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Int J Sports Med 2019; 40(09): 601-608
DOI: 10.1055/a-0946-1293
Clinical Sciences
© Georg Thieme Verlag KG Stuttgart · New York

Methodological Considerations for a Vascular Function Test Battery

Rachel Kimble
1   Sport, Exercise and Rehabilitation, Northumbria University, Newcastle upon Tyne, United Kingdom of Great Britain and Northern Ireland
,
Karen M. Keane
1   Sport, Exercise and Rehabilitation, Northumbria University, Newcastle upon Tyne, United Kingdom of Great Britain and Northern Ireland
,
John K. Lodge
2   Applied Sciences, Northumbria University, Newcastle upon Tyne, United Kingdom of Great Britain and Northern Ireland
,
Glyn Howatson
1   Sport, Exercise and Rehabilitation, Northumbria University, Newcastle upon Tyne, United Kingdom of Great Britain and Northern Ireland
› Author Affiliations
Further Information

Publication History



accepted 21 May 2019

Publication Date:
15 July 2019 (online)

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Abstract

There is a dearth of information regarding the reliability of non-invasive measures of vascular function taken in a single testing session. This study aimed to determine the test-retest reliability of a test battery of vascular function measures: automated blood pressure (BP), laser Doppler imaging with iontophoresis (LDI), digital volume pulse (DVP), pulse wave velocity (PWV), augmentation index (AIx) measured by pulse wave analysis (PWA) and flow-mediated dilation (FMD) taken within and between sessions. Measures were taken in 21 non-smoking males intra-session and again inter-session (one week apart) to determine repeatability and reproducibility, respectively. There was moderate to excellent repeatability (ICC: 0.53–0.93; CV=2.2–18.1%) and reproducibility (ICC: 0.71–0.96; CV 1.9–14.2%) for BP, DVP stiffness index, PWV, AIx, AIx normalised to heart rate (75 bpm), absolute and percentage FMD. Repeatability of the DVP reflection index was moderate (ICC: 0.64; CV=9.5%) but there was poor reproducibility (ICC: 0.17; CV=15.1%). Moreover, the repeatability and reproducibility of the LDI measures ranged from poor to good (ICC: 0.31–0.84; CV=28.4–36.7%). These data indicated that there was considerable variability in the repeatability and reproducibility of measurements of endothelial function and arterial stiffness taken in a battery of measurements, which needs careful consideration in future research designs.

