Blood pressure, sympathovagal tone, exercise capacity and metabolic status are linked in Turner syndrome
Abstract
Abstract Objectives We studied cardiac autonomic changes in relation to metabolic factors, body composition and 24‐hour ambulatory blood pressure measurements in Turner syndrome patients without known hypertension. Design Cross sectional. Patients Participants were 48 TS women and 24 healthy female controls aged over 18 years. Methods Short‐term power spectral analysis was obtained in supine‐standing‐supine position. Bedside tests included three conventional cardiovascular reflex tests of heart rate response to standing up, heart rate response to deep breathing and blood pressure response to standing up. Mean heart rate during the last 2 minutes of work was used to calculate the maximal aerobic power (VO2max). Results We found a significantly higher mean reciprocal of the heart rate per second (RR) in TS. Testing for interaction between position and status (TS or control), there were highly significant differences between TS and controls in high‐frequency (HF) power, the coefficient of component variation (square root of HF power/mean RR) and low‐frequency (LF): HF ratio, with a dampened decline in vagal activity among TS during standing. Bedside test showed TS had a significantly higher diastolic BP in the supine position compared to controls, and the adaptive rise in BP, when changing to upright position was reduced. VO2max and self‐reported level of physical activity were significantly correlated to systolic ambulatory blood pressure both 24‐hour and night diastolic ambulatory blood pressure. Conclusion Vagal tone and modulation of the sympathovagal balance during alteration in body position are impaired in TS. These changes can be risk factors for cardiovascular disease.
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There is no evidence that exercise capacity is intrinsically lower in TS.
“There is no evidence that exercise capacity is intrinsically lower in TS.499,500”
From Clinical practice guidelines for the care of girls and women with Turner syndrome. (2024) · cites this paper as [500]
Cites
Heart rate variability: Standards of measurement, physiological interpretation, and clinical use
Malik, M., Bigger, J. T., Camm, A. J., Kleiger, R. E., Malliani, A., Moss, A. J., & Schwartz, P. J. (1996) · European Heart Journal · doi:10.1093/oxfordjournals.eurheartj.a014868 · Cited by 15,289 · see citing works
The Value of Cardiovascular Autonomic Function Tests: 10 Years Experience in Diabetes
Ewing, D. J., Martyn, C., Young, R. J., & Clarke, B. F. (1985) · Diabetes Care · doi:10.2337/diacare.8.5.491 · Cited by 1,436 · see citing works
Gravholt, C. H., Andersen, N. H., Conway, G. S., Dekkers, O. M., Geffner, M. E., Klein, K. O., Lin, A. E., Mauras, N., Quigley, C. A., Rubin, K., et al. (2017) · European Journal of Endocrinology · doi:10.1530/eje-17-0430 · Cited by 1,101 · see citing works
Self-citationLa Rovere, M. T., Pinna, G. D., Maestri, R., Mortara, A., Capomolla, S., Febo, O., Ferrari, R., Franchini, M., Gnemmi, M., Opasich, C., et al. (2003) · Circulation · doi:10.1161/01.cir.0000047275.25795.17 · Cited by 917 · see citing works
Accuracy of assessment of cardiac vagal tone by heart rate variability in normal subjects.
