Abstract
Purpose
Low vitamin D levels have been associated with elevated blood pressure in the general population. Prospective studies, however, have produced conflicting evidence about the blood pressure-lowering effects of vitamin D supplementation. Cardiorespiratory fitness may modulate the vitamin D–blood pressure association. We therefore examined this association in professional athletes, whose high training load serves as a biological control for physical fitness.
Methods
50 male professional handball players (age 26 ± 5 years) were examined. We assessed the central aortic pressure parameters using transfer function-based analysis of oscillometrically obtained peripheral arterial waveforms. Serum 25-OH vitamin D concentrations were determined by chemiluminescent immunoassay. The threshold for insufficiency was set at values of < 30 ng/mL.
Results
Central blood pressure (cBP) was 98 ± 7/60 ± 10 mmHg. The aortic pulse wave velocity (PWV) was 6.3 ± 1.0 m/s. Nine athletes (18%) displayed insufficient 25-OH vitamin D levels and had a significantly (p < 0.01) higher cBP compared with the 41 (82%) athletes with sufficient 25-OH vitamin D levels (106 ± 5/68 ± 8 vs. 97 ± 7/58 ± 9 mmHg). Central systolic blood pressure (cSBP) in vitamin D-sufficient athletes was significantly lower in comparison to the healthy reference population (97 mmHg vs. 103 mmHg, p < 0.001). This significance of difference was lost in vitamin D-insufficient athletes (106 mmHg vs. 103 mmHg, p = 0.12).
Conclusion
Significantly raised central systolic and diastolic blood pressure in vitamin D-insufficient elite athletes implicates vitamin D as a potential modifier of vascular functional health.
Similar content being viewed by others
Abbreviations
- Aix:
-
Augmentation index
- Aix@75:
-
Augmentation index at heart rate of 75 beats per minute
- BMI:
-
Body mass index
- cBP:
-
Central blood pressure
- cDBP:
-
Central diastolic blood pressure
- cSBP:
-
Central systolic blood pressure
- CRF:
-
Cardiorespiratory fitness
- CLIA:
-
Chemiluminescent immunoassay
- ECG:
-
Electrocardiogram
- K2EDTA:
-
Dipotassium ethylene diamine tetra-acetic acid
- min:
-
Minute
- MPO:
-
Maximum power output
- PTH:
-
Parathyroid hormone
- PWV:
-
Aortic pulse wave velocity
- RHR:
-
Resting heart rate
- SD:
-
Standard deviation
- VO2max :
-
Maximum oxygen uptake
References
Al Mheid I, Patel R, Murrow J, Morris A, Rahman A, Fike L, Kavtaradze N, Uphoff I, Hooper C, Tangpricha V, Alexander RW, Brigham K, Quyyumi AA (2011) Vitamin D status is associated with arterial stiffness and vascular dysfunction in healthy humans. J Am Coll Cardiol 58(2):186–192. https://doi.org/10.1016/j.jacc.2011.02.051
Anderson JL, May HT, Horne BD, Bair TL, Hall NL, Carlquist JF, Lappe DL, Muhlestein JB, Intermountain Heart Collaborative Study G (2010) Relation of vitamin D deficiency to cardiovascular risk factors, disease status, and incident events in a general healthcare population. Am J Cardiol 106(7):963–968. https://doi.org/10.1016/j.amjcard.2010.05.027
Arora P, Wang TJ (2017) Effect of vitamin D supplementation on arterial stiffness and central blood pressure indexes: demystifying the evidence. J Am Heart Assoc 6:10. https://doi.org/10.1161/JAHA.117.007466
Ashor AW, Lara J, Siervo M, Celis-Morales C, Mathers JC (2014) Effects of exercise modalities on arterial stiffness and wave reflection: a systematic review and meta-analysis of randomized controlled trials. PLoS One 9(10):e110034. https://doi.org/10.1371/journal.pone.0110034
