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Exercise Training Improves Baroreflex Sensitivity in Type 2 Diabetes
Open accessAbstract
Type 2 diabetes is a strong risk factor for coronary heart disease and sudden cardiac death. It is associated with reduced baroreflex sensitivity (BRS) and heart rate variability (HRV), which are indicators of increased risk for mortality and morbidity in various patient populations. This study was designed to assess the effects of exercise training on BRS, HRV, and hemodynamics in patients with type 2 diabetes. Subjects (50 men, mean age 53.3 ± 5.1 years) with type 2 diabetes were randomized into either a control group, in which they received conventional treatment only, or an exercise group, in which they received conventional treatment together with heart rate−controlled endurance training twice a week and supervised muscle strength training twice a week for 12 months. Measurements taken at baseline and follow-up included Vo2max, standard time and frequency domain measures of HRV during 24-h recording, and BRS by the phenylephrine method. Cardiac index, systemic vascular resistance index, stroke index, and pulse wave velocity were measured by whole-body impedance cardiography. Significant improvements in Vo2max (exercise group: +2.3 ml · kg−1 · min−1; P < 0.005 vs. control group), muscle strength, and glycemic control (exercise group: HbA1c −0.9%; P < 0.001 vs. control group) were observed in the exercise group. BRS increased in the exercise group, from 6.8 to 8.6 ms/mmHg, and decreased in the control group, from 7.5 to 6.4 ms/mmHg (95% CI for the difference between 0.05 and 4.36 ms/mmHg; P < 0.05). No significant changes in the time or frequency domain measures of HRV or in systemic hemodynamics were observed. We concluded that exercise training improves BRS sensitivity in type 2 diabetes subjects in addition to increasing the exercise capacity and muscle strength and improving glucose control. These beneficial effects in reflectory autonomic regulation and glucose control caused by exercise may be associated with improved prognosis of type 2 diabetes patients.
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“Moderate-intensity aerobic training can improve autonomic function in individuals with and without CV autonomic neuropathy (CAN) ( 112 , 176 , 208 ); however, improvements may only be evident after an acute submaximal exercise ( 78 ).”
From Exercise and Type 2 Diabetes (2010) · cites this paper as [176]
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Journal of Pharmaceutical and Biomedical Sciences
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“In patients without CAN an early stage of functional BRS abnormalities [29] still responsive to life-style intervention – physical training [30] or dietary improvement and weight reduction [31] – has been documented.”
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Evidence-based practice guideline for the treatment for diabetes in Japan 2013
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Resistance exercise training improves heart rate variability in women with fibromyalgia
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BackgroundMethodResultInfluentialModulation of Insulin Sensitivity by Exercise Training: Implications for Cardiovascular Prevention
Iaccarino, G., Franco, D., Sorriento, D., Strisciuglio, T., Barbato, E., & Morisco, C. (2021) · Journal of Cardiovascular Translational Research · doi:10.1007/s12265-020-10057-w · Cited by 106
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A new table for prevention of hypoglycaemia during physical activity in type 1 diabetic patients
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“An intervention study [102] showed that physical exercise has beneficial effects on baroreflex function in patients with type 2 diabetes.”
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FinnDiane Study Group, Rosengård‐Bärlund, M., Bernardi, L., Fagerudd, J. A., Mäntysaari, M., af Björkesten, C.-G., Lindholm, H. J., Forsblom, C. M., Wadén, J., & Groop, P. (2009) · Diabetologia · doi:10.1007/s00125-009-1340-9 · Cited by 83
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BackgroundEffect of combined aerobic and resistance training versus aerobic training on arterial stiffness
Montero, D., Vinet, A., & Roberts, C. K. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.10.147 · Cited by 85
“We obtained and reviewed the full text of the remaining 58 articles and excluded 42 for the following reasons: no randomized controlled trials (n = 27), resistance training alone (n = 8), only peripheral PWV (n = 2) [51,52], unconventional PWV measurement (n = 1) [53], duplicate data (n = 2) [35,36] or data not availa…”
MethodExercise training and cardiac autonomic function in type 2 diabetes mellitus: A systematic review
Bhati, P., Shenoy, S., & Hussain, M. E. (2017) · Diabetes & Metabolic Syndrome Clinical Research & Reviews · doi:10.1016/j.dsx.2017.08.015 · Cited by 83
Exercise training improves arterial baro- and chemoreflex in control and diabetic rats
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Hills, A. P., Shultz, S. P., Soares, M. J., Byrne, N. M., Hunter, G., King, N. A., & Misra, A. (2009) · Obesity Reviews · doi:10.1111/j.1467-789x.2009.00692.x · Cited by 79
“AT interventions and combinations of AT and RT consistently increased VO2peak (29,30,45,48,51), with studies also showing concomitant improvements in insulin resistance (48,51).”
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“In several studies, it has been suggested that exercise training improves cardiac autonomic regulation in healthy subjects and also various patient populations, as in patients with coronary artery disease [18, 19], chronic heart failure [20], chronic obstructive pulmonary disease [21] and diabetes mellitus [22, 23].”
