European Journal of Applied Physiology

, Volume 117, Issue 3, pp 431–440 | Cite as

Sex differences in the response of total PYY and GLP-1 to moderate-intensity continuous and sprint interval cycling exercise

  • Tom J. Hazell
  • Logan K. Townsend
  • Jillian R. Hallworth
  • Jon Doan
  • Jennifer L. Copeland
Original Article

Abstract

Background

Exercise interventions are often less effective at improving body composition for females than males, potentially due to post-exercise hormonal responses that increase energy intake in females. Recently, sprint interval training was shown to effectively reduce body fat in females despite being relatively low during exercise energy expenditure.

Purpose

To determine whether any sex difference in total PYY, GLP-1 or perceived hunger exists following moderate-intensity continuous exercise (MICT) and sprint interval exercise (SIT)

Methods

Twenty-one active participants (11 females) participated in three sessions in a randomized crossover design: (1) MICT, 30-min cycling at 65% VO2max; (2) SIT, 6 × 30 s “all-out” sprints with 4-min recovery periods; (3) control (CTRL; no exercise). Blood samples were collected pre-exercise, immediately and 90 min post-exercise for the measurement of total PYY and GLP-1. Subjective perceptions of hunger were assessed using a visual analogue scale pre-breakfast and before all blood samples.

Results

Concentrations of total PYY and GLP-1 were greater during MICT (P = 0.05) and SIT (P = 0.005) compared to CTRL. Total PYY increased more immediately post-exercise in males than females (P = 0.030). GLP-1 only increased in females following MICT (P = 0.034) and SIT (P = 0.024) compared to CTRL. Perceived hunger was lower immediately post-MICT (P = 0.016) and SIT (P = 0.006) compared to CTRL.

Conclusions

These results suggest that total PYY and GLP-1 respond differently to exercise in males and females over 90 min following various exercise intensities. The observed post-exercise hormonal response would not be expected to create a compensatory increase in energy intake in females.

Keywords

Appetite regulation Anorexigenic Satiety High-intensity interval training Aerobic exercise 