Key words

endothelial function - arterial stiffness - repeatability - reproducibility
 

  • References

  • 1 Townsend N, Wilson L, Bhatnagar P, Wickramasinghe K, Rayner M, Nichols M. Cardiovascular disease in Europe: Epidemiological update 2016. Eur Heart J 2016; 37: 3232-3245
    CrossrefPubMedGoogle Scholar
  • 2 Yusuf S, Hawken S, Ôunpuu S, Dans T, Avezum A, Lanas F, McQueen M, Budaj A, Pais P, Varigos J. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): Case-control study. Lancet 2004; 364: 937-952
    CrossrefPubMedGoogle Scholar
  • 3 Herrod PJ, Doleman B, Blackwell JE, O’Boyle F, Williams JP, Lund JN, Phillips BE. Exercise and other nonpharmacological strategies to reduce blood pressure in older adults: A systematic review and meta-analysis. J Am Soc Hypertens 2018; 12: 248-267
    CrossrefPubMedGoogle Scholar
  • 4 Luís Â, Domingues F, Pereira L. Association between berries intake and cardiovascular diseases risk factors: A systematic review with meta-analysis and trial sequential analysis of randomized controlled trials. Food Funct 2018; 9: 740-757
    CrossrefPubMedGoogle Scholar
  • 5 Anderson TJ, Phillips SA. Assessment and prognosis of peripheral artery measures of vascular function. Prog Cardiovasc Dis 2015; 57: 497-509
    CrossrefPubMedGoogle Scholar
  • 6 Houston M. The role of noninvasive cardiovascular testing, applied clinical nutrition and nutritional supplements in the prevention and treatment of coronary heart disease. Ther Adv Cardiovasc Dis 2018; 12: 85-108
    CrossrefPubMedGoogle Scholar
  • 7 Keane KM, George TW, Constantinou CL, Brown MA, Clifford T, Howatson G. Effects of Montmorency tart cherry (Prunus Cerasus L.) consumption on vascular function in men with early hypertension. Am J Clin Nutr 2016; 103: 1531-1539
    CrossrefPubMedGoogle Scholar
  • 8 Okamoto T, Masuhara M, Ikuta K. Combined aerobic and resistance training and vascular function: Effect of aerobic exercise before and after resistance training. J Appl Physiol (1985) 2007; 103: 1655-1661
    CrossrefPubMedGoogle Scholar
  • 9 Rodriguez-Mateos A, Rendeiro C, Bergillos-Meca T, Tabatabaee S, George TW, Heiss C, Spencer JP. Intake and time dependence of blueberry flavonoid–induced improvements in vascular function: A randomized, controlled, double-blind, crossover intervention study with mechanistic insights into biological activity. Am J Clin Nutr 2013; 98: 1179-1191
    CrossrefPubMedGoogle Scholar
  • 10 Kay CD, Hooper L, Kroon PA, Rimm EB, Cassidy A. Relative impact of flavonoid composition, dose and structure on vascular function: A systematic review of randomised controlled trials of flavonoid-rich food products. Mol Nutr Food Res 2012; 56: 1605-1616
    CrossrefPubMedGoogle Scholar
  • 11 Ashor AW, Lara J, Siervo M, Celis-Morales C, Oggioni C, Jakovljevic DG, Mathers JC. Exercise modalities and endothelial function: A systematic review and dose–response meta-analysis of randomized controlled trials. Sports Med 2015; 45: 279-296
    CrossrefPubMedGoogle Scholar
  • 12 Fairlie-Jones L, Davison K, Fromentin E, Hill AM. The effect of anthocyanin-rich foods or extracts on vascular function in adults: A systematic review and meta-analysis of randomised controlled trials. Nutrients 2017; 9: 908
    CrossrefPubMedGoogle Scholar
  • 13 Pierce DR, Doma K, Leicht AS. Acute effects of exercise mode on arterial stiffness and wave reflection in healthy young adults: A systematic review and meta-analysis. Front Physiol 2018; 9: 73
    CrossrefPubMedGoogle Scholar
  • 14 Collier S, Kanaley J, Carhart Jr R, Frechette V, Tobin M, Hall A, Luckenbaugh A, Fernhall B. Effect of 4 weeks of aerobic or resistance exercise training on arterial stiffness, blood flow and blood pressure in pre-and stage-1 hypertensives. J Hum Hypertens 2008; 22: 678
    CrossrefPubMedGoogle Scholar
  • 15 Ashor AW, Lara J, Siervo M, Celis-Morales C, Mathers JC. Effects of exercise modalities on arterial stiffness and wave reflection: A systematic review and meta-analysis of randomized controlled trials. PLoS One 2014; 9: e110034
    Google Scholar
  • 16 Nigam A, Mitchell GF, Lambert J, Tardif JC. Relation between conduit vessel stiffness (assessed by tonometry) and endothelial function (assessed by flow-mediated dilatation) in patients with and without coronary heart disease. Am J Cardiol 2003; 92: 395-399
