Skip to main content

Advertisement

SpringerLink
Log in

Low total haemoglobin mass, blood volume and aerobic capacity in men with type 1 diabetes

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Blood O2 carrying capacity affects aerobic capacity (VO2max). Patients with type 1 diabetes have a risk for anaemia along with renal impairment, and they often have low VO2max. We investigated whether total haemoglobin mass (tHb-mass) and blood volume (BV) differ in men with type 1 diabetes (T1D, n = 12) presently without complications and in healthy men (CON, n = 23) (age-, anthropometry-, physical activity-matched), to seek an explanation for low VO2max. We determined tHb-mass, BV, haemoglobin concentration ([Hb]), and VO2max in T1D and CON. With similar (mean ± SD) [Hb] (144 vs. 145 g l−1), T1D had lower tHb-mass (10.1 ± 1.4 vs. 11.0 ± 1.1 g kg−1, P < 0.05), BV (76.8 ± 9.5 vs. 83.5 ± 8.3 ml kg−1, P < 0.05) and VO2max (35.4 ± 4.8 vs. 44.9 ± 7.5 ml kg−1 min−1, P < 0.001) than CON. VO2max correlated with tHb-mass and BV both in T1D (r = 0.71, P < 0.01 and 0.67, P < 0.05, respectively) and CON (r = 0.54, P < 0.01 and 0.66, P < 0.001, respectively), but not with [Hb]. Linear regression slopes were shallower in T1D than CON both between VO2max and tHb-mass (2.4 and 3.6 ml kg−1 min−1 vs. g kg−1, respectively) and VO2max and BV (0.3 and 0.6 ml kg−1 min−1 vs. g kg−1, respectively), indicating that T1D were unable to reach similar VO2max than CON at a given tHb-mass and BV. In conclusion, low tHb-mass and BV partly explained low VO2max in T1D and may provide early and more sensitive markers of blood O2 carrying capacity than [Hb] alone.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

BM:

Body mass

BMI:

Body mass index

BSA:

Body surface area

BV:

Blood volume

CON:

Healthy controls

ECG:

Electrocardiography

EDV:

End-diastolic volume

EPO:

Erythropoietin

EV:

Erythrocyte volume

EXT:

Step incremental exercise protocol

FFM:

Fat free mass

FFMI:

Fat free mass index

[Hb]:

Haemoglobin concentration

HbA1c:

Glycated haemoglobin

Hct:

Haematocrit

HR:

Heart rate

HRmax :

Heart rate at maximal exercise

LTPA:

Leisure-time physical activity

LV:

Left ventricular

PV:

Plasma volume

RAS:

Renin-angiotensin system

RPE:

Borg rating of perceived exertion

SpO2 :

Oxygen saturation of arterial blood

SV:

Stroke volume

T1D:

Patients with type 1 diabetes

tHb-mass:

Total haemoglobin mass

%TE:

Typical error

V E :

Ventilation

V Emax :

Ventilation at maximal exercise

VO2max :

Aerobic capacity

References

  • American Diabetes Association (2004) Position statement. Physical activity/exercise and diabetes. Diabetes Care 27(S1):S58–62

    Google Scholar 

  • Astor BC, Muntner P, Levin A, Eustace JA, Coresh J (2002) Association of kidney function with anemia: the Third National Health and Nutrition Examination Survey (1988–1994). Arch Intern Med 162(12):1401–1408

    Article  PubMed  Google Scholar 

  • Balakumar P, Jagadeesh G (2010) Cardiovascular and renal pathologic implications of prorenin, renin, and the (pro)renin receptor: promising young players from the old renin-angiotensin-aldosterone system. J Cardiovasc Pharmacol 56(5):570–579

    Article  PubMed  CAS  Google Scholar 

  • Baldi JC, Hofman PL (2010) Does careful glycemic control improve aerobic capacity in subjects with type 1 diabetes? Exerc Sport Sci Rev 38(4):161–167