Abbreviations

ANOVA

Analysis of variance

AUC

Area under the curve

BMI

Body mass index

CTRL

Control

CV

Coefficient of variation

EDTA

Ethylenediaminetetraacetic acid

ELISA

Enzyme-linked immunosorbent assay

GLP-1

Glucagon-like peptide-1

HIIT

High-intensity interval training

HR

Heart rate

MICT

Moderate-intensity continuous training

PYY

Peptide tyrosine tyrosine

RER

Respiratory exchange ratio

SD

Standard deviation

SIT

Sprint interval training

VAS

Visual analogue scale

VO2

Oxygen consumption

VO2max

Maximal oxygen uptake

References

  1. Alajmi N, Deighton K, King JA, Reischak-Oliveira A, Wasse LK, Jones J, Batterham RL, Stensel DJ (2016) Appetite and energy intake responses to acute energy deficits in females versus males. Med Sci Sports Exerc 48:412–420. doi:10.1249/MSS.0000000000000793 CrossRefPubMedGoogle Scholar
  2. Asarian L, Geary N (2013) Sex differences in the physiology of eating. Am J Physiol Regul Integr Comp Physiol 305:R1215–R1267. doi:10.1152/ajpregu.00446.2012 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Beaulieu K, Olver TD, Abbott KC, Lemon PWR (2015) Energy intake over 2 days is unaffected by acute sprint interval exercise despite increased appetite and energy expenditure. Appl Physiol Nutr Metab 40:79–86. doi:10.1139/apnm-2014-0229 CrossRefPubMedGoogle Scholar
  4. Broom DR, Stensel DJ, Bishop NC, Burns SF, Miyashita M (2007) Exercise-induced suppression of acylated ghrelin in humans. J Appl Physiol 102:2165–2171. doi:10.1152/japplphysiol.00759.2006 CrossRefPubMedGoogle Scholar
  5. Caudwell P, Gibbons C, Hopkins M, King N, Finlayson G, Blundell J (2013) No sex difference in body fat in response to supervised and measured exercise. Med Sci Sports Exerc 45:351–358. doi:10.1249/MSS.0b013e31826ced79 CrossRefPubMedGoogle Scholar
  6. Clegg DJ, Riedy CA, Smith KAB, Benoit SC, Woods SC (2003) Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 52:682–687. doi:10.2337/diabetes.52.3.682 CrossRefPubMedGoogle Scholar
  7. Clegg DJ, Brown LM, Zigman JM, Kemp CJ, Strader AD, Benoit SC, Woods SC, Mangiaracina M, Geary N (2007) Estradiol-dependent decrease in the orexigenic potency of ghrelin in female rats. Diabetes 56:1051–1058. doi:10.2337/db06-0015 CrossRefPubMedGoogle Scholar
  8. Cummings DE, Overduin J (2007) Gastrointestinal regulation of food intake. J Clin Invest 117:13–23. doi:10.1172/JCI30227 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Davidsen L, Vistisen B, Astrup A (2007) Impact of the menstrual cycle on determinants of energy balance: a putative role in weight loss attempts. Int J Obes 31:1777–1785. doi:10.1038/sj.ijo.0803699 CrossRefGoogle Scholar
  10. Deighton K, Barry R, Connon CE, Stensel DJ (2012) Appetite, gut hormone and energy intake responses to low volume sprint interval and traditional endurance exercise. Euro J Appl Physiol 113:1147–1156. doi:10.1007/s00421-012-2535-1 CrossRefGoogle Scholar
  11. Deighton K, Karra E, Batterham RL, Stensel DJ (2013) Appetite, energy intake, and PYY3–36 responses to energy-matched continuous exercise and submaximal high-intensity exercise. Appl Physiol Nutr Metab 38:947–952. doi:10.1139/apnm-2012-0484 CrossRefPubMedGoogle Scholar
  12. Donnelly JE, Hill JO, Jacobsen DJ, Potteiger J, Sullivan DK, Johnson SL, Heelan K, Hise M, Fennessey PV, Sonko B, Sharp T, Jakicic JM, Blair SN, Tran ZV, Mayo M, Gibson C, Washburn RA (2003) Effects of a 16-month randomized controlled exercise trial on body weight and composition in young, overweight men and women. Arch Int Med 163:1343–1350. doi:10.1001/archinte.163.11.1343 CrossRefGoogle Scholar
  13. Dye L, Blundell JE (1997) Menstrual cycle and appetite control: implications for weight regulation. Human Reprod 12:1142–1151CrossRefGoogle Scholar
  14. Flint A, Raben A, Blundell JE, Astrup A (2000) Reproducibility, power and validity of visual analogue scales in assessment of appetite sensations in single test meal studies. Int J Obes Relat Metab Disord 24:38–48CrossRefPubMedGoogle Scholar
  15. Gillen JB, Gibala MJ (2014) Is high-intensity interval training a time-efficient exercise strategy to improve health and fitness? Appl Physiol Nutr Metab 39:409–412. doi:10.1139/apnm-2013-0187 CrossRefPubMedGoogle Scholar
  16. Gonzalez JT, Veasey RC, Rumbold PLS, Stevenson EJ (2013) Breakfast and exercise contingently affect postprandial metabolism and energy balance in physically active males. Br J Nutr 110:721–732. doi:10.1017/S0007114512005582 CrossRefPubMedGoogle Scholar
  17. Hagobian TA, Sharoff CG, Stephens BR, Wade GN, Silva JE, Chipkin SR, Braun B (2009) Effects of exercise on energy-regulating hormones and appetite in men and women. Am J Physiol Regul Integr Comp Physiol 296:233–242. doi:10.1152/ajpregu.90671.2008 CrossRefGoogle Scholar
