Skip to main content
Log in

A Combined Analysis of Peak and Submaximal Exercise Parameters in Delineating Underlying Mechanisms of Sex Differences in Healthy Adolescents

  • Published:
Pediatric Cardiology Aims and scope Submit manuscript

Abstract

Peak exercise parameters are considered the gold standard to quantify cardiac reserve in cardiopulmonary exercise testing (CPET). We studied whether submaximal parameters would add additional values in analyzing sex differences in CPET. We reviewed CPET of age-matched healthy male and female adolescents by cycle ergometer. Besides peak parameters, submaximal CPET parameters, including ventilatory anaerobic threshold (VAT), oxygen uptake efficiency slope (OUES), and submaximal slopes of Δoxygen consumption (ΔVO2)/Δwork rate (ΔWR), Δheart rate (ΔHR)/ΔWR, ΔVO2/ΔHR, and Δminute ventilation (ΔVE)/ΔCO2 production (ΔVCO2), were obtained. We studied 35 male and 40 female healthy adolescents. Peak VO2 (pVO2), peak oxygen pulse (pOP), and VAT were significantly lower in females than males (1.9 ± 0.4 vs. 2.5 ± 0.6 L/min; 10 ± 2.0 vs. 13.2 ± 3.5 ml/beat; 1.23 ± 0.3 vs. 1.52 ± 0.5 L/min, respectively, all p < 0.005). Females showed significantly lower pVO2, VAT, and OUES with the same body weight than males, implying higher skeletal muscle mass in males. When simultaneously examining ΔHR/ΔWR and pOP, females showed higher dependency on increases in HR than in stroke volume. Females demonstrated significantly lower pOP with the same levels of ΔVO2/ΔHR, suggesting more limited exercise persistence than males under an anaerobic condition at peak exercise. Oxygen uptake efficiency in relation to peak VE was significantly higher in males. There was no sex difference in either ΔVO2/ΔWR or ΔVE/ΔVCO2. Combinational assessment of peak and submaximal CPET parameters delineates the multiple mechanisms that contribute to the sex differences in exercise performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

BMI:

Body mass index

CPET:

Cardiopulmonary exercise testing

OP:

Oxygen pulse

OUES:

Oxygen uptake efficiency slope

RAMP:

Raise, activate, mobilize, potentiate/performance

VO2:

Oxygen consumption

VCO2:

Carbon dioxide production

VAT:

Ventilatory anaerobic threshold

VE:

Minute ventilation

WR:

Work rate

References

  1. Albouaini K, Egred M, Alahmar A, Wright DJ (2007) Cardiopulmonary exercise testing and its application. Postgrad Med J 83:675–682

    Article  Google Scholar 

  2. Mezzani A (2017) Cardiopulmonary exercise testing: basics of methodology and measurements. Ann Am Thorac Soc 14:S3–S11

    Article  Google Scholar 

  3. Takken T, Blank AC, Hulzebos EH, Van Brussel M, Groen WG, Helders PJ (2009) Cardiopulmonary exercise testing in congenital heart disease: equipment and test protocols. Neth Heart J 17:339–344

    Article  CAS  Google Scholar 

  4. Cooper DM, Leu S-Y, Galassetti P, Radom-Aizik S (2014) Dynamic interactions of gas exchange, body mass, and progressive exercise in children. Med Sci Sports Exerc 46:877–886

    Article  CAS  Google Scholar 

  5. Cooper DM, Leu SY, Taylor-Lucas C, Lu K, Galassetti P, Radom-Aizik S (2016) Cardiopulmonary exercise testing in children and adolescents with high body mass index. Pediatr Exerc Sci 28:98–108

    Article  Google Scholar 

  6. Herdy AH, Ritt LE, Stein R, Araujo CG, Milani M, Meneghelo RS, Ferraz AS, Hossri C, Almeida AE, Fernandes-Silva MM, Serra SM (2016) Cardiopulmonary exercise test: background, applicability and interpretation. Arq Bras Cardiol 107:467–481

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Ten Harkel A, Takken T (2011) Normal values for cardiopulmonary exercise testing in children. Eur J Cardiovasc Prev Rehabil 18:676–677

    Article  Google Scholar 

  8. Drinkwater BL (1973) Physiological responses of women to exercise. Exerc Sport Sci Rev 1:125–153

    Article  CAS  Google Scholar 

  9. Rowland T, Goff D, Martel L, Ferrone L (2000) Influence of cardiac functional capacity on gender differences in maximal oxygen uptake in children. Chest 117:629–635

    Article  CAS  Google Scholar 

  10. Ansdell P, Thomas K, Hicks KM, Hunter SK, Howatson G, Goodall S (2020) Physiological sex differences affect the integrative response to exercise: acute and chronic implications. Exp Physiol 105:2007–2021

    Article  Google Scholar 

  11. Wheatley CM, Snyder EM, Johnson BD, Olson TP (2014) Sex differences in cardiovascular function during submaximal exercise in humans. Springerplus 3:445

    Article  Google Scholar 

  12. Armstrong N, Welsman JR (1994) Assessment and interpretation of aerobic fitness in children and adolescents. Exerc Sport Sci Rev 22:435–476