Aspelund T, Grubler MR, Smith AV, Gudmundsson EF, Keppel M, Cotch MF, Harris TB, Jorde R, Grimnes G, Joakimsen R, Schirmer H, Wilsgaard T, Mathiesen EB, Njolstad I, Lochen ML, Marz W, Kleber ME, Tomaschitz A, Grove-Laugesen D, Rejnmark L, Swart KMA, Brouwer IA, Lips P, van Schoor NM, Sempos CT, Durazo-Arvizu RA, Skrabakova Z, Dowling KG, Cashman KD, Kiely M, Pilz S, Gudnason V, Eiriksdottir G (2019) Effect of genetically low 25-hydroxyvitamin D on mortality risk: Mendelian randomization analysis in 3 large European cohorts. Nutrients 11:1. https://doi.org/10.3390/nu11010074
Bauer P, Henni S, Dorr O, Bauer T, Hamm CW, Most A (2018) High prevalence of vitamin D insufficiency in professional handball athletes. Phys Sportsmed 2018:1–7. https://doi.org/10.1080/00913847.2018.1520055
Beveridge LA, Struthers AD, Khan F, Jorde R, Scragg R, Macdonald HM, Alvarez JA, Boxer RS, Dalbeni A, Gepner AD, Isbel NM, Larsen T, Nagpal J, Petchey WG, Stricker H, Strobel F, Tangpricha V, Toxqui L, Vaquero MP, Wamberg L, Zittermann A, Witham MD, Collaboration DP (2015) Effect of vitamin D supplementation on blood pressure: a systematic review and meta-analysis incorporating individual patient data. JAMA Intern Med 175(5):745–754. https://doi.org/10.1001/jamainternmed.2015.0237
Caselli S, Vaquer Segui A, Quattrini F, Di Gacinto B, Milan A, Assorgi R, Verdile L, Spataro A, Pelliccia A (2016) Upper normal values of blood pressure response to exercise in Olympic athletes. Am Heart J 177:120–128. https://doi.org/10.1016/j.ahj.2016.04.020
Cheng HM, Chuang SY, Sung SH, Yu WC, Pearson A, Lakatta EG, Pan WH, Chen CH (2013) Derivation and validation of diagnostic thresholds for central blood pressure measurements based on long-term cardiovascular risks. J Am Coll Cardiol 62(19):1780–1787. https://doi.org/10.1016/j.jacc.2013.06.029
Christakos S, Hewison M, Gardner DG, Wagner CL, Sergeev IN, Rutten E, Pittas AG, Boland R, Ferrucci L, Bikle DD (2013) Vitamin D: beyond bone. Ann N Y Acad Sci 1287:45–58. https://doi.org/10.1111/nyas.12129
Davidson T, Vainshelboim B, Kokkinos P, Myers J, Ross R (2018) Cardiorespiratory fitness versus physical activity as predictors of all-cause mortality in men. Am Heart J 196:156–162. https://doi.org/10.1016/j.ahj.2017.08.022
Denham J, Brown NJ, Tomaszewski M, Williams B, O'Brien BJ, Charchar FJ (2016) Aortic augmentation index in endurance athletes: a role for cardiorespiratory fitness. Eur J Appl Physiol 116(8):1537–1544. https://doi.org/10.1007/s00421-016-3407-x
Eijsvogels TMH, Thompson PD, Franklin BA (2018) The "Extreme Exercise Hypothesis": recent findings and cardiovascular health implications. Curr Treat Options Cardiovasc Med 20(10):84. https://doi.org/10.1007/s11936-018-0674-3
Fan F, Qi L, Jia J, Xu X, Liu Y, Yang Y, Qin X, Li J, Li H, Zhang Y, Huo Y (2016) Noninvasive central systolic blood pressure is more strongly related to kidney function decline than peripheral systolic blood pressure in a Chinese community-based population. Hypertension 67(6):1166–1172. https://doi.org/10.1161/HYPERTENSIONAHA.115.07019
Forman JP, Williams JS, Fisher ND (2010) Plasma 25-hydroxyvitamin D and regulation of the renin–angiotensin system in humans. Hypertension 55(5):1283–1288. https://doi.org/10.1161/HYPERTENSIONAHA.109.148619
