Advertisement

European Journal of Applied Physiology

, Volume 118, Issue 11, pp 2307–2318 | Cite as

Age-related attenuation of conduit artery blood flow response to passive heating differs between the arm and leg

  • Anna Oue
  • Chie Asashima
  • Risa Oizumi
  • Tomoko Ichinose-Kuwahara
  • Narihiko Kondo
  • Yoshimitsu Inoue
Original Article

Abstract

Purpose

Little is known about why the attenuation of heat loss responses with aging begins in the lower limbs. This study sought to determine whether passive heating causes the age-related decrease and limb-specific difference of blood flow (BF) responses between conduit brachial and femoral arteries, which are related to differences of cutaneous vascular conductance (CVC) between the upper and lower limbs.

Method

In 15 older and 12 younger males, BF in the brachial and femoral arteries was ultrasonically measured and CVC in the forearm and thigh was assessed during lower leg immersion in hot water at 42 °C (ambient temperature: 30 °C, relative humidity: 45%) for 40 min.

Results

The increased BF of brachial artery at the end of passive heating was similar between both age groups (older: 140 ± 4%; younger: 146 ± 11%), while that of femoral artery was smaller in older than younger group (119 ± 4% vs. 166 ± 11%, P < 0.01). Moreover, the increased CVC in the forearm was similar between the age groups (older: 356 ± 50%; younger: 308 ± 46%), although CVC in the thigh was significantly lower in older than younger group (303 ± 33% vs. 427 ± 51%, P < 0.05). These results corresponded to the BF responses of the brachial and femoral arteries, respectively.

Conclusion

These results indicate that age-related decrease and limb-specific difference occur also in conduit arteries of arm and leg, which might be related to the different reduction in CVC between forearm and thigh.

Keywords

Heat exposure Femoral artery blood flow Brachial artery blood flow Skin blood flow Older males 

Abbreviations

BF

Blood flow

CVC

Cutaneous vascular conductance

FMD

Flow-mediated vasodilation

HR

Heart rate

MAP

Mean arterial blood pressure

SkBF

Skin blood flow

SR

Sweat rate

\({\bar {T}_{\text{b}}}\)

Mean body temperature

Tor

Oral temperature

\({\bar {T}_{{\text{sk}}}}\)

Mean skin temperature

\(\dot {V}\)CO2

Carbon dioxide output

\(\dot {V}\)O2

Oxygen uptake

\(\dot {V}\)O2peak

Peak oxygen uptake

Notes

Acknowledgements

This research was supported by a grant from the Japan Society for the Promotion of Science, and a Grant-in-Aid for Scientific Research (No. 16207022 and No. 16H04851). We are grateful to the subjects who volunteered to participate in this study.

Author contributions

AO analyzed data and wrote the manuscript. CA, RO and TI-K conducted experiments and analyzed data. NK provided advice on the data about thermoregulation. YI conceived and designed research. All authors read and approved the manuscript.