    Article  PubMed  Google Scholar 

  • Baldi JC, Cassuto NA, Foxx-Lupo WT, Wheatley CM, Snyder EM (2010) Glycemic status affects cardiopulmonary exercise response in athletes with type I diabetes. Med Sci Sports Exerc 42(8):1454–1459

    Article  PubMed  CAS  Google Scholar 

  • Beaver WL, Lamarra N, Wasserman K (1981) Breath-by-breath measurement of true alveolar gas exchange. J Appl Physiol 51(6):1662–1675

    PubMed  CAS  Google Scholar 

  • Bosman DR, Winkler AS, Marsden JT, Macdougall IC, Watkins PJ (2001) Anemia with erythropoietin deficiency occurs early in diabetic nephropathy. Diabetes Care 24(3):495–499

    Article  PubMed  CAS  Google Scholar 

  • Cherney DZ, Lai V, Scholey JW, Miller JA, Zinman B, Reich HN (2010) Effect of direct renin inhibition on renal hemodynamic function, arterial stiffness, and endothelial function in humans with uncomplicated type 1 diabetes: a pilot study. Diabetes Care 33(2):361–365

    Article  PubMed  CAS  Google Scholar 

  • de la Sierra A, Salazar J (2011) What is the role of direct renin inhibitors in the treatment of the hypertensive diabetic patient? Adv Ther 28(9):716–727

    Article  PubMed  CAS  Google Scholar 

  • Ditzel J (1976) Oxygen transport impairment in diabetes. Diabetes 25(2 SUPPL):832–838

    PubMed  CAS  Google Scholar 

  • Donnelly S (2001) Why is erythropoietin made in the kidney? The kidney functions as a critmeter. Am J Kidney Dis 38(2):415–425

    Article  PubMed  CAS  Google Scholar 

  • Donnelly S, Shah BR (1999) Erythropoietin deficiency in hyporeninemia. Am J Kidney Dis 33(5):947–953

    Article  PubMed  CAS  Google Scholar 

  • Dunn A, Donnelly S (2007) The role of the kidney in blood volume regulation: the kidney as a regulator of the hematocrit. Am J Med Sci 334(1):65–71

    Article  PubMed  CAS  Google Scholar 

  • Ekblom B (1968) Effect of physical training on oxygen transport system in man. Acta Physiologica Scandinavica 328(S):1–45

    Google Scholar 

  • Erslev AJ, Caro J, Besarab A (1985) Why the kidney? Nephron 41(3):213–216

    Article  PubMed  CAS  Google Scholar 

  • Gore CJ, Hahn AG, Burge CM, Telford RD (1997) VO2max and haemoglobin mass of trained athletes during high intensity training. Int J Sports Med 18(6):477–482

    Article  PubMed  CAS  Google Scholar 

  • Gusso S, Hofman P, Lalande S, Cutfield W, Robinson E, Baldi JC (2008) Impaired stroke volume and aerobic capacity in female adolescents with type 1 and type 2 diabetes mellitus. Diabetologia 51(7):1317–1320

    Article  PubMed  CAS  Google Scholar 

  • Hopkins WG (2000) Measures of reliability in sports medicine and science. Sports Med 30(1):1–15

    Article  PubMed  CAS  Google Scholar 

  • Jones AM, Carter H (2000) The effect of endurance training on parameters of aerobic fitness. Sports Med 29(6):373–386

    Article  PubMed  CAS  Google Scholar 

  • Kanstrup IL, Ekblom B (1984) Blood volume and hemoglobin concentration as determinants of maximal aerobic power. Med Sci Sports Exerc 16(3):256–262

    PubMed  CAS  Google Scholar 

  • Kikkawa R, Kitamura E, Fujiwara Y, Haneda M, Shigeta Y (1986) Biphasic alteration of renin-angiotensin-aldosterone system in streptozotocin-diabetic rats. Ren Physiol 9(3):187–192