Franzen K, Reppel M, Koster J, Mortensen K (2016) Acute and chronic effects on central hemodynamics and arterial stiffness in professional rowers. Physiol Meas 37(4):544–553. https://doi.org/10.1088/0967-3334/37/4/544
Green DJ, Smith KJ (2018) Effects of exercise on vascular function, structure, and health in humans. Cold Spring Harb Perspect Med 8:4. https://doi.org/10.1101/cshperspect.a029819
Harriss DJ, Macsween A, Atkinson G (2017) Standards for ethics in sport and exercise science research: 2018 update. Int J Sports Med 38(14):1126–1131. https://doi.org/10.1055/s-0043-124001
He CS, Aw Yong XH, Walsh NP, Gleeson M (2016) Is there an optimal vitamin D status for immunity in athletes and military personnel? Exerc Immunol Rev 22:42–64
Herbert A, Cruickshank JK, Laurent S, Boutouyrie P, Values Reference, for Arterial Measurements C, (2014) Establishing reference values for central blood pressure and its amplification in a general healthy population and according to cardiovascular risk factors. Eur Heart J 35(44):3122–3133. https://doi.org/10.1093/eurheartj/ehu293
Hodson B, Norton GR, Booysen HL, Sibiya MJ, Raymond A, Maseko MJ, Majane OH, Libhaber E, Sareli P, Woodiwiss AJ (2016) Brachial pressure control fails to account for most distending pressure-independent, age-related aortic hemodynamic changes in adults. Am J Hypertens 29(5):605–613. https://doi.org/10.1093/ajh/hpv140
Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, Murad MH, Weaver CM, Endocrine S (2011) Evaluation, treatment, and prevention of vitamin D deficiency: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab 96(7):1911–1930. https://doi.org/10.1210/jc.2011-0385
Holick MF, Binkley NC, Bischoff-Ferrari HA, Gordon CM, Hanley DA, Heaney RP, Murad MH, Weaver CM (2012) Guidelines for preventing and treating vitamin D deficiency and insufficiency revisited. J Clin Endocrinol Metab 97(4):1153–1158. https://doi.org/10.1210/jc.2011-2601
Kaess BM, Rong J, Larson MG, Hamburg NM, Vita JA, Levy D, Benjamin EJ, Vasan RS, Mitchell GF (2012) Aortic stiffness, blood pressure progression, and incident hypertension. JAMA 308(9):875–881. https://doi.org/10.1001/2012.jama.10503
Knez WL, Sharman JE, Jenkins DG, Coombes JS (2008) Central hemodynamics in ultra-endurance athletes. J Sci Med Sport 11(4):390–395. https://doi.org/10.1016/j.jsams.2006.11.005
Krzywanski J, Mikulski T, Krysztofiak H, Mlynczak M, Gaczynska E, Ziemba A (2016) Seasonal vitamin D status in Polish Elite athletes in relation to sun exposure and oral supplementation. PLoS One 11(10):e0164395. https://doi.org/10.1371/journal.pone.0164395
Kunutsor SK, Apekey TA, Steur M (2013) Vitamin D and risk of future hypertension: meta-analysis of 283,537 participants. Eur J Epidemiol 28(3):205–221. https://doi.org/10.1007/s10654-013-9790-2
La Gerche A, Heidbuchel H (2014) Can intensive exercise harm the heart? You can get too much of a good thing. Circulation 130(12):992–1002. https://doi.org/10.1161/CIRCULATIONAHA.114.008141
La Gerche A, Burns AT, Mooney DJ, Inder WJ, Taylor AJ, Bogaert J, Macisaac AI, Heidbuchel H, Prior DL (2012) Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J 33(8):998–1006. https://doi.org/10.1093/eurheartj/ehr397
Laurent P, Marenco P, Castagna O, Smulyan H, Blacher J, Safar ME (2011) Differences in central systolic blood pressure and aortic stiffness between aerobically trained and sedentary individuals. J Am Soc Hypertens 5(2):85–93. https://doi.org/10.1016/j.jash.2011.01.003