  18. Hagobian TA, Yamashiro M, Hinkel-Lipsker J, Streder K, Evero N, Hackney T (2013) Effects of acute exercise on appetite hormones and ad libitum energy intake in men and women. Appl Physiol Nutr Metab 38:66–72. doi:10.1139/apnm-2012-0104 CrossRefPubMedGoogle Scholar
  19. Hallworth JR, Copeland JC, Doan J, Hazell TJ (in press) The effect of exercise intensity on total PYY and GLP-1 in healthy females. J Nutr MetabGoogle Scholar
  20. Hazell TJ, Olver TD, Hamilton CD, Lemon PWR (2012) Two minutes of sprint-interval exercise elicits 24-hr oxygen consumption similar to that of 30 min of continuous endurance exercise. Int J Sport Nutr Exerc Metab 22:276–283CrossRefPubMedGoogle Scholar
  21. Hazell TJ, Hamilton CD, Olver TD, Lemon PWR (2014) Running sprint interval training induces fat loss in women. Appl Physiol Nutr Metab 39:944–950. doi:10.1139/apnm-2013-0503 CrossRefPubMedGoogle Scholar
  22. Hazell TJ, Islam H, Townsend LK, Schmale MS, Copeland JL (2016) Effects of exercise intensity on plasma concentrations of appetite-regulating hormones: potential mechanisms. Appetite 98:80–88. doi:10.1016/j.appet.2015.12.016 CrossRefPubMedGoogle Scholar
  23. Hazell TJ, Islam H, Hallworth JR, Copeland JL, Hazell TJ (2017) Total PYY and GLP-1 responses to submaximal continuous and supramaximal sprint interval cycling in men. Appetite 108:238–244. doi:10.1016/j.appet.2016.10.006 CrossRefPubMedGoogle Scholar
  24. Hickey MS, Houmard JA, Considine RV, Tyndall GL, Midgette JB, Gavigan KE, Weidner ML, McCammon MR, Israel RG, Caro JF (1997) Gender-dependent effects of exercise training on serum leptin levels in humans. Am J Physiol 272:E562–E566PubMedGoogle Scholar
  25. Imbeault P, Saint-Pierre S, Alméras N, Tremblay A (1997) Acute effects of exercise on energy intake and feeding behaviour. Br J Nutr 77:511–521CrossRefPubMedGoogle Scholar
  26. Jackson AS, Pollock ML, Ward A (1980) Generalized equations for predicting body density of women. Med Sci Sports Exerc 2:175–182. doi:10.1249/00005768-198023000-00009 Google Scholar
  27. Jacobsen DJ, Bailey BW, LeCheminant JD, Hill JO, Mayo MS, Donnelly JE (2005) A comparison of three methods of analyzing post-exercise oxygen consumption. Int J Sports Med 26:34–38. doi:10.1055/s-2004-815819 CrossRefPubMedGoogle Scholar
  28. Kawano H, Mineta M, Asaka M, Miyashita M, Numao S, Gando Y, Ando T, Sakamoto S, Higuchi M (2013) Effects of different modes of exercise on appetite and appetite-regulating hormones. Appetite 66:26–33. doi:10.1016/j.appet.2013.01.017 CrossRefPubMedGoogle Scholar
  29. King JA, Miyashita M, Wasse LK, Stensel DJ (2010) Influence of prolonged treadmill running on appetite, energy intake and circulating concentrations of acylated ghrelin. Appetite 54:492–498. doi:10.1016/j.appet.2010.02.002 CrossRefPubMedGoogle Scholar
  30. King JA, Wasse LK, Stensel DJ (2011) The acute effects of swimming on appetite, food intake, and plasma acylated ghrelin. J Obes 2011:1–8. doi:10.1155/2011/351628 CrossRefGoogle Scholar
  31. Laan DJ, Leidy HJ, Lim E, Campbell WW (2010) Effects and reproducibility of aerobic and resistance exercise on appetite and energy intake in young, physically active adults. Appl Physiol Nutr Metab 35:842–847. doi:10.1139/H10-072 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Larson-Meyer DE, Palm S, Bansal A, Austin KJ, Hart AM, Alexander BM (2012) Influence of running and walking on hormonal regulators of appetite in women. J Obes 2012:1–15. doi:10.1155/2012/730409 CrossRefGoogle Scholar
  33. Lean MEJ, Malkova D (2015) Altered gut and adipose tissue hormones in overweight and obese individuals: cause or consequence? Int J Obes. doi:10.1038/ijo.2015.220 Google Scholar
  34. Leidy HJ, Gardner JK, Frye BR, Snook ML, Schuchert MK, Richard EL, Williams NI (2004) Circulating ghrelin is sensitive to changes in body weight during a diet and exercise program in normal-weight young women. J Clin Endocrin Metab 89:2659–2664. doi:10.1210/jc.2003-031471 CrossRefGoogle Scholar
  35. MacPherson REK, Hazell TJ, Olver TD, Paterson DH, Lemon PWR (2011) Run sprint interval training improves aerobic performance but not maximal cardiac output. Med Sci Sports Exerc 43:115–122. doi:10.1249/MSS.0b013e3181e5eacd CrossRefPubMedGoogle Scholar
  36. Martins C, Morgan LM, Bloom SR, Robertson MD (2007) Effects of exercise on gut peptides, energy intake and appetite. J Endocrin 193:251–258. doi:10.1677/JOE-06-0030 CrossRefGoogle Scholar
  37. Martins C, Stensvold D, Finlayson G, Holst J, Wisloff U, Nulseng B, Morgan L, King NA (2015) Effect of moderate- and high-intensity acute exercise on appetite in obese individuals. Med Sci Sports Exerc 47:40–48. doi:10.1249/MSS.0000000000000372 CrossRefPubMedGoogle Scholar