Hayano, J., Sakakibara, Y., Yamada, A., Yamada, M., Mukai, S., Fujinami, T., Yokoyama, K., Watanabe, Y., & Takata, K. (1991) · The American Journal of Cardiology · doi:10.1016/0002-9149(91)90445-q · Cited by 746 · see citing works
Maser, R. E., Mitchell, B. D., Vinik, A. I., & Freeman, R. L. (2003) · Diabetes Care · doi:10.2337/diacare.26.6.1895 · Cited by 678 · see citing works
Prevalence, incidence, diagnostic delay, and mortality in Turner syndrome
Stochholm, K., Juul, S., Juel, K., Naeraa, R. W., & Højbjerg Gravholt, C. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0558 · Cited by 652 · see citing works
Aortic Dilatation and Dissection in Turner Syndrome
Matura, L. A., Ho, V. B., Rosing, D. R., & Bondy, C. A. (2007) · Circulation · doi:10.1161/circulationaha.106.685487 · Cited by 364 · see citing works
Mortality in women with Turner syndrome in Great Britain: a national cohort study
Schoemaker, M. J., Swerdlow, A. J., Higgins, C. D., Wright, A. F., & Jacobs, P. A. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1049 · Cited by 360 · see citing works
Coarse-graining spectral analysis: new method for studying heart rate variability
Yamamoto, Y., & Hughson, R. L. (1991) · Journal of Applied Physiology · doi:10.1152/jappl.1991.71.3.1143 · Cited by 357 · see citing works
Zhang, D., Shen, X., & Qi, X. (2015) · Canadian Medical Association Journal · doi:10.1503/cmaj.150535 · Cited by 329 · see citing works
Heart rate variability and its sympatho-vagal modulation
Lombardi, F. (1996) · Cardiovascular Research · doi:10.1016/0008-6363(96)00116-2 · Cited by 246 · see citing works
Heitmann, B. L. (1990) · PubMed · Cited by 218 · see citing works
Cardiovascular Phenotype in Turner Syndrome—Integrating Cardiology, Genetics, and Endocrinology
Mortensen, K. H., Andersen, N. H., & Gravholt, C. H. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1059 · Cited by 217 · see citing works
Self-citationGravholt, C. H., Naeraa, R. W., Nyholm, B., Gerdes, L. U., Christiansen, E., Schmitz, O., & Christiansen, J. S. (1998) · Diabetes Care · doi:10.2337/diacare.21.7.1062 · Cited by 204 · see citing works
Hypertension is a major risk factor for aortic root dilatation in women with Turner's syndrome
Elsheikh, M., Casadei, B., Conway, G. S., & Wass, J. A. H. (2001) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2001.01154.x · Cited by 173 · see citing works
Landin-Wilhelmsen, K., Bryman, I., & Wilhelmsen, L. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.9.7818 · Cited by 113 · see citing works
Mortensen, K. H., Hjerrild, B. E., Stochholm, K., Andersen, N. H., Sørensen, K. E., Lundorf, E., Hørlyck, A., Pedersen, E. M., Christiansen, J. S., & Gravholt, C. H. (2011) · Journal of Cardiovascular Magnetic Resonance · doi:10.1186/1532-429x-13-24 · Cited by 99 · see citing works
Nocturnal hypertension and impaired sympathovagal tone in Turner syndrome
Gravholt, C. H., Hansen, K. W., Erlandsen, M., Ebbehøj, E., & Christiansen, J. S. (2006) · Journal of Hypertension · doi:10.1097/01.hjh.0000200509.17947.0f · Cited by 90 · see citing works
Self-citationPatel, V. N., Pierce, B. R., Bodapati, R. K., Brown, D., Ives, D. G., & Stein, P. K. (2017) · JACC Heart Failure · doi:10.1016/j.jchf.2016.12.015 · Cited by 87 · see citing works
Ostberg, J. E., Thomas, E. L., Hamilton, G., Hosseinzadeh‐Attar, M. J., Bell, J. D., & Conway, G. S. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1939 · Cited by 83 · see citing works
Min, K., Min, J., Paek, D., & Cho, S. (2008) · Pacing and Clinical Electrophysiology · doi:10.1111/j.1540-8159.2008.01045.x · Cited by 72 · see citing works
Aortic dilatation and outcome in women with Turner syndrome
Duijnhouwer, A. L., Bons, L. R., Timmers, H. J. L. M., van Kimmenade, R. R. L., Snoeren, M., Timmermans, J., van den Hoven, A. T., Kempers, M., van Dijk, A. P. J., Fleischer, K., et al. (2019) · Heart · doi:10.1136/heartjnl-2018-313716 · Cited by 60 · see citing works
Christ, M., Seyffart, K., & Wehling, M. (1999) · The Lancet · doi:10.1016/s0140-6736(99)00639-x · Cited by 57 · see citing works
Mortensen, K. H., Erlandsen, M., Andersen, N. H., & Gravholt, C. H. (2013) · Journal of Cardiovascular Magnetic Resonance · doi:10.1186/1532-429x-15-47 · Cited by 54 · see citing works
Self-citationFarag, N. H., Nelesen, R. A., Parry, B. L., Loredo, J. S., Dimsdale, J. E., & Mills, P. J. (2002) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2002.122248 · Cited by 50 · see citing works
Physiological and catecholamine response to sympathetic stimulation in turner syndrome
Zuckerman‐Levin, N., Zinder, O., Greenberg, A., Levin, M., Jacob, G., & Hochberg, Z. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2006.02483.x · Cited by 46 · see citing works
Muscle Fiber Composition and Capillary Density in Turner Syndrome
Gravholt, C. H., Nyholm, B., Saltin, B., Schmitz, O., & Christiansen, J. S. (2001) · Diabetes Care · doi:10.2337/diacare.24.9.1668 · Cited by 39 · see citing works
Self-citationMultimodality cardiac imaging in Turner syndrome
Mortensen, K. H., Gopalan, D., Nørgaard, B. L., Andersen, N. H., & Gravholt, C. H. (2016) · Cardiology in the Young · doi:10.1017/s1047951115002735 · Cited by 30 · see citing works
Self-citationBrun, S., Cleemann, L., Holm, K., Salskov, G., Erlandsen, M., Berglund, A., Andersen, N. H., & Gravholt, C. H. (2019) · Hypertension · doi:10.1161/hypertensionaha.118.11742 · Cited by 24 · see citing works
Self-citationManzella, D., Carbonella, M., Ragno, E., Passariello, N., Grella, R., & Paolisso, G. (2002) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2002.01596.x · Cited by 8 · see citing works
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Clinical practice guidelines for the care of girls and women with Turner syndrome.