References

  1. Al-Shaer MH, Choueiri NE, Correia ML, Sinkey CA, Barenz TA, Haynes WG (2006) Effects of aging and atherosclerosis on endothelial and vascular smooth muscle function in humans. Int J Cardiol 109:201–206PubMedCrossRefGoogle Scholar
  2. Amano T, Koga S, Inoue Y, Nishiyasu T, Kondo N (2013) Characteristics of sweating responses and peripheral sweat gland function during passive heating in sprinters. Eur J Appl Physiol 113:2067–2075PubMedCrossRefGoogle Scholar
  3. Brandes RP, Fleming I, Busse R (2005) Endothelial aging. Cardiovasc Res 66:286–294PubMedCrossRefGoogle Scholar
  4. Brunt VE, Howard MJ, Francisco MA, Ely BR, Minson CT (2016) Passive heat therapy improves endothelial function, arterial stiffness and blood pressure in sedentary humans. J Physiol 594:5329–5342PubMedPubMedCentralCrossRefGoogle Scholar
  5. Chiesa ST, Trangmar SJ, Kalsi KK, Rakobowchuk M, Banker DS, Lotlikar MD, Ali L, González-Alonso J (2015) Local temperature-sensitive mechanisms are important mediators of limb tissue hyperemia in the heat-stressed human at rest and during small muscle mass exercise. Am J Physiol Heart Circ Physiol 309:H369–H380PubMedPubMedCentralCrossRefGoogle Scholar
  6. Chiesa ST, Trangmar SJ, González-Alonso J (2016) Temperature and blood flow distribution in the human leg during passive heat stress. J Appl Physiol 120:1047–1058PubMedPubMedCentralCrossRefGoogle Scholar
  7. Dinenno FA, Jones PP, Seals DR, Tanaka H (1999) Limb blood flow and vascular conductance are reduced with age in healthy humans: relation to elevations in sympathetic nerve activity and declines in oxygen demand. Circulation 100:164–170PubMedCrossRefGoogle Scholar
  8. Dinenno FA, Seals DR, DeSouza CA, Tanaka H (2001) Age-related decreases in basal limb blood flow in humans: time course, determinants and habitual exercise effects. J Physiol 531:573–579PubMedPubMedCentralCrossRefGoogle Scholar
  9. Eiken O, Kölegård R (2004) Comparison of vascular distensibility in the upper and lower extremity. Acta Physiol Scand 181:281–287PubMedCrossRefGoogle Scholar
  10. Fujimoto S, Watanabe T (1969) Studies on the body surface area of Japanese. Acta Med Nagasaki 13:1–13Google Scholar
  11. Gagnon D, Romero SA, Ngo H, Sarma S, Cornwell WK, Poh P, Stoller D, Levine BD, Crandall CG (2017) Volume loading augments cutaneous vasodilatation and cardiac output of heat stressed older adults. J Physiol 595:6489–6498PubMedCrossRefGoogle Scholar
  12. Greaney JL, Stanhewicz AE, Proctor DN, Alexander LM, Kenney WL (2015) Impairments in central cardiovascular function contribute to attenuated reflex vasodilation in aged skin. J Appl Physiol 119:1411–1420PubMedPubMedCentralCrossRefGoogle Scholar
  13. Hardly RF, DuBois EF (1937) Regulation of heat loss from the human body. Proc Nat Acad Sci (Washington) 23:624–631CrossRefGoogle Scholar
  14. Havenith G, Inoue Y, Luttikholt V, Kenney WL (1995) Age predicts cardiovascular, but not thermoregulatory, responses to humid heat stress. Eur J Appl Physiol 70:88–96CrossRefGoogle Scholar
  15. Heinonen I, Brothers RM, Kemppainen J, Knuuti J, Kalliokoski KK, Crandall CG (2011) Local heating, but not indirect whole body heating, increases human skeletal muscle blood flow. J Appl Physiol 111:818–824PubMedPubMedCentralCrossRefGoogle Scholar
  16. Holowatz LA, Houghton BL, Wong BJ, Wilkins BW, Harding AW, Kenney WL, Minson CT (2003) Nitric oxide and attenuated reflex cutaneous vasodilation in aged skin. Am J Physiol Heart Circ Physiol 284:H1662–H1667PubMedCrossRefGoogle Scholar