Lee DC, Artero EG, Sui X, Blair SN (2010) Mortality trends in the general population: the importance of cardiorespiratory fitness. J Psychopharmacol 24(4 Suppl):27–35. https://doi.org/10.1177/1359786810382057
Lee IM, Shiroma EJ, Lobelo F, Puska P, Blair SN, Katzmarzyk PT, Lancet Physical Activity Series Working G (2012) Effect of physical inactivity on major non-communicable diseases worldwide: an analysis of burden of disease and life expectancy. Lancet 380(9838):219–229. https://doi.org/10.1016/S0140-6736(12)61031-9
Levine BD, Baggish AL, Kovacs RJ, Link MS, Maron MS, Mitchell JH, American Heart Association E, Arrhythmias Committee of Council on Clinical Cardiology CoCDiYCoC, Stroke Nursing CoFG, Translational B, American College of C (2015) Eligibility and disqualification recommendations for competitive athletes with cardiovascular abnormalities: task force 1: classification of sports: dynamic, static, and impact: a scientific statement from the American Heart Association and American College of Cardiology. Circulation 132(22):e262–266. https://doi.org/10.1161/CIR.0000000000000237
Maroon JC, Mathyssek CM, Bost JW, Amos A, Winkelman R, Yates AP, Duca MA, Norwig JA (2015) Vitamin D profile in National Football League players. Am J Sports Med 43(5):1241–1245. https://doi.org/10.1177/0363546514567297
Mehran N, Schulz BM, Neri BR, Robertson WJ, Limpisvasti O (2016) Prevalence of vitamin D insufficiency in professional hockey players. Orthop J Sports Med 4(12):2325967116677512. https://doi.org/10.1177/2325967116677512
Merghani A, Maestrini V, Rosmini S, Cox AT, Dhutia H, Bastiaenan R, David S, Yeo TJ, Narain R, Malhotra A, Papadakis M, Wilson MG, Tome M, AlFakih K, Moon JC, Sharma S (2017) Prevalence of subclinical coronary artery disease in masters endurance athletes with a low atherosclerotic risk profile. Circulation 136(2):126–137. https://doi.org/10.1161/CIRCULATIONAHA.116.026964
Mitchell GF (2009) Arterial stiffness and wave reflection: biomarkers of cardiovascular risk. Artery Res 3(2):56–64. https://doi.org/10.1016/j.artres.2009.02.002
Morton JP, Iqbal Z, Drust B, Burgess D, Close GL, Brukner PD (2012) Seasonal variation in vitamin D status in professional soccer players of the English Premier League. Appl Physiol Nutr Metab 37(4):798–802. https://doi.org/10.1139/h2012-037
Norman AW (2008) From vitamin D to hormone D: fundamentals of the vitamin D endocrine system essential for good health. Am J Clin Nutr 88(2):491S–499S. https://doi.org/10.1093/ajcn/88.2.491S
Owens DJ, Fraser WD, Close GL (2015) Vitamin D and the athlete: emerging insights. Eur J Sport Sci 15(1):73–84. https://doi.org/10.1080/17461391.2014.944223
Pludowski P, Karczmarewicz E, Bayer M, Carter G, Chlebna-Sokol D, Czech-Kowalska J, Debski R, Decsi T, Dobrzanska A, Franek E, Gluszko P, Grant WB, Holick MF, Yankovskaya L, Konstantynowicz J, Ksiazyk JB, Ksiezopolska-Orlowska K, Lewinski A, Litwin M, Lohner S, Lorenc RS, Lukaszkiewicz J, Marcinowska-Suchowierska E, Milewicz A, Misiorowski W, Nowicki M, Povoroznyuk V, Rozentryt P, Rudenka E, Shoenfeld Y, Socha P, Solnica B, Szalecki M, Talalaj M, Varbiro S, Zmijewski MA (2013) Practical guidelines for the supplementation of vitamin D and the treatment of deficits in Central Europe—recommended vitamin D intakes in the general population and groups at risk of vitamin D deficiency. Endokrynol Pol 64(4):319–327