  38. Midgley AW, McNaughton LR, Jones AM (2007) Training to enhance the physiological determinants of long-distance running performance. Sports Med 37:857–880. doi:10.2165/00007256-200737100-00003 CrossRefPubMedGoogle Scholar
  39. Murphy KG, Bloom SR (2006) Gut hormones and the regulation of energy homeostasis. Nature 444:854–859. doi:10.1038/nature05484 CrossRefPubMedGoogle Scholar
  40. Neary NM, Small CJ, Druce MR, Park AJ, Ellis SM, Semjonous NM, Dakin CL, Filipsson K, Wang F, Kent AS, Frost GS, Ghatei MA, Bloom SR (2005) Peptide YY3-36 and glucagon-like peptide-17-36 inhibit food intake additively. Endocrinology 146:5120–5127. doi:10.1210/en.2005-0237 CrossRefPubMedGoogle Scholar
  41. Pomerleau M, Imbeault P, Parker T, Doucet E (2004) Effects of exercise intensity on food intake and appetite in women. Am J Clin Nutr 80:1230–1236PubMedGoogle Scholar
  42. Potteiger JA, Jacobsen DJ, Donnelly JE, Hill JO (2003) Glucose and insulin responses following 16 months of exercise training in overweight adults: the midwest exercise trial. Metabolism 52:1175–1181. doi:10.1016/S0026-0495(03)00146-X CrossRefPubMedGoogle Scholar
  43. Ravussin E, Tschöp M, Morales S, Bouchard C, Heiman ML (2001) Plasma ghrelin concentration and energy balance: overfeeding and negative energy balance studies in twins. J Clin Endocrin Metab 86:4547–4551. doi:10.1210/jcem.86.9.8003 CrossRefGoogle Scholar
  44. Sartorio A, Maffiuletti NA, Agosti F, Lafortuna CL (2005) Gender-related changes in body composition, muscle strength and power output after a short-term multidisciplinary weight loss intervention in morbid obesity. J Endocrin Invest 28:494–501. doi:10.1007/BF03347236 CrossRefGoogle Scholar
  45. Schubert MM, Desbrow B, Sabapathy S, Leveritt M (2013a) Acute exercise and subsequent energy intake. A meta-analysis. Appetite 63:92–104. doi:10.1016/j.appet.2012.12.010 CrossRefPubMedGoogle Scholar
  46. Schubert MM, Sabapathy S, Leveritt M, Desbrow B (2013b) Acute exercise and hormones related to appetite regulation: A meta-analysis. Sports Med 44:387–403. doi:10.1007/s40279-013-0120-3 CrossRefGoogle Scholar
  47. Shaw KA, Gennat HC, O’Rourke P, Del Mar C (2006) Exercise for overweight or obesity. Cochrane Database Sys Rev. doi:10.1002/14651858.CD003817.pub3 Google Scholar
  48. Shorten AL, Wallman KE, Guelfi KJ (2009) Acute effect of environmental temperature during exercise on subsequent energy intake in active men. Am J Clin Nutr 90:1215–1221. doi:10.3945/ajcn.2009.28162 CrossRefPubMedGoogle Scholar
  49. Sim AY, Wallman KE, Fairchild TJ, Guelfi KJ (2014) High-intensity intermittent exercise attenuates ad-libitum energy intake. Int J Obes 38:417–422. doi:10.1038/ijo.2013.102 CrossRefGoogle Scholar
  50. Stubbs RJ, Sepp A, Hughes DA, Johnstone AM, Horgan GW, King N, Blundell JE (2002a) The effect of graded levels of exercise on energy intake and balance in free-living men, consuming their normal diet. Euro J Clin Nutr 56:129–140. doi:10.1038/sj.ejcn.1601295 CrossRefGoogle Scholar
  51. Stubbs RJ, Sepp A, Hughes DA, Johnstone AM, King N, Horgan GW, Blundell JE (2002b) The effect of graded levels of exercise on energy intake and balance in free-living women. Int J Obes 866–869Google Scholar
  52. Townsend LK, Couture KM, Hazell TJ (2014) Mode of exercise and sex are not important for oxygen consumption during and in recovery from sprint interval training. Appl Physiol Nutr Metab 39:1388–1394. doi:10.1139/apnm-2014-0145 CrossRefPubMedGoogle Scholar
  53. Ueda SY, Yoshikawa T, Katsura Y, Usui T, Nakao H, Fujimoto S (2009) Changes in gut hormone levels and negative energy balance during aerobic exercise in obese young males. J Endocrin 201:151–159. doi:10.1677/JOE-08-0500 CrossRefGoogle Scholar
  54. Wade GN, Jones JE (2004) Neuroendocrinology of nutritional infertility. Am J Physiol Regul Integr Comp Physiol 287:R1277–R1296. doi:10.1152/ajpregu.00475.2004 CrossRefPubMedGoogle Scholar
  55. Wasse LK, Sunderland C, King JA, Miyashita M, Stensel DJ (2013) The influence of vigorous running and cycling exercise on hunger perceptions and plasma acylated ghrelin concentrations in lean young men. Appl Physiol Nutr Metab 38:1–6. doi:10.1139/apnm-2012-0154 CrossRefPubMedGoogle Scholar
  56. Westerterp KR, Meijer GA, Janssen EM, Saris WH, Hoor Ten F (1992) Long-term effect of physical activity on energy balance and body composition. Br J Nutr 68:21–30CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Kinesiology and Physical EducationWilfrid Laurier UniversityWaterlooCanada
  2. 2.Department of Kinesiology and Physical EducationUniversity of LethbridgeLethbridgeCanada

Personalised recommendations