    PubMed  CAS  Google Scholar 

  • Komatsu WR, Gabbay MA, Castro ML, Saraiva GL, Chacra AR, de Barros Neto TL, Dib SA (2005) Aerobic exercise capacity in normal adolescents and those with type 1 diabetes mellitus. Pediatr Diabetes 6(3):145–149

    Article  PubMed  Google Scholar 

  • Lalande S, Hofman PL, Baldi JC (2010) Effect of reduced total blood volume on left ventricular volumes and kinetics in type 2 diabetes. Acta Physiol (Oxf) 199(1):23–30

    Article  CAS  Google Scholar 

  • Lundby C, Thomsen JJ, Boushel R, Koskolou M, Warberg J, Calbet JA, Robach P (2007) Erythropoietin treatment elevates haemoglobin concentration by increasing red cell volume and depressing plasma volume. J Physiol 578(Pt 1):309–314

    PubMed  CAS  Google Scholar 

  • Lush DJ, King JA, Fray JC (1993) Pathophysiology of low renin syndromes: sites of renal renin secretory impairment and prorenin overexpression. Kidney Int 43(5):983–999

    Article  PubMed  CAS  Google Scholar 

  • Meriwether RA, McMahon PM, Islam N, Steinmann WC (2006) Physical activity assessment: validation of a clinical assessment tool. Am J Prev Med 31(6):484–491

    Article  PubMed  Google Scholar 

  • Mori H, Okubo M, Okamura M, Yamane K, Kado S, Egusa G, Hiramoto T, Hara H, Yamakido M (1992) Abnormalities of pulmonary function in patients with non-insulin-dependent diabetes mellitus. Intern Med 31(2):189–193

    Article  PubMed  CAS  Google Scholar 

  • Mosteller RD (1987) Simplified calculation of body-surface area. N Engl J Med 317(17):1098

    PubMed  CAS  Google Scholar 

  • Nadeau KJ, Regensteiner JG, Bauer TA, Brown MS, Dorosz JL, Hull A, Zeitler P, Draznin B, Reusch JEB (2010) Insulin resistance in adolescents with type 1 diabetes and its relationship to cardiovascular function. J Clin Endocrinol Metab 95(2):513–521

    Google Scholar 

  • Niranjan V, McBrayer DG, Ramirez LC, Raskin P, Hsia CCW (1997) Glycemic control and cardiopulmonary function in patients with insulin-dependent diabetes mellitus. Am J Med 103(6):504–513

    Article  PubMed  CAS  Google Scholar 

  • Palmieri V, Capaldo B, Russo C, Iaccarino M, Pezzullo S, Quintavalle G, Di Minno G, Riccardi G, Celentano A (2008) Uncomplicated type 1 diabetes and preclinical left ventricular myocardial dysfunction: insights from echocardiography and exercise cardiac performance evaluation. Diabetes Res Clin Pract 79(2):262–268

    Article  PubMed  Google Scholar 

  • Parisotto R, Gore CJ, Emslie KR, Ashenden MJ, Brugnara C, Howe C, Martin DT, Trout GJ, Hahn AG (2000) A novel method utilising markers of altered erythropoiesis for the detection of recombinant human erythropoietin abuse in athletes. Haematologica 85(6):564–572

    PubMed  CAS  Google Scholar 

  • Paulsen EP, Seip RL, Ayers CR, Croft BY, Kaiser DL (1989) Plasma renin activity and albumin excretion in teenage type I diabetic subjects. A prospective study. Hypertension 13(6 Pt 2):781–788

    Article  PubMed  CAS  Google Scholar 

  • Peltonen JE, Koponen AS, Pullinen K, Hagglund H, Aho JM, Kyrolainen H, Tikkanen HO (2012) Alveolar gas exchange and tissue deoxygenation during exercise in type 1 diabetes patients and healthy controls. Respir Physiol Neurobiol 181(3):267–276

    Article  PubMed  CAS  Google Scholar 

  • Prommer N, Heckel A, Schmidt W (2007) Timeframe to detect blood withdrawal associated with autologous blood doping. Med Sci Sports Exerc 39(5 Suppl):S3