Priemel M, von Domarus C, Klatte TO, Kessler S, Schlie J, Meier S, Proksch N, Pastor F, Netter C, Streichert T, Puschel K, Amling M (2010) Bone mineralization defects and vitamin D deficiency: histomorphometric analysis of iliac crest bone biopsies and circulating 25-hydroxyvitamin D in 675 patients. J Bone Miner Res 25(2):305–312. https://doi.org/10.1359/jbmr.090728
Rodriguez AJ, Scott D, Srikanth V, Ebeling P (2016) Effect of vitamin D supplementation on measures of arterial stiffness: a systematic review and meta-analysis of randomized controlled trials. Clin Endocrinol (Oxf) 84(5):645–657. https://doi.org/10.1111/cen.13031
Roman MJ, Devereux RB, Kizer JR, Lee ET, Galloway JM, Ali T, Umans JG, Howard BV (2007) Central pressure more strongly relates to vascular disease and outcome than does brachial pressure: the Strong Heart Study. Hypertension 50(1):197–203. https://doi.org/10.1161/HYPERTENSIONAHA.107.089078
Schumacher G, Kaden JJ, Trinkmann F (2018) Multiple coupled resonances in the human vascular tree: refining the Westerhof model of the arterial system. J Appl Physiol 1985 124(1):131–139. https://doi.org/10.1152/japplphysiol.00405.2017
Scragg R, Stewart AW, Waayer D, Lawes CMM, Toop L, Sluyter J, Murphy J, Khaw KT, Camargo CA Jr (2017) Effect of monthly high-dose vitamin D supplementation on cardiovascular disease in the vitamin D assessment study : a randomized clinical trial. JAMA Cardiol 2(6):608–616. https://doi.org/10.1001/jamacardio.2017.0175
Sluyter JD, Camargo CA Jr, Stewart AW, Waayer D, Lawes CMM, Toop L, Khaw KT, Thom SAM, Hametner B, Wassertheurer S, Parker KH, Hughes AD, Scragg R (2017) Effect of monthly, high-dose, long-term vitamin D supplementation on central blood pressure parameters: a randomized controlled trial substudy. J Am Heart Assoc 6:10. https://doi.org/10.1161/JAHA.117.006802
Somjen D, Weisman Y, Kohen F, Gayer B, Limor R, Sharon O, Jaccard N, Knoll E, Stern N (2005) 25-Hydroxyvitamin D3-1alpha-hydroxylase is expressed in human vascular smooth muscle cells and is upregulated by parathyroid hormone and estrogenic compounds. Circulation 111(13):1666–1671. https://doi.org/10.1161/01.CIR.0000160353.27927.70
Sotiriou P, Kouidi E, Karagiannis A, Koutlianos N, Geleris P, Vassilikos V, Deligiannis A (2019) Arterial adaptations in athletes of dynamic and static sports disciplines—a pilot study. Clin Physiol Funct Imaging 39(3):183–191. https://doi.org/10.1111/cpf.12554
Stephen Hedley J, Phelan D (2017) Athletes and the aorta: normal adaptations and the diagnosis and management of pathology. Curr Treat Options Cardiovasc Med 19(11):88. https://doi.org/10.1007/s11936-017-0586-7
Tarcin O, Yavuz DG, Ozben B, Telli A, Ogunc AV, Yuksel M, Toprak A, Yazici D, Sancak S, Deyneli O, Akalin S (2009) Effect of vitamin D deficiency and replacement on endothelial function in asymptomatic subjects. J Clin Endocrinol Metab 94(10):4023–4030. https://doi.org/10.1210/jc.2008-1212
Thijssen DH, Carter SE, Green DJ (2016) Arterial structure and function in vascular ageing: are you as old as your arteries? J Physiol 594(8):2275–2284. https://doi.org/10.1113/JP270597