    CrossrefPubMedGoogle Scholar
  • 17 Hobbs DA, Goulding MG, Nguyen A, Malaver T, Walker CF, George TW, Methven L, Lovegrove JA. Acute ingestion of beetroot bread increases endothelium-independent vasodilation and lowers diastolic blood pressure in healthy men: A randomized controlled trial. J Nutr 2013; 143: 1399-1405
    CrossrefPubMedGoogle Scholar
  • 18 Ibrahimi K, De Graaf Y, Draijer R, Danser AJ, VanDenBrink AM, van den Meiracker AH. Reproducibility and agreement of different non-invasive methods of endothelial function assessment. Microvasc Res 2018; 117: 50-56
    CrossrefPubMedGoogle Scholar
  • 19 Woodman RJ, Kingwell BA, Beilin LJ, Hamilton SE, Dart AM, Watts GF. Assessment of central and peripheral arterial stiffness: Atudies indicating the need to use a combination of techniques. Am J Hypertens 2005; 18: 249-260
    CrossrefPubMedGoogle Scholar
  • 20 Millasseau S, Kelly R, Ritter J, Chowienczyk P. Determination of age-related increases in large artery stiffness by digital pulse contour analysis. Clin Sci 2002; 103: 371-377
    CrossrefPubMedGoogle Scholar
  • 21 Millasseau SC, Kelly RP, Ritter JM, Chowienczyk PJ. The vascular impact of aging and vasoactive drugs: Comparison of two digital volume pulse measurements. Am J Hypertens 2003; 16: 467-472
    CrossrefPubMedGoogle Scholar
  • 22 Mahe G, Comets E, Nouni A, Paillard F, Dourmap C, Le Faucheur A, Jaquinandi V. A minimal resting time of 25 min is needed before measuring stabilized blood pressure in subjects addressed for vascular investigations. Sci Rep 2017; 7: 12893
    CrossrefPubMedGoogle Scholar
  • 23 Green DJ, Dawson EA, Groenewoud HM, Jones H, Thijssen DH. Is flow-mediated dilation nitric oxide mediated? A meta-analysis. Hypertension 2014; 63: 376-382
    CrossrefPubMedGoogle Scholar
  • 24 Turner J, Belch JJ, Khan F. Current concepts in assessment of microvascular endothelial function using laser Doppler imaging and iontophoresis. Trends Cardiovasc Med 2008; 18: 109-116
    CrossrefPubMedGoogle Scholar
  • 25 Sugawara J, Komine H, Hayashi K, Yoshizawa M, Yokoi T, Otsuki T, Shimojo N, Miyauchi T, Maeda S, Tanaka H. Effect of systemic nitric oxide synthase inhibition on arterial stiffness in humans. Hypertens Res 2007; 30: 411
    CrossrefPubMedGoogle Scholar
  • 26 Harriss D, MacSween A, Atkinson G. Standards for ethics in sport and exercise science research: 2018 update. Int J Sports Med 2017; 38: 1126-1131
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Reinders A, Reggiori F, Shennan AH. Validation of the DINAMAP ProCare blood pressure device according to the international protocol in an adult population. Blood Press Monit 2006; 11: 293-296
    CrossrefPubMedGoogle Scholar
  • 28 Mancia G, Fagard R, Narkiewicz K, Redon J, Zanchetti A, Böhm M, Christiaens T, Cifkova R, De Backer G, Dominiczak A. 2013 ESH/ESC guidelines for the management of arterial hypertension: The Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). Blood Press 2013; 22: 193-278
    CrossrefPubMedGoogle Scholar
  • 29 National Clinical Guideline Centre (UK). Hypertension: The Clinical Management of Primary Hypertension in Adults: Update of Clinical Guidelines 18 and 34 [Internet]. London: Royal College of Physicians (UK); 2011 Aug. (NICE Clinical Guidelines, No. 127.) Available from: https://www.ncbi.nlm.nih.gov/books/NBK83274/
    PubMed
  • 30 Pickering TG, Hall JE, Appel LJ, Falkner BE, Graves J, Hill MN, Jones DW, Kurtz T, Sheps SG, Roccella EJ. Recommendations for blood pressure measurement in humans and experimental animals: Part 1: Blood pressure measurement in humans: A statement for professionals from the Subcommittee of Professional and Public Education of the American Heart Association Council on High Blood Pressure Research. Circulation 2005; 111: 697-716
    CrossrefPubMedGoogle Scholar
  • 31 Millasseau SC, Ritter JM, Takazawa K, Chowienczyk PJ. Contour analysis of the photoplethysmographic pulse measured at the finger. J Hypertens 2006; 24: 1449-1456
    CrossrefPubMedGoogle Scholar
  • 32 Pauca AL, O’rourke MF, Kon ND. Prospective evaluation of a method for estimating ascending aortic pressure from the radial artery pressure waveform. Hypertension 2001; 38: 932-937