  17. Holowatz LA, Thompson CS, Kenney WL (2006) l-Arginine supplementation or arginase inhibition augments reflex cutaneous vasodilatation in aged human skin. J Physiol 574:573–581PubMedPubMedCentralCrossRefGoogle Scholar
  18. Holowatz LA, Thompson-Torgerson CS, Kenney WL (2007) Altered mechanisms of vasodilation in aged human skin. Exerc Sport Sci Rev 35:119–125PubMedCrossRefGoogle Scholar
  19. Inoue Y, Nakao M, Okudaira S, Ueda H, Araki T (1995) Seasonal variation in sweating responses of older and younger men. Eur J Appl Physiol 70:6–12CrossRefGoogle Scholar
  20. Inoue Y, Shibasaki M, Hirata K, Araki T (1998) Relationship between skin blood flow and sweating rate, and age related regional differences. Eur J Appl Physiol 79:117–123CrossRefGoogle Scholar
  21. Inoue Y, Havenith G, Kenney WL, Loomis JL, Buskirk ER (1999a) Exercise- and methylcholine-induced sweating responses in older and younger men: effect of heat acclimation and aerobic fitness. Int J Biometeorol 42:210–216PubMedCrossRefGoogle Scholar
  22. Inoue Y, Shibasaki M, Ueda H, Ishizashi H (1999b) Mechanisms underlying the age-related decrement in the human sweating response. Eur J Appl Physiol Occup Physiol 79:121–126PubMedCrossRefGoogle Scholar
  23. Inoue Y, Shibasaki M, Araki T (2002) Strategy for preventing heat illness in children and the elderly. In: Nose H, Gisolfi CV, Imaizumi K (eds) Exercise, nutrition and environmental stress. Cooper Publishing Group, Traverse City, pp 239–271Google Scholar
  24. Inoue Y, Kuwahara T, Araki T (2004) Maturation- and aging-related changes in heat loss effector function. J Physiol Anthropol Appl Human Sci 23:289–294PubMedCrossRefGoogle Scholar
  25. Kenney WL, Fowler SR (1988) Methylcholine-activated eccrine sweat gland density and output as a function of age. J Appl Physiol 65:1082–1086PubMedCrossRefGoogle Scholar
  26. Kenney WL, Morgan AL, Farquhar WB, Brooks EM, Pierzga JM, Derr JA (1997) Decreased active vasodilator sensitivity in aged skin. Am J Physiol 272:H1609–H1614PubMedGoogle Scholar
  27. Kuhlenhoelter AM, Kim K, Neff D, Nie Y, Blaize AN, Wong BJ, Kuang S, Stout J, Song Q, Gavin TP, Roseguini BT (2016) Heat therapy promotes the expression of angiogenic regulators in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 311:R377–R391PubMedPubMedCentralCrossRefGoogle Scholar
  28. Martin HL, Loomis JL, Kenney WL (1995) Maximal skin vascular conductance in subjects aged 5–85 year. J Appl Physiol 79:297–301PubMedCrossRefGoogle Scholar
  29. McCarty MF, Barroso-Aranda J, Contreras F (2009) Regular thermal therapy may promote insulin sensitivity while boosting expression of endothelial nitric oxide synthase–effects comparable to those of exercise training. Med Hypotheses 73:103–105PubMedCrossRefGoogle Scholar
  30. Minson CT, Kenney WL (1997) Age and cardiac output cycle exercise in thermoneutral and warm. Med Sci Sports Exerc 29:75–81PubMedCrossRefGoogle Scholar
  31. Minson CT, Wladkowski SL, Cardell AF, Pawelczyk JA, Kenney WL (1998) Age alters the cardiovascular response to direct passive heating. J Appl Physiol 84:1323–1332PubMedCrossRefGoogle Scholar
  32. Minson CT, Wladkowski SL, Pawelczyk JA, Kenney WL (1999) Age, splanchnic vasoconstriction, and heat stress during tilting. Am J Physiol 276:R203–R212PubMedGoogle Scholar
  33. Moreau KL, Donato AJ, Tanaka H, Jones PP, Gates PE, Seals DR (2003) Basal leg blood flow in healthy women is related to age and hormone replacement therapy status. J Physiol 547:309–316PubMedCrossRefGoogle Scholar