    Google Scholar 

  • Schmidt W, Prommer N (2005) The optimised CO-rebreathing method: a new tool to determine total haemoglobin mass routinely. Eur J Appl Physiol 95(5–6):486–495

    Article  PubMed  CAS  Google Scholar 

  • Schmidt W, Prommer N (2010) Impact of Alterations in Total Hemoglobin Mass on VO2max. Exerc Sport Sci Rev 38(2):68–75

    Article  PubMed  Google Scholar 

  • Schmidt WF, Doerfler C, Wachsmuth N, Voelzke C, Treff G, Thoma S, Steinacker JAN, Prommer N (2009) Influence of body mass, body composition, and performance state on total hemoglobin mass: 2790: Board #184 May 29 3:30 PM–5:00 PM. Med Sci Sports Exerc 41(5 Supplement 1):541

    Google Scholar 

  • Thomas MC, MacIsaac RJ, Tsalamandris C, Molyneaux L, Goubina I, Fulcher G, Yue D, Jerums G (2004) Anemia in patients with type 1 diabetes. J Clin Endocrinol Metab 89(9):4359–4363

    Article  PubMed  CAS  Google Scholar 

  • Traynor J, Mactier R, Geddes CC, Fox JG (2006) How to measure renal function in clinical practice. Br Med J 333(7571):733–737

    Article  Google Scholar 

  • Veves A, Saouaf R, Donaghue VM, Mullooly CA, Kistler JA, Giurini JM, Horton ES, Fielding RA (1997) Aerobic exercise capacity remains normal despite impaired endothelial function in the micro- and macrocirculation of physically active IDDM patients. Diabetes 46(11):1846–1852

    Article  PubMed  CAS  Google Scholar 

  • Wanke T, Formanek D, Auinger M, Zwick H, Irsigler K (1992) Pulmonary gas exchange and oxygen uptake during exercise in patients with type 1 diabetes mellitus. Diabet Med 9(3):252–257

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was partly funded by Tekes—the Finnish Funding Agency for Technology and Innovation (40043/07), and Ministry of Education and Culture. We thank Ari Suojalehto, MD, Department of Sports and Exercise Medicine, Institute of Clinical Medicine, University of Helsinki, Finland, and Maija Kopo, Foundation for Sports and Exercise Medicine, Helsinki, Finland, for the assistance in collecting the data, and Prof. Stephen Cheung of Brock University, Canada, for critical review of the manuscript.

Conflict of interest

The authors have no conflict of interests.

Author information

Authors and Affiliations

  1. Department of Sports and Exercise Medicine, Institute of Clinical Medicine, University of Helsinki, Paasikivenkatu 4, 00250, Helsinki, Finland

    Anne S. Koponen, Juha E. Peltonen, Harriet J. Hägglund & Heikki O. Tikkanen

  2. Foundation for Sports and Exercise Medicine, Paasikivenkatu 4, 00250, Helsinki, Finland

    Juha E. Peltonen, Marja K. Päivinen, Jyrki M. Aho, Arja L. Uusitalo & Heikki O. Tikkanen

  3. Finnish Institute of Occupational Health, Topeliuksenkatu 41 a A, 00250, Helsinki, Finland

    Harri J. Lindholm

Authors
  1. Anne S. Koponen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juha E. Peltonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marja K. Päivinen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jyrki M. Aho
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Harriet J. Hägglund
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Arja L. Uusitalo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Harri J. Lindholm
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Heikki O. Tikkanen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anne S. Koponen.

Additional information

Communicated by Fabio Fischetti.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koponen, A.S., Peltonen, J.E., Päivinen, M.K. et al. Low total haemoglobin mass, blood volume and aerobic capacity in men with type 1 diabetes. Eur J Appl Physiol 113, 1181–1188 (2013). https://doi.org/10.1007/s00421-012-2532-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-012-2532-4

Keywords

Search

Navigation