10.1146/annurev.ph.38.030176.001421 CrossRefPubMedGoogle Scholar
  19. Iaia FM, Hellsten Y, Nielsen JJ, Fernstrom M, Sahlin K, Bangsbo J (2009) Four weeks of speed endurance training reduces energy expenditure during exercise and maintains muscle oxidative capacity despite a reduction in training volume. J Appl Physiol 106:73–80. doi: 10.1152/japplphysiol.90676.2008 CrossRefPubMedGoogle Scholar
  20. Keating SE et al (2015) Effect of aerobic exercise training dose on liver fat and visceral adiposity. J Hepatol 63:174–182. doi: 10.1016/j.jhep.2015.02.022 CrossRefPubMedGoogle Scholar
  21. Kim JA, Montagnani M, Koh KK, Quon MJ (2006) Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113:1888–1904. doi: 10.1161/CIRCULATIONAHA.105.563213 CrossRefPubMedGoogle Scholar
  22. Kohl HW, Craig CL, Lambert EV, Inoue S, Alkandari JR, Leetongin G, Kahlmeier S (2012) The pandemic of physical inactivity: global action for public health. Lancet 380:294–305. doi: 10.1016/s0140-6736(12)60898-8 CrossRefPubMedGoogle Scholar
  23. Lazar JM, Khanna N, Chesler R, Salciccioli L (2013) Swimming and the heart. Int J Cardiol 168:19–26. doi: 10.1016/j.ijcard.2013.03.063 CrossRefPubMedGoogle Scholar
  24. Little JP, Francois ME (2014) High-intensity interval training for improving postprandial hyperglycemia. Res Q Exerc Sport 85:451–456. doi: 10.1080/02701367.2014.963474 CrossRefPubMedGoogle Scholar
  25. Little JP et al (2011) Low-volume high-intensity interval training reduces hyperglycemia and increases muscle mitochondrial capacity in patients with type 2 diabetes. J Appl Physiol 111:1554–1560. doi: 10.1152/japplphysiol.00921.2011 CrossRefPubMedGoogle Scholar
  26. Marsh SA, Coombes JS (2005) Exercise and the endothelial cell. Int J Cardiol 99:165–169. doi: 10.1016/j.ijcard.2004.02.005 CrossRefPubMedGoogle Scholar
  27. Mohr M, Krustrup P, Nielsen JJ, Nybo L, Rasmussen MK, Juel C, Bangsbo J (2007) Effect of two different intense training regimens on skeletal muscle ion transport proteins and fatigue development. Am J Physiol Regul Integr Comp Physiol 292:R1594–R1602. doi: 10.1152/ajpregu.00251.2006 CrossRefPubMedGoogle Scholar
  28. Mohr M, Lindenskov A, Holm PM, Nielsen HP, Mortensen J, Weihe P, Krustrup P (2014a) Football training improves cardiovascular health profile in sedentary, premenopausal hypertensive women. Scand J Med Sci Sports 24(Suppl 1):36–42. doi: 10.1111/sms.12278 CrossRefPubMedGoogle Scholar
  29. Mohr M et al (2014b) High-intensity intermittent swimming improves cardiovascular health status for women with mild hypertension. BioMed research international 2014:728289. doi: 10.1155/2014/728289 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Motta VF, Aguila MB, Mandarim-De-Lacerda CA (2015) High-intensity interval training (swimming) significantly improves the adverse metabolism and comorbidities in diet-induced obese mice. The Journal of Sports Medicine and Physical Fitness 54:203–209Google Scholar
  31. Nordsborg NB, Connolly L, Weihe P, Iuliano E, Krustrup P, Saltin B, Mohr M (2015) Oxidative capacity and glycogen content increase more in arm than leg muscle in sedentary women after intense training. J Appl Physiol 119:116–123. doi: 10.1152/japplphysiol.00101.2015 CrossRefPubMedGoogle Scholar
  32. Nualnim N, Parkhurst K, Dhindsa M, Tarumi T, Vavrek J, Tanaka H (2012) Effects of swimming training on blood pressure and vascular function in adults >50 years of age. Am J Cardiol 109:1005–1010. doi: 10.1016/j.amjcard.2011.11.029 CrossRefPubMedGoogle Scholar
  33. Nyberg M, Seidelin K, Andersen TR, Overby NN, Hellsten Y, Bangsbo J (2014) Biomarkers of vascular function in premenopausal and recent postmenopausal women of similar age: effect of exercise training. Am J Physiol Regul Integr Comp Physiol 306:R510–R517. doi: 10.1152/ajpregu.00539.2013 CrossRefPubMedGoogle Scholar
  34. Padilla J, Harris RA, Rink LD, Wallace JP (2008) Characterization of the brachial artery shear stress following walking exercise. Vasc Med 13:105–111. doi: 10.1177/1358863x07086671 CrossRefPubMedGoogle Scholar