    CrossrefPubMedGoogle Scholar
  • 33 Wilkinson IB, MacCallum H, Flint L, Cockcroft JR, Newby DE, Webb DJ. The influence of heart rate on augmentation index and central arterial pressure in humans. J Physiol 2000; 525: 263-270
    CrossrefPubMedGoogle Scholar
  • 34 Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: A report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002; 39: 257–265
    PubMed
  • 35 Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: A report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002; 39: 257-265
    PubMedGoogle Scholar
  • 36 Thijssen DH, Black MA, Pyke KE, Padilla J, Atkinson G, Harris RA, Parker B, Widlansky ME, Tschakovsky ME, Green DJ. Assessment of flow-mediated dilation in humans: A methodological and physiological guideline. Am J Physiol Heart Circ Physiol 2010; 300: H2-H12
    PubMedGoogle Scholar
  • 37 Hopkins WG. Measures of reliability in sports medicine and science. Sports Med 2000; 30: 1-15
    CrossrefPubMedGoogle Scholar
  • 38 Koo TK, Li MY. A guideline of selecting and reporting intraclass correlation coefficients for reliability research. J Chiropr Med 2016; 15: 155-163
    Google Scholar
  • 39 Batterham AM, George KP. Reliability in evidence-based clinical practice: A primer for allied health professionals. Phys Ther Sport 2000; 1: 54-62
    CrossrefPubMedGoogle Scholar
  • 40 Bedeian AG, Mossholder KW. On the use of the coefficient of variation as a measure of diversity. Organ Res Methods 2000; 3: 285-297
    CrossrefPubMedGoogle Scholar
  • 41 Tew GA, Klonizakis M, Moss J, Ruddock AD, Saxton JM, Hodges GJ. Reproducibility of cutaneous thermal hyperaemia assessed by laser Doppler flowmetry in young and older adults. Microvasc Res 2011; 81: 177-182
    CrossrefPubMedGoogle Scholar
  • 42 Atkinson G, Nevill AM. Statistical methods for assessing measurement error (reliability) in variables relevant to sports medicine. Sports Med 1998; 26: 217-238
    CrossrefPubMedGoogle Scholar
  • 43 Poitras VJ, Pyke KE. The impact of acute mental stress on vascular endothelial function: Evidence, mechanisms and importance. Int J Psychophysiol 2013; 88: 124-135
    CrossrefPubMedGoogle Scholar
  • 44 Stanforth PR, Gagnon J, Rice T, Bouchard C, Leon AS, Rao D, Skinner JS, Wilmore JH. Reproducibility of resting blood pressure and heart rate measurements: The HERITAGE Family Study. Ann Epidemiol 2000; 10: 271-277
    CrossrefPubMedGoogle Scholar
  • 45 Bonetti PO, Lerman LO, Lerman A. Endothelial dysfunction: A marker of atherosclerotic risk. Arterioscler Thromb Vasc Biol 2003; 23: 168-175
    CrossrefPubMedGoogle Scholar
  • 46 Grover-Páez F, Zavalza-Gómez AB. Endothelial dysfunction and cardiovascular risk factors. Diabetes Res Clin Pract 2009; 84: 1-10
    CrossrefPubMedGoogle Scholar
  • 47 Hansell J, Henareh L, Agewall S, Norman M. Non-invasive assessment of endothelial function–relation between vasodilatory responses in skin microcirculation and brachial artery. Clin Physiol Funct Imaging 2004; 24: 317-322
    CrossrefPubMedGoogle Scholar
  • 48 Anderson TJ. Arterial stiffness or endothelial dysfunction as a surrogate marker of vascular risk. Can J Cardiol 2006; 22: 72B-80B
    CrossrefPubMedGoogle Scholar
  • 49 Roustit M, Cracowski J-L. Assessment of endothelial and neurovascular function in human skin microcirculation. Trends Pharmacol Sci 2013; 34: 373-384
    CrossrefPubMedGoogle Scholar
  • 50 Loader J, Roustit M, Taylor F, MacIsaac RJ, Stewart S, Lorenzen C, Walther G. Assessing cutaneous microvascular function with iontophoresis: Avoiding non-specific vasodilation. Microvasc Res 2017; 113: 29-39
    CrossrefPubMedGoogle Scholar
  • 51 Jadhav S, Sattar N, Petrie JR, Cobbe SM, Ferrell WR. Reproducibility and repeatability of peripheral microvascular assessment using iontophoresis in conjunction with laser Doppler imaging. J Cardiovasc Pharmacol 2007; 50: 343-349
    CrossrefPubMedGoogle Scholar
  • 52 Jin Y, Alimbetov D, George T, Gordon M, Lovegrove JA. A randomised trial to investigate the effects of acute consumption of a blackcurrant juice drink on markers of vascular reactivity and bioavailability of anthocyanins in human subjects. Eur J Clin Nutr 2011; 65: 849
    CrossrefPubMedGoogle Scholar
