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Published in: European Journal of Applied Physiology 5/2018

Open Access 01-05-2018 | Original Article

Forearm vasodilator responses to environmental stress and reactive hyperaemia are impaired in young South Asian men

Authors: Natalie G. Ormshaw, Rehan T. Junejo, Janice M. Marshall

Published in: European Journal of Applied Physiology | Issue 5/2018

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Abstract

Purpose

Prevalence of cardiovascular disease (CVD) is greater in South Asians (SAs) than White Europeans (WEs). Endothelial dysfunction and blunted forearm vasodilatation to environmental stressors have been implicated in CVD. We investigated whether these features are present in young SA men.

Methods

In 15 SA and 16 WE men (19–23 years), we compared changes in forearm blood flow, arterial blood pressure (ABP), forearm vascular conductance (FVC), heart rate, and electrodermal resistance (EDR; sweating) following release of arterial occlusion (reactive hyperaemia endothelium-dependent) and 5 single sounds at 5–10 min intervals (stressors).

Results

All were normotensive. Peak reactive hyperaemia was smaller in SAs than WEs (FVC increase: 0.36 ± 0.038 vs 0.44 ± 0.038 units; P < 0.05). Furthermore, in WEs, mean FVC increased at 5, 15, and 20 s of each sound (vasodilatation), but increased at 5 s only in SAs, decreasing by 20 s (vasoconstriction). This reflected a smaller proportion of SAs showing forearm vasodilatation at 15 s (5/15 SAs vs 11/16 WEs: P < 0.01), the remainder showing vasoconstriction. Concomitantly, WEs showed greater bradycardia and EDR changes. Intra-class correlation analyses showed that all responses were highly reproducible over five sounds in both WEs and SAs. Moreover, sound-evoked changes in ABP and FVC were negatively correlated in each ethnicity (P < 0.01). However, WEs showed preponderance of forearm vasodilatation and depressor responses; SAs showed preponderance of vasoconstriction and pressor responses.