  35. Rizzoli R et al (2014) The role of dietary protein and vitamin D in maintaining musculoskeletal health in postmenopausal women: a consensus statement from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO). Maturitas 79:122–132. doi: 10.1016/j.maturitas.2014.07.005 CrossRefPubMedGoogle Scholar
  36. Sabatier MJ, Schwark EH, Lewis R, Sloan G, Cannon J, McCully K (2008) Femoral artery remodeling after aerobic exercise training without weight loss in women. Dyn Med. doi: 10.1186/1476-5918-7-13 PubMedPubMedCentralGoogle Scholar
  37. Shaban N, Kenno KA, Milne KJ (2014) The effects of a 2 week modified high intensity interval training program on the homeostatic model of insulin resistance (HOMA-IR) in adults with type 2 diabetes. J Sports Med Phys Fitness 54:203–209PubMedGoogle Scholar
  38. Shufelt C, Braunstein GD, Pepine CJ, Bairey Merz CN (2015) Recognizing Sex Similarities in Cardiovascular Disease Research. J Am Coll Cardiol 65:2152–2153. doi: 10.1016/j.jacc.2015.02.066 CrossRefPubMedGoogle Scholar
  39. Song A, Wang C, Ren L, Zhao J (2014) Swimming improves high-fat induced insulin resistance by regulating lipid and energy metabolism and the insulin pathway in rats. Int J Mol Med 33:1671–1679. doi: 10.3892/ijmm.2014.1738 PubMedGoogle Scholar
  40. Sundstedt M, Jonason T, Ahren T, Damm S, Wesslen L, Henriksen E (2003) Left ventricular volume changes during supine exercise in young endurance athletes. Acta Physiol Scand 177:467–472. doi: 10.1046/j.1365-201X.2003.01098.x CrossRefPubMedGoogle Scholar
  41. Talanian JL, Galloway SD, Heigenhauser GJ, Bonen A, Spriet LL (2007) Two weeks of high-intensity aerobic interval training increases the capacity for fat oxidation during exercise in women. J Appl Physiol 102:1439–1447. doi: 10.1152/japplphysiol.01098.2006 CrossRefPubMedGoogle Scholar
  42. Terada S, Yokozeki T, Kawanaka K, Ogawa K, Higuchi M, Ezaki O, Tabata I (2001) Effects of high-intensity swimming training on GLUT-4 and glucose transport activity in rat skeletal muscle. J Appl Physiol 90:2019–2024PubMedGoogle Scholar
  43. Trapp EG, Chisholm DJ, Freund J, Boutcher SH (2008) The effects of high-intensity intermittent exercise training on fat loss and fasting insulin levels of young women. Int J Obes (Lond) 32:684–691. doi: 10.1038/sj.ijo.0803781 CrossRefGoogle Scholar
  44. Vollestad NK, Blom PC (1985) Effect of varying exercise intensity on glycogen depletion in human muscle fibres. Acta Physiol Scand 125:395–405. doi: 10.1111/j.1748-1716.1985.tb07735.x CrossRefPubMedGoogle Scholar
  45. Weyer C, Yudkin JS, Stehouwer CD, Schalkwijk CG, Pratley RE, Tataranni PA (2002) Humoral markers of inflammation and endothelial dysfunction in relation to adiposity and in vivo insulin action in Pima Indians. Atherosclerosis 161:233–242CrossRefPubMedGoogle Scholar
  46. Wisloff U, Ellingsen O, Kemi OJ (2009) High-intensity interval training to maximize cardiac benefits of exercise training? Exerc Sport Sci Rev 37:139–146. doi: 10.1097/JES.0b013e3181aa65fc CrossRefPubMedGoogle Scholar
  47. World Health Organization (2016) Physical Inactivity: A Global Public Health Problem. http://www.who.int/dietphysicalactivity/factsheet_inactivity/en/. Accessed 11/03/16 2016
  48. Yokoyama H et al (2003) Quantitative insulin sensitivity check index and the reciprocal index of homeostasis model assessment in normal range weight and moderately obese type 2 diabetic patients. Diabetes Care 26:2426–2432CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Luke J. Connolly
    • 1
  • Nikolai B. Nordsborg
    • 2
  • Michael Nyberg
    • 2
  • Pál Weihe
    • 3
    • 4
  • Peter Krustrup
    • 1
    • 2
  • Magni Mohr
    • 4
    • 5
  1. 1.Sport and Health SciencesCollege of Life and Environmental Sciences, University of ExeterExeterUK
  2. 2.Department of Nutrition, Exercise and Sports, Section of Integrative PhysiologyUniversity of CopenhagenCopenhagenDenmark
  3. 3.Department of Occupational Medicine and Public HealthThe Faroese Hospital SystemTórshavnFaroe Islands
  4. 4.Faculty of Natural and Health SciencesUniversity of the Faroe IslandsTórshavnFaroe Islands
  5. 5.Department of Food and Nutrition, and Sport Sciences, Center for Health and Human PerformanceUniversity of GothenburgGothenburgSweden

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