Vimaleswaran KS, Cavadino A, Berry DJ, R, Jorde, Dieffenbach AK, Lu C, Alves AC, Heerspink HJ, Tikkanen E, Eriksson J, Wong A, Mangino M, Jablonski KA, Nolte IM, Houston DK, Ahluwalia TS, van der Most PJ, Pasko D, Zgaga L, Thiering E, Vitart V, Fraser RM, Huffman JE, de Boer RA, Schottker B, Saum KU, McCarthy MI, Dupuis J, Herzig KH, Sebert S, Pouta A, Laitinen J, Kleber ME, Navis G, Lorentzon M, Jameson K, Arden N, Cooper JA, Acharya J, Hardy R, Raitakari O, Ripatti S, Billings LK, Lahti J, Osmond C, Penninx BW, Rejnmark L, Lohman KK, Paternoster L, Stolk RP, Hernandez DG, Byberg L, Hagstrom E, Melhus H, Ingelsson E, Mellstrom D, Ljunggren O, Tzoulaki I, McLachlan S, Theodoratou E, Tiesler CM, Jula A, Navarro P, Wright AF, Polasek O, H, International Consortium for Blood P, Cohorts for H, Aging Research in Genomic Epidemiology c, Global Blood Pressure Genetics c, Caroline, Wilson JF, Rudan I, Salomaa V, Heinrich J, Campbell H, Price JF, Karlsson M, Lind L, Michaelsson K, Bandinelli S, Frayling TM, Hartman CA, Sorensen TI, Kritchevsky SB, Langdahl BL, Eriksson JG, Florez JC, Spector TD, Lehtimaki T, Kuh D, Humphries SE, Cooper C, Ohlsson C, Marz W, de Borst MH, Kumari M, Kivimaki M, Wang TJ, Power C, Brenner H, Grimnes G, van der Harst P, Snieder H, Hingorani AD, Pilz S, Whittaker JC, Jarvelin MR, Hypponen E (2014) Association of vitamin D status with arterial blood pressure and hypertension risk: a mendelian randomisation study. Lancet Diabetes Endocrinol 2(9):719–729. https://doi.org/10.1016/S2213-8587(14)70113-5
Vlachopoulos C, Kardara D, Anastasakis A, Baou K, Terentes-Printzios D, Tousoulis D, Stefanadis C (2010) Arterial stiffness and wave reflections in marathon runners. Am J Hypertens 23(9):974–979. https://doi.org/10.1038/ajh.2010.99
Wang TJ (2016) Vitamin D and cardiovascular disease. Annu Rev Med 67:261–272. https://doi.org/10.1146/annurev-med-051214-025146
Wilkinson IB, Franklin SS, Hall IR, Tyrrell S, Cockcroft JR (2001) Pressure amplification explains why pulse pressure is unrelated to risk in young subjects. Hypertension 38(6):1461–1466
Williams B, Lacy PS, Thom SM, Cruickshank K, Stanton A, Collier D, Hughes AD, Thurston H, O'Rourke M, Investigators C, Trial Anglo-Scandinavian Cardiac Outcomes, I, Committee CS, Writing C, (2006) Differential impact of blood pressure-lowering drugs on central aortic pressure and clinical outcomes: principal results of the Conduit Artery Function Evaluation (CAFE) study. Circulation 113(9):1213–1225. https://doi.org/10.1161/CIRCULATIONAHA.105.595496
Yoshikawa T, Kumagai H, Myoenzono K, Tsujimoto T, Tanaka K, Maeda S (2019) Aerobic exercise training normalizes central blood pressure regulation after oral glucose loading in overweight/obese men. Clin Exp Hypertens 41(1):28–35. https://doi.org/10.1080/10641963.2018.1441857
Acknowledgements
The authors thank Elizabeth Martinson, PhD, for editorial assistance.
Author information
Authors and Affiliations
Contributions
PB, AM, CH, OD, HN contributed to the conception and design of the study. PB, AM, LK, SH, ST contributed to the acquisition, analysis, or interpretation of data for the work. PB and AM drafted the manuscript. PB, AM, LK, SH, ST, OD, HN critically revised the manuscript. All gave final approval and agree to be accountable for all aspects of work ensuring integrity and accuracy.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no potential conflicts of interest.
Additional information
Communicated by Keith Phillip George.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Bauer, P., Kraushaar, L., Hölscher, S. et al. Elite athletes as research model: vitamin D insufficiency associates with elevated central blood pressure in professional handball athletes. Eur J Appl Physiol 119, 2265–2274 (2019). https://doi.org/10.1007/s00421-019-04210-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-019-04210-w