Conclusions

Endothelium-dependent vasodilatation is blunted in young SA men. This could explain their impaired forearm vasodilatation and greater pressor responses to repeated environmental stressors, so predisposing SAs to hypertension and CVD.
Literature
go back to reference Agyemand C, Bhopal RS (2002) Is the blood pressure of South Asian adults in the UK higher or lower than that in European white adults? A review of cross-sectional data. J Hum Hypertens 16:739–751 Agyemand C, Bhopal RS (2002) Is the blood pressure of South Asian adults in the UK higher or lower than that in European white adults? A review of cross-sectional data. J Hum Hypertens 16:739–751
go back to reference Anderson TJ, Charbonneau F, Title LM, Buithieu J, Rose MS, Conradson H, Hildebrand K, Fung M. Verma S, Lonn EM (2011) Microvascular function predicts cardiovascular events in primary prevention: long-term results from the Firefighters and Their Endothelium (FATE) study. Circulation 123:163–169PubMed Anderson TJ, Charbonneau F, Title LM, Buithieu J, Rose MS, Conradson H, Hildebrand K, Fung M. Verma S, Lonn EM (2011) Microvascular function predicts cardiovascular events in primary prevention: long-term results from the Firefighters and Their Endothelium (FATE) study. Circulation 123:163–169PubMed
go back to reference Brod J, Fencl V, Hejl Z, Jirka J (1959) Circulatory changes underlying blood pressure elevation during acute emotional stress (mental arithmetic) in normotensive and hypertensive subjects. Clin Sci 18:269–279PubMed Brod J, Fencl V, Hejl Z, Jirka J (1959) Circulatory changes underlying blood pressure elevation during acute emotional stress (mental arithmetic) in normotensive and hypertensive subjects. Clin Sci 18:269–279PubMed
go back to reference Callister R, Suwarno NO, Seals DR (1992) Sympathetic activity is influenced by task difficulty and stress perception during mental challenge in humans. J Physiol 454:373–387PubMedPubMedCentral Callister R, Suwarno NO, Seals DR (1992) Sympathetic activity is influenced by task difficulty and stress perception during mental challenge in humans. J Physiol 454:373–387PubMedPubMedCentral
go back to reference Cardillo C, Kilcoyne CM, Canon RO III, Panza JA (1998a) Racial differences in the nitric oxide–mediated vasodilator response to mental stress in the forearm circulation. Hypertension 31:1235–1239PubMed Cardillo C, Kilcoyne CM, Canon RO III, Panza JA (1998a) Racial differences in the nitric oxide–mediated vasodilator response to mental stress in the forearm circulation. Hypertension 31:1235–1239PubMed
go back to reference Cardillo C, Kilcoyne CM, Cannon RO, Panza JA (1998b) Impairment of the nitric oxide–mediated vasodilator response to mental stress in hypertensive but not in hypercholesterolemic patients. JACC 32:1207–1213PubMed Cardillo C, Kilcoyne CM, Cannon RO, Panza JA (1998b) Impairment of the nitric oxide–mediated vasodilator response to mental stress in hypertensive but not in hypercholesterolemic patients. JACC 32:1207–1213PubMed
go back to reference Carlsson I, Sollevi A, Wennmalm A (1987) The role of myogenic relaxation, adenosine and prostaglandins in human forearm reactive hyperaemia. J Physiol 389:147–161PubMedPubMedCentral Carlsson I, Sollevi A, Wennmalm A (1987) The role of myogenic relaxation, adenosine and prostaglandins in human forearm reactive hyperaemia. J Physiol 389:147–161PubMedPubMedCentral
go back to reference Carter JR, Ray CA (2009) Sympathetic neural responses to mental stress: responders, nonresponders and sex differences. Am J Physiol Heart Circ Physiol 296:H847-853 Carter JR, Ray CA (2009) Sympathetic neural responses to mental stress: responders, nonresponders and sex differences. Am J Physiol Heart Circ Physiol 296:H847-853
go back to reference Chida Y, Steptoe A (2010) Greater cardiovascular responses to laboratory mental stress are associated with poor subsequent cardiovascular risk status: a meta-analysis of prospective evidence. Hypertension 55:1026–1032PubMed Chida Y, Steptoe A (2010) Greater cardiovascular responses to laboratory mental stress are associated with poor subsequent cardiovascular risk status: a meta-analysis of prospective evidence. Hypertension 55:1026–1032PubMed
go back to reference Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24:385–396PubMed Cohen S, Kamarck T, Mermelstein R (1983) A global measure of perceived stress. J Health Soc Behav 24:385–396PubMed
go back to reference Crecelius AR, Richards JC, Luckasen GJ, Larson DG, Dienno FA (2013) Reactive hyperemia occurs via activation of inwardly rectifying potassium channels and Na+/K+-ATPase in humans. Circ Res 113:1023–1032PubMed Crecelius AR, Richards JC, Luckasen GJ, Larson DG, Dienno FA (2013) Reactive hyperemia occurs via activation of inwardly rectifying potassium channels and Na+/K+-ATPase in humans. Circ Res 113:1023–1032PubMed