  • 53 Macready AL, George TW, Chong MF, Alimbetov DS, Jin Y, Vidal A, Spencer JP, Kennedy OB, Tuohy KM, Minihane A-M. Flavonoid-rich fruit and vegetables improve microvascular reactivity and inflammatory status in men at risk of cardiovascular disease—FLAVURS: A randomized controlled trial. Am J Clin Nutr 2014; 99: 479-489
    CrossrefPubMedGoogle Scholar
  • 54 Kubli S, Waeber B, Dalle-Ave A, Feihl F. Reproducibility of laser Doppler imaging of skin blood flow as a tool to assess endothelial function. J Cardiovasc Pharmacol 2000; 36: 640-648
    CrossrefPubMedGoogle Scholar
  • 55 Morris S, Shore A. Skin blood flow responses to the iontophoresis of acetylcholine and sodium nitroprusside in man: Possible mechanisms. J Physiol 1996; 496: 531-542
    CrossrefPubMedGoogle Scholar
  • 56 Tibiriçá E, Matheus AS, Nunes B, Sperandei S, Gomes MB. Repeatability of the evaluation of systemic microvascular endothelial function using laser doppler perfusion monitoring: Clinical and statistical implications. Clinics 2011; 66: 599-605
    PubMedGoogle Scholar
  • 57 Bellien J, Iacob M, Gutierrez L, Isabelle M, Lahary A, Thuillez C, Joannides R. Crucial role of NO and endothelium-derived hyperpolarizing factor in human sustained conduit artery flow-mediated dilatation. Hypertension 2006; 48: 1088-1094
    CrossrefPubMedGoogle Scholar
  • 58 Newton D, Davies J, Belch J, Khan F. Role of endothelium-derived hyperpolarising factor in acetylcholine-mediated vasodilatation in skin. Int Angiol 2013; 32: 312-318
    PubMedGoogle Scholar
  • 59 Scholze A, Burkert A, Mardanzai K, Suvd-Erdene S, Hausberg M, Zidek W, Tepel M. Increased arterial vascular tone during the night in patients with essential hypertension. J Hum Hypertens 2007; 21: 60
    CrossrefPubMedGoogle Scholar
  • 60 van Mil AC, Greyling A, Zock PL, Geleijnse JM, Hopman MT, Mensink RP, Reesink KD, Green DJ, Ghiadoni L, Thijssen DH. Impact of volunteer-related and methodology-related factors on the reproducibility of brachial artery flow-mediated vasodilation: Analysis of 672 individual repeated measurements. J Hypertens 2016; 34: 1738-1745
    CrossrefPubMedGoogle Scholar
  • 61 Greyling A, van Mil AC, Zock PL, Green DJ, Ghiadoni L, Thijssen DH. Adherence to guidelines strongly improves reproducibility of brachial artery flow-mediated dilation. Atherosclerosis 2016; 248: 196-202
    CrossrefPubMedGoogle Scholar
  • 62 Mattace-Raso FU, van der Cammen TJ, Hofman A, van Popele NM, Bos ML, Schalekamp MA, Asmar R, Reneman RS, Hoeks AP, Breteler MM. Arterial stiffness and risk of coronary heart disease and stroke: The Rotterdam Study. Circulation 2006; 113: 657-663
    CrossrefPubMedGoogle Scholar
  • 63 Gunarathne A, Patel JV, Hughes EA, Lip GY. Measurement of stiffness index by digital volume pulse analysis technique: Clinical utility in cardiovascular disease risk stratification. Am J Hypertens 2008; 21: 866-872
    CrossrefPubMedGoogle Scholar
  • 64 Vakalis K, Bechlioulis A, Naka KK, Pappas K, Katsouras CS, Michalis LK. Clinical utility of digital volume pulse analysis in prediction of cardiovascular risk and the presence of angiographic coronary artery disease. Artery Res 2015; 9: 33-39
    CrossrefPubMedGoogle Scholar
  • 65 Tripkovic L, Hart KH, Frost GS, Lodge JK. Interindividual and intraindividual variation in pulse wave velocity measurements in a male population. Blood Press Monit 2014; 19: 233-241
    CrossrefPubMedGoogle Scholar
  • 66 Cheng LT, Tang LJ, Cheng L, Huang HY, Wang T. Limitation of the augmentation index for evaluating arterial stiffness. Hypertens Res 2007; 30: 713
    CrossrefPubMedGoogle Scholar
  • 67 Hughes AD, Park C, Davies J, Francis D, Thom SAM, Mayet J, Parker KH. Limitations of augmentation index in the assessment of wave reflection in normotensive healthy individuals. PLoS One 2013; 8: e59371
    CrossrefPubMedGoogle Scholar
  • 68 O'brien E, Asmar R, Beilin L, Imai Y, Mallion JM, Mancia G, Mengden T, Myers M, Padfield P, Palatini P. European Society of Hypertension recommendations for conventional, ambulatory and home blood pressure measurement. J Hypertens 2003; 21: 821-848
    CrossrefPubMedGoogle Scholar
  • 69 Sala C, Santin E, Rescaldani M, Magrini F. How long shall the patient rest before clinic blood pressure measurement?. Am J Hypertens 2006; 19: 713-717
    CrossrefPubMedGoogle Scholar