    Article  CAS  Google Scholar 

  13. Baba R, Masami N, Masahiko G, Yoshiko N, Mitsuhiro Y, Nobuo T, Kenji N (1996) Oxygen uptake efficieny slope: a new index of cardiorespiratory functional reserve derived from the relation between oxygen uptake and minute ventilation during incremental exercise. JACC 28:1567–1572

    Article  CAS  Google Scholar 

  14. Armstrong N, Welsman J (2019) Sex-specific longitudinal modeling of youth peak oxygen uptake. Pediatr Exerc Sci 31:204–212

    Article  Google Scholar 

  15. Rowland TW (1990) Developmental aspects of physiological function relating to aerobic exercise in children. Sports Med 10:255–266

    Article  CAS  Google Scholar 

  16. Haizlip KM, Harrison BC, Leinwand LA (2015) Sex-based differences in skeletal muscle kinetics and fiber-type composition. Physiology (Bethesda) 30:30–39

    CAS  PubMed Central  Google Scholar 

  17. Sparling PB (1980) A meta-analysis of studies comparing maximal oxygen uptake in men and women. Res Q Exerc Sport 51:542–552

    Article  CAS  Google Scholar 

  18. Fomin A, Ahlstrand M, Schill HG, Lund LH, Stahlberg M, Manouras A, Gabrielsen A (2012) Sex differences in response to maximal exercise stress test in trained adolescents. BMC Pediatr 12:127

    Article  Google Scholar 

  19. Turley KR, Wilmore JH (1997) Cardiovascular responses to submaximal exercise in 7- to 9-yr-old boys and girls. Med Sci Sports Exerc 29:824–832

    Article  CAS  Google Scholar 

  20. Hossack KF, Bruce RA (1982) Maximal cardiac function in sedentary normal men and women: comparison of age-related changes. J Appl Physiol Respir Environ Exerc Physiol 53:799–804

    CAS  PubMed  Google Scholar 

  21. Wilmore JHC, David L, Kenney WL (2008) Sex Differences in sport and exercise. Physiology of sport and exercise. Human Kinetics Publishers, Champaign, pp 422–446

    Google Scholar 

  22. Bar-Yoseph R, Porszasz J, Radom-Aizik S, Lu KD, Stehli A, Law P, Cooper DM (2019) The effect of test modality on dynamic exercise biomarkers in children, adolescents, and young adults. Physiol Rep 7:e14178

    Article  Google Scholar 

  23. Handelsman DJ, Hirschberg AL, Bermon S (2018) Circulating testosterone as the hormonal basis of sex differences in athletic performance. Endocr Rev 39:803–829

    Article  Google Scholar 

  24. Tarnopolsky LJ, MacDougall JD, Atkinson SA, Tarnopolsky MA, Sutton JR (1990) Gender differences in substrate for endurance exercise. J Appl Physiol (1985) 68:302–308

    Article  CAS  Google Scholar 

  25. Dominelli PB, Molgat-Seon Y, Sheel AW (2019) Sex differences in the pulmonary system influence the integrative response to exercise. Exerc Sport Sci Rev 47:142–150

    Article  Google Scholar 

  26. Sheel AW, Richards JC, Foster GE, Guenette JA (2004) Sex differences in respiratory exercise physiology. Sports Med 34:567–579

    Article  Google Scholar 

  27. McClaran SR, Harms CA, Pegelow DF, Dempsey JA (1998) Smaller lungs in women affect exercise hyperpnea. J Appl Physiol (1985) 84:1872–1881

    Article  CAS  Google Scholar 

  28. Masuki S, Eisenach JH, Schrage WG, Johnson CP, Dietz NM, Wilkins BW, Sandroni P, Low PA, Joyner MJ (2007) Reduced stroke volume during exercise in postural tachycardia syndrome. J Appl Physiol (1985) 103:1128–1135

    Article  Google Scholar 

  29. Claessen G, La Gerche A, Van De Bruaene A, Claeys M, Willems R, Dymarkowski S, Bogaert J, Claus P, Budts W, Heidbuchel H, Gewillig M (2019) Heart rate reserve in fontan patients: chronotropic incompetence or hemodynamic limitation? J Am Heart Assoc 8:e012008

    Article  Google Scholar 

Download references

Acknowledgements

Authors thank Ms. Kimberley Eissmann and Ms. Michelle Stofa for editing this manuscript.

Funding

Authors declare no financial or non-financial interests that are directly or indirectly related to the work submitted for publication.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takeshi Tsuda.

Ethics declarations

Conflict of interest

No conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

246_2022_2832_MOESM1_ESM.pptx

Supplementary file1 (PPTX 58 kb). Supplemental Figure 1 Submaximal slope parameters of CPET in 9-year-old male. ΔVO2/ΔWR (exercise efficiency), ΔHR/ΔWR (heart rate dependency), ΔVO2*/ΔHR (stroke volume indexed by weight), OUES (oxygen uptake efficiency slope), and ΔVE/ΔVCO2 (ventilatory efficiency). An excellent correlation was seen in each graph

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kernizan, D., Glass, A., D’Aloisio, G. et al. A Combined Analysis of Peak and Submaximal Exercise Parameters in Delineating Underlying Mechanisms of Sex Differences in Healthy Adolescents. Pediatr Cardiol 43, 1122–1130 (2022). https://doi.org/10.1007/s00246-022-02832-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00246-022-02832-0

Keywords

Navigation