go back to reference Dakak N, Husain S, Mulcahy D, Andrews NP, Panza JA, Waclawiw M, Schenke W, Quyyumi AA (1998) Contribution of nitric oxide to reactive hyperemia impact of endothelial dysfunction. Hypertension 32:9–15PubMed Dakak N, Husain S, Mulcahy D, Andrews NP, Panza JA, Waclawiw M, Schenke W, Quyyumi AA (1998) Contribution of nitric oxide to reactive hyperemia impact of endothelial dysfunction. Hypertension 32:9–15PubMed
go back to reference Dietz NM, Rivera JM, Eggener SE, Fix RT, Warner DO, Joyner MJ (1994) Nitric oxide contributes to the rise in forearm blood flow during mental stress in humans. J Physiol 480:361–368PubMedPubMedCentral Dietz NM, Rivera JM, Eggener SE, Fix RT, Warner DO, Joyner MJ (1994) Nitric oxide contributes to the rise in forearm blood flow during mental stress in humans. J Physiol 480:361–368PubMedPubMedCentral
go back to reference Donadio V, Karlsson T, Elam M, Wallin BG (2002) Interindividual differences in sympathetic and effector responses to arousal in humans. J Physiol 544:293–302PubMedPubMedCentral Donadio V, Karlsson T, Elam M, Wallin BG (2002) Interindividual differences in sympathetic and effector responses to arousal in humans. J Physiol 544:293–302PubMedPubMedCentral
go back to reference Donadio V, Liguori R, Elam M, Karlsson T, Giannoccaro MP, Pegenius G, Giambattistelli F, Wallin BG (2012) Muscle sympathetic response to arousal predicts neurovascular reactivity during mental stress. J Physiol 590:2885–2896PubMedPubMedCentral Donadio V, Liguori R, Elam M, Karlsson T, Giannoccaro MP, Pegenius G, Giambattistelli F, Wallin BG (2012) Muscle sympathetic response to arousal predicts neurovascular reactivity during mental stress. J Physiol 590:2885–2896PubMedPubMedCentral
go back to reference Edwards CM, Marshall JM, Pugh M (1998) Lack of habituation of the pattern of cardiovascular response evoked by sound in subjects with primary Raynaud’s disease. Clin Sci 95:249–260 Edwards CM, Marshall JM, Pugh M (1998) Lack of habituation of the pattern of cardiovascular response evoked by sound in subjects with primary Raynaud’s disease. Clin Sci 95:249–260
go back to reference Edwards CM, Marshall JM, Pugh M (1999) Cardiovascular responses evoked by mild cool stimuli in primary Raynaud’s disease: the role of endothelin. Clin Sci 96:577–588 Edwards CM, Marshall JM, Pugh M (1999) Cardiovascular responses evoked by mild cool stimuli in primary Raynaud’s disease: the role of endothelin. Clin Sci 96:577–588
go back to reference Engelke KA, Halliwill JR, Proctor DN, Dietz NM, Joyner MJ (1996) Contribution of nitric oxide and prostaglandins to reactive hyperemia in the human forearm. J Appl Physiol 81:1807–1814PubMed Engelke KA, Halliwill JR, Proctor DN, Dietz NM, Joyner MJ (1996) Contribution of nitric oxide and prostaglandins to reactive hyperemia in the human forearm. J Appl Physiol 81:1807–1814PubMed
go back to reference Fonkoue IT, Carter JR (2015) Sympathetic neural reactivity to mental stress in humans: test–retest reproducibility. Am J Physiol Regul Integr Comp Physiol 309:R1380–R1386PubMedPubMedCentral Fonkoue IT, Carter JR (2015) Sympathetic neural reactivity to mental stress in humans: test–retest reproducibility. Am J Physiol Regul Integr Comp Physiol 309:R1380–R1386PubMedPubMedCentral
go back to reference Fonkoue IT, Wang M, Carter JR (2016) Sympathetic neural reactivity to mental stress in offspring of hypertensive parents: 20 years revisited. Am J Physiol Heart Circ Physiol 311:H426–H432PubMedPubMedCentral Fonkoue IT, Wang M, Carter JR (2016) Sympathetic neural reactivity to mental stress in offspring of hypertensive parents: 20 years revisited. Am J Physiol Heart Circ Physiol 311:H426–H432PubMedPubMedCentral
go back to reference Ghiadoni L, Donald AE, Cropley M, Mullen MJ, Oakley G, Taylor M, O’Connor G, Betteridge J, Klein N, Steptoe A, Deanfield JE (2002) Mental stress induces transient endothelial dysfunction in humans. Circulation 102:2473–2478 Ghiadoni L, Donald AE, Cropley M, Mullen MJ, Oakley G, Taylor M, O’Connor G, Betteridge J, Klein N, Steptoe A, Deanfield JE (2002) Mental stress induces transient endothelial dysfunction in humans. Circulation 102:2473–2478
go back to reference Gianaros PJ, Quigley KS (2001) Autonomic origins of a nonsignal stimulus-elicited bradycardia and its habituation in humans. Psychophysiology 38:540–547PubMedPubMedCentral Gianaros PJ, Quigley KS (2001) Autonomic origins of a nonsignal stimulus-elicited bradycardia and its habituation in humans. Psychophysiology 38:540–547PubMedPubMedCentral