Gravholt, C. H., Andersen, N. H., Christin-Maitre, S., Davis, S. M., Duijnhouwer, A., Gawlik, A., Maciel-Guerra, A. T., Gutmark-Little, I., Fleischer, K., Hong, D., et al. (2024) · European Journal of Endocrinology · doi:10.1093/ejendo/lvae050 · Cited by 224 · see citing works
Self-citationThe changing face of Turner syndrome
Gravholt, C. H., Viuff, M., Just, J., Sandahl, K., Brun, S., van der Velden, J., Andersen, N. H., & Skakkebaek, A. (2023) · Endocrine Reviews · doi:10.1210/endrev/bnac016 · Cited by 149 · see citing works
Natural history of hypertension in Turner syndrome during a 12-year pragmatic interventional study
Sandahl, K., Wen, J., Erlandsen, M., Andersen, N. H., & Gravholt, C. H. (2020) · Hypertension · doi:10.1161/hypertensionaha.120.15292 · Cited by 17 · see citing works
Hypertension in Turner syndrome: a review of proposed mechanisms, management and new directions
Jones, L., Blair, J., Hawcutt, D. B., Lip, G. Y. H., & Shantsila, A. (2023) · Journal of Hypertension · doi:10.1097/hjh.0000000000003321 · Cited by 13 · see citing works
- Authors
- Brun, S., Berglund, A., Mortensen, K. H., Hjerrild, B. E., Hansen, K. W., Andersen, N. H., & Gravholt, C. H.
- Affiliations
- Aarhus University Hospital (DK)
- Great Ormond Street Hospital (GB)
- Regionshospitalet Silkeborg (DK)
- Aalborg University Hospital (DK)
- Corresponding author
- Andersen, Niels H.
- ORCID
- Venue
- Clinical Endocrinology
- Publisher
- Wiley
- Published
- 2019-04-12
- Volume
- 91
- Issue
- 1
- Pages
- 148-155
- ISSN
- 0300-0664 (ISSN-L)
- 1365-2265
- OpenAlex
- W2925752872
- Cited by
- 13
- References
- 31
- Citations by year
- 2025: 1 · 2024: 4 · 2022: 4 · 2021: 3 · 2020: 1
- FWCI
- 1.45
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- VBN Forskningsportal (Aalborg Universitet) (submittedVersion)
- Funders
- Lundbeckfonden
- Augustinus Fonden
- Toyota Foundation
- Novo Nordisk Fonden (NNF13OC0003234, NNF15OC0016474)
- Fonden til Lægevidenskabens Fremme
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Clinical Aspects of Sex Determination and Chromosomal Abnormalities
- Health Sciences › Medicine › Surgery › Cardiovascular Syncope and Autonomic Disorders
- Keywords
- Turner syndrome, sympathovagal balance, cardiac autonomic function, vagal tone, ambulatory blood pressure, heart rate variability, exercise capacity, VO2max, physical activity, posture, cardiovascular risk, body composition
- MeSH terms
- Adult, Autonomic Nervous System, Blood Pressure, Cross-Sectional Studies, Female, Heart Rate, Humans, Male, Middle Aged, Turner Syndrome, Biomarkers, Exercise Tolerance
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