  34. Neff D, Kuhlenhoelter AM, Lin C, Wong BJ, Motaganahalli RL, Roseguini BT (2016) Thermotherapy reduces blood pressure and circulating endothelin-1 concentration and enhances leg blood flow in patients with symptomatic peripheral artery disease. Am J Physiol Regul Integr Comp Physiol 311:R392–R400PubMedPubMedCentralCrossRefGoogle Scholar
  35. Newcomer SC, Leuenberger UA, Hogeman CS, Handly BD, Proctor DN (2004) Different vasodilator responses of human arms and legs. J Physiol 556:1001–1011PubMedPubMedCentralCrossRefGoogle Scholar
  36. Nishiyama SK, Wray DW, Richardson RS (2008) Aging affects vascular structure and function in a limb-specific manner. J Appl Physiol 105:1661–1670PubMedCrossRefGoogle Scholar
  37. Ooue A, Ichinose KT, Shamsuddin AKM, Inoue Y, Nishiyasu T, Koga S, Kondo N (2007) Changes in blood flow in a conduit artery and superficial vein of the upper arm during passive heating in humans. Eur J Appl Physiol 101:97–103PubMedCrossRefGoogle Scholar
  38. Ooue A, Ichinose TK, Inoue Y, Nishiyasu T, Koga S, Kondo N (2008) Changes in blood flow in conduit artery and veins of the upper arm during leg exercise in humans. Eur J Appl Physiol 103:367–373PubMedCrossRefGoogle Scholar
  39. Romero SA, Gagnon D, Adams AN, Cramer MN, Kouda K, Crandall CG (2017) Acute limb heating improves macro- and microvascular dilator function in the leg of aged humans. Am J Physiol Heart Circ Physiol 312:H89–H97PubMedCrossRefGoogle Scholar
  40. Sasaki T (1981) Body temperature. In: Nakayama A (ed) Thermal physiology. Rikogakusya, Tokyo, pp 6–32Google Scholar
  41. Seals DR, Esler MD (2000) Human ageing and the sympathoadrenal system. J Physiol 528:407–417PubMedPubMedCentralCrossRefGoogle Scholar
  42. Silber HA, Lima JA, Bluemke DA, Astor BC, Gupta SN, Foo TK, Ouyang P (2007) Arterial reactivity in lower extremities is progressively reduced as cardiovascular risk factors increase: comparison with upper extremities using magnetic resonance imaging. J Am Coll Cardiol 49:939–945PubMedCrossRefGoogle Scholar
  43. Stanhewicz AE, Alexander LM, Kenney WL (2015) Folic acid supplementation improves microvascular function in older adults through nitric oxide-dependent mechanisms. Clin Sci (Lond) 129:159–167CrossRefGoogle Scholar
  44. Taddei S, Virdis A, Ghiadoni L, Salvetti G, Bernini G, Magagna A, Salvetti A (2001) Age-related reduction of NO availability and oxidative stress in humans. Hypertension 38:274–279PubMedCrossRefGoogle Scholar
  45. Tao J, Jin YF, Yang Z, Wang LC, Gao XR, Lui L, Ma H (2004) Reduced arterial elasticity is associated with endothelial dysfunction in persons of advancing age: comparative study of noninvasive pulse wave analysis and laser Doppler blood flow measurement. Am J Hypertens 17:654–659PubMedCrossRefGoogle Scholar
  46. Wray DW, Uberoi A, Lawrenson L, Richardson RS (2006) Evidence of preserved endothelial function and vascular plasticity with age. Am J Physiol Heart Circ Physiol 290:H1271–H1277PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Anna Oue
    • 1
  • Chie Asashima
    • 2
  • Risa Oizumi
    • 2
  • Tomoko Ichinose-Kuwahara
    • 2
  • Narihiko Kondo
    • 3
  • Yoshimitsu Inoue
    • 2
  1. 1.Faculty of Food and Nutritional SciencesToyo UniversityGunmaJapan
  2. 2.Laboratory for Human Performance ResearchOsaka International UniversityMoriguchiJapan
  3. 3.Laboratory for Applied Human Physiology, Graduate School of Human Development and EnvironmentKobe UniversityKobeJapan

Personalised recommendations