go back to reference Gupta M, Singh N, Verma S (2006) South Asians and cardiovascular risk: what clinicians should know. Circulation 113:924–929 Gupta M, Singh N, Verma S (2006) South Asians and cardiovascular risk: what clinicians should know. Circulation 113:924–929
go back to reference Halliwill JR, Lawler LA, Eickhoff TJ, Dietz DM, Naus LA, Joyner MJ (1997) Forearm sympathetic withdrawal and vasodilatation during mental stress in humans. J Physiol 504:211–220PubMedPubMedCentral Halliwill JR, Lawler LA, Eickhoff TJ, Dietz DM, Naus LA, Joyner MJ (1997) Forearm sympathetic withdrawal and vasodilatation during mental stress in humans. J Physiol 504:211–220PubMedPubMedCentral
go back to reference Hilton SM (1982) The defence-arousal system and its relevance for circulatory and respiratory control. J Exp Biol 100:159–174PubMed Hilton SM (1982) The defence-arousal system and its relevance for circulatory and respiratory control. J Exp Biol 100:159–174PubMed
go back to reference Khan SG, Geer A, Fok HW, Shabeeh H, Brett SE, Shah AM, Chowienczyk PJ (2015) Impaired neuronal nitric oxide synthase–mediated vasodilator responses to mental stress in essential hypertension. Hypertension 65:903–909PubMed Khan SG, Geer A, Fok HW, Shabeeh H, Brett SE, Shah AM, Chowienczyk PJ (2015) Impaired neuronal nitric oxide synthase–mediated vasodilator responses to mental stress in essential hypertension. Hypertension 65:903–909PubMed
go back to reference Lambert EA, Schlaich MP (2004) Reduced sympathoneural responses to the cold pressor test in individuals with essential hypertension and in those genetically predisposed to hypertension. No support for the “pressor reactor” hypothesis of hypertension development. Am J Hypertens 17:863–868PubMed Lambert EA, Schlaich MP (2004) Reduced sympathoneural responses to the cold pressor test in individuals with essential hypertension and in those genetically predisposed to hypertension. No support for the “pressor reactor” hypothesis of hypertension development. Am J Hypertens 17:863–868PubMed
go back to reference Matsukawa T, Gotoh E, Uneda S, Miyajima E, Shionoiri H, Tochikubo O, Ishii M (1991) Augmented sympathetic nerve activity in response to stressors in young borderline hypertensive men. Acta Physiol Scand 141:157–165PubMed Matsukawa T, Gotoh E, Uneda S, Miyajima E, Shionoiri H, Tochikubo O, Ishii M (1991) Augmented sympathetic nerve activity in response to stressors in young borderline hypertensive men. Acta Physiol Scand 141:157–165PubMed
go back to reference Murphy C, Kanaganayagam GS, Jiang B, Chowienczyk PJ, Zbinden R, Saha M, Rahman S, Shah AM, Marber MS, Kearney MT (2007) Vascular dysfunction and reduced circulating endothelial progenitor cells in young healthy UK South Asian men. Arterioscler Thromb Vasc Biol 27:936–942PubMed Murphy C, Kanaganayagam GS, Jiang B, Chowienczyk PJ, Zbinden R, Saha M, Rahman S, Shah AM, Marber MS, Kearney MT (2007) Vascular dysfunction and reduced circulating endothelial progenitor cells in young healthy UK South Asian men. Arterioscler Thromb Vasc Biol 27:936–942PubMed
go back to reference Oparil S, Zaman MA, Calhoun DA (2003) Pathogenesis of hypertension. Ann Intern Med 139:761–776PubMed Oparil S, Zaman MA, Calhoun DA (2003) Pathogenesis of hypertension. Ann Intern Med 139:761–776PubMed
go back to reference Ormshaw N, Junejo J, Marshall JM (2016) Both endothelium-dependent dilator responses and muscle vasodilator responses to environmental stressors are impaired in young South Asians and may predispose to hypertension. J Hum Hypertens 29:644 PD03 Ormshaw N, Junejo J, Marshall JM (2016) Both endothelium-dependent dilator responses and muscle vasodilator responses to environmental stressors are impaired in young South Asians and may predispose to hypertension. J Hum Hypertens 29:644 PD03
go back to reference Raji A, Gerhard-Herman MD, Warren M, Silverman SG, Raptopoulos V, Mantzoros CS, Simonson DC (2004) Insulin resistance and vascular dysfunction in nondiabetic Asian Indians. J Clin Endocrinol Metab 89:3965–3972PubMed Raji A, Gerhard-Herman MD, Warren M, Silverman SG, Raptopoulos V, Mantzoros CS, Simonson DC (2004) Insulin resistance and vascular dysfunction in nondiabetic Asian Indians. J Clin Endocrinol Metab 89:3965–3972PubMed
go back to reference Rana A, de Souza RJ, Kandasamy S, Lear SA, Anand SS (2014) Cardiovascular risk among South Asians living in Canada: a systematic review and meta-analysis. CMAJ Open 2:E183-191 Rana A, de Souza RJ, Kandasamy S, Lear SA, Anand SS (2014) Cardiovascular risk among South Asians living in Canada: a systematic review and meta-analysis. CMAJ Open 2:E183-191
go back to reference Ray CJ, Abbas MR, Coney AM, Marshall JM (2002) Interactions of adenosine, prostaglandins and nitric oxide in hypoxia-induced vasodilatation: in vivo and in vitro studies. J Physiol 544:195–209PubMedPubMedCentral Ray CJ, Abbas MR, Coney AM, Marshall JM (2002) Interactions of adenosine, prostaglandins and nitric oxide in hypoxia-induced vasodilatation: in vivo and in vitro studies. J Physiol 544:195–209PubMedPubMedCentral
go back to reference Schlach MP, Ahlers BA, Parnell MM, Kaye DM (2002) βAdrenoceptor-mediated, nitric-oxide-dependent vasodilatation is abnormal in early hypertension: restoration by l-arginine. J Hypertens 22:1917–1925 Schlach MP, Ahlers BA, Parnell MM, Kaye DM (2002) β­Adrenoceptor-mediated, nitric-oxide-dependent vasodilatation is abnormal in early hypertension: restoration by l-arginine. J Hypertens 22:1917–1925
go back to reference Schneider GM, Jacobs DW, Gevirtz RN, O’Connor DT (2003) Cardiovascular haemodynamic response to repeated mental stress in normotensive subjects at genetic risk of hypertension: evidence of enhanced reactivity, blunted adaptation and delayed recovery. J Hum Hypertens 17:829–840PubMed Schneider GM, Jacobs DW, Gevirtz RN, O’Connor DT (2003) Cardiovascular haemodynamic response to repeated mental stress in normotensive subjects at genetic risk of hypertension: evidence of enhanced reactivity, blunted adaptation and delayed recovery. J Hum Hypertens 17:829–840PubMed
go back to reference Schwartz CE, Durocher JJ, Carter JR (2011) Neurovascular responses to mental stress in prehypertensive humans. J Appl Physiol 110:76–82PubMed Schwartz CE, Durocher JJ, Carter JR (2011) Neurovascular responses to mental stress in prehypertensive humans. J Appl Physiol 110:76–82PubMed
go back to reference Seddon MD, Chowienczyk PJ, Brett SE, Casadei B, Shah AM (2008) Neuronal nitric oxide synthase regulates basal microvascular tone in humans in vivo. Circulation 117:1991–1996PubMed Seddon MD, Chowienczyk PJ, Brett SE, Casadei B, Shah AM (2008) Neuronal nitric oxide synthase regulates basal microvascular tone in humans in vivo. Circulation 117:1991–1996PubMed
go back to reference Tagawa T, Imaizumi T, Endo T, Shiramoto M, Harasawa Y, Takeshita A (1994) Role of nitric oxide in reactive hyperemia in human forearm vessels. Circulation 90:2285–2290PubMed Tagawa T, Imaizumi T, Endo T, Shiramoto M, Harasawa Y, Takeshita A (1994) Role of nitric oxide in reactive hyperemia in human forearm vessels. Circulation 90:2285–2290PubMed
go back to reference Turpin G, Schaefer F, Boucsein W (1999) Effects of stimulus intensity, risetime, and duration on autonomic and behavioral responding: Implications for the differentiation of orienting, startle, and defense responses. Psychophysiology 36:453–463PubMed Turpin G, Schaefer F, Boucsein W (1999) Effects of stimulus intensity, risetime, and duration on autonomic and behavioral responding: Implications for the differentiation of orienting, startle, and defense responses. Psychophysiology 36:453–463PubMed
go back to reference Wild SH, Fischbacher C, Brock A, Griffiths C, Bhopal R (2007) Mortality from all causes and circulatory disease by country of birth in England and Wales 2001–2003. J Public Health (Oxf) 29:191–198 Wild SH, Fischbacher C, Brock A, Griffiths C, Bhopal R (2007) Mortality from all causes and circulatory disease by country of birth in England and Wales 2001–2003. J Public Health (Oxf) 29:191–198
go back to reference Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, McQueen M, Budaj A, Pais P, Vargios J, Lisheng L (2004) Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case–control study. Lancet 364:937–952PubMed Yusuf S, Hawken S, Ounpuu S, Dans T, Avezum A, Lanas F, McQueen M, Budaj A, Pais P, Vargios J, Lisheng L (2004) Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case–control study. Lancet 364:937–952PubMed
go back to reference Zbrozyna AW, Krebbel F (1985) Habituation of the cold pressor response in normo- and hypertensive human subjects. Eur J Appl Physiol 54:136–144 Zbrozyna AW, Krebbel F (1985) Habituation of the cold pressor response in normo- and hypertensive human subjects. Eur J Appl Physiol 54:136–144
go back to reference Zbrozyna A, Westwood D (1988) Habituation of vasodilatation in the calf elicited by repeated sensory stimulation in man. Eur J Appl Physiol 58:284–290 Zbrozyna A, Westwood D (1988) Habituation of vasodilatation in the calf elicited by repeated sensory stimulation in man. Eur J Appl Physiol 58:284–290
Metadata
Title
Forearm vasodilator responses to environmental stress and reactive hyperaemia are impaired in young South Asian men
Authors
Natalie G. Ormshaw
Rehan T. Junejo
Janice M. Marshall
Publication date
01-05-2018
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 5/2018
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-018-3829-8

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