Balducci, S., Zanuso, S., Massarini, M., Corigliano, G., Nicolucci, A., Missori, S., Cavallo, S., Cardelli, P., Alessi, E., Pugliese, G., et al. (2008) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2007.07.006 · Cited by 59
Diabetic cardiovascular autonomic neuropathy: clinical implications
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“Exercise training lowers sympathetic nerve traffic [9], increases baroreflex sensitivity (BRS), and improves glycemic control and insulin sensitivity [8].”
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Moraes-Silva, I. C., Mostarda, C. T., Silva‐Filho, A. C., & Irigoyen, M. C. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-4304-8_5 · Cited by 57
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“Our results agree with those of Loimaala et al. (2003), and in addition, we have taken their study further, by using DM + HTN to assess HRV, and by also examining the effects of exercise on HbA1C levels and blood pressure in these patients.”
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“…of exercise (Gaudet-Savard et al. 2007; Balducci et al. 2004, 2006; Honkola et al. 1997; Ozdirenç et al. 2004; Tokmakidis et al. 2004; Tudor-Locke et al. 2004; Agurs-Collins et al. 1997; Castaneda et al. 2002; Giannopoulou et al. 2005; Ibañez et al. 2005; Loimaala et al. 2003; Cauza et al. 2006).”
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“This is in contrast to a trial in unselected type 2 diabetic patients, in which baroreflex sensitivity, but not heart-rate variability, was shown to improve following exercise training [8].”
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RetractedExercise training does not improve myocardial diastolic tissue velocities in Type 2 diabetes
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Self-citationInspiratory Muscle Training in Type 2 Diabetes with Inspiratory Muscle Weakness
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Cassidy, S., Vaidya, V., Houghton, D., Zalewski, P., Seferović, J. P., Hallsworth, K., MacGowan, G. A., Trenell, M. I., & Jakovljević, D. G. (2018) · Diabetes and Vascular Disease Research · doi:10.1177/1479164118816223 · Cited by 49
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“In spite of the number of works analysing the control of glycaemia through regular physical activity [23, 24, 29, 31, 32, 45–47, 60, 72, 73, 78, 79, 82, 119, 132, 152], very few have focused on the effects of physical activity on the formation of AGEs in diabetic patients and/or during aging [96, 98].”
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“Physical training has been shown to improve both respiratory and cardiovascular control in patients with heart failure [50], and is also known to improve cardiovascular and autonomic nervous function in type 2 diabetes [3, 4].”
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“Type 2 DM patients [93] 12 months (of twice weekly endurance and muscle strength training sessions) May be connected to exercise-induced improvements in endothelial function and endoneurial circulation ≠glycemic control; ≠exercise capacity; ≠muscle strength”
BackgroundCardiovascular Autonomic Nervous System Function and Aerobic Capacity in Type 1 Diabetes
Hägglund, H., Uusitalo, A. L. T., Peltonen, J. E., Koponen, A. S., Aho, J. M., Tiinanen, S., Seppänen, T., Tulppo, M. P., & Tikkanen, H. O. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00356 · Cited by 35
“In addition, exercise training has also been related to improved cardiovascular ANS function in patients who already www.frontiersin.org September 2012 | Volume 3 | Article 356 | 1 have caught type 2 diabetes (Loimaala et al., 2003; Pagkalos et al., 2008).”
BackgroundCardiorespiratory Fitness and Cardiac Autonomic Function in Diabetes
Röhling, M., Strom, A., Bönhof, G. J., Roden, M., & Ziegler, D. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0959-z · Cited by 34
Heart-Rate Profile during Exercise as a Predictor of Sudden Death
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“antioxidant and anti-inflammatory status (Teixeira de Lemos, Oliveira, Pascoa Pinheiro, & Reis, 2012), reduced hyperglycemia (Duclos, Virally, & Dejager, 2011), increased exercise capacity and muscle strength, as well as improved baroreflex sensitivity (Loimaala et al., 2003).”
BackgroundPark, J., & Lee, Y.-E. (2015) · Journal of Physical Therapy Science · doi:10.1589/jpts.27.3559 · Cited by 33
Li, X., Yu, S., Chen, H., Lu, C. H., Zhang, K., & Li, F. (2014) · Journal of Diabetes Investigation · doi:10.1111/jdi.12270 · Cited by 31
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“While EM may have some contraindications (e.g. for patients with AMI Killip III and IV), it may also be synergistic with other BRS-enhancing interventions, such as beta-blockers (Malfatto et al., 1998) as well as other accepted treatments.”
BackgroundInfluentialBaroreflex analysis in diabetes mellitus: linear and nonlinear approaches
Javorka, M., Lazarova, Z., Tonhajzerová, I., Turianiková, Z., Honzíková, N., Fišer, B., Javorka, K., & Baumert, M. (2010) · Medical & Biological Engineering & Computing · doi:10.1007/s11517-010-0707-x · Cited by 31
“to-beat blood pressure measurement the assessment of reflectory cardiovascular control by means of BRS testing has become feasible [19, 34].”
BackgroundMethodExercise might improve cardiovascular autonomic regulation in adolescents with type 1 diabetes
Lucini, D., Zuccotti, G., Scaramuzza, A. E., Malacarne, M., Gervasi, F., & Pagani, M. (2012) · Acta Diabetologica · doi:10.1007/s00592-012-0416-z · Cited by 30
“Although there are relatively few studies on this topic, exercise training improves baroreflex gain [22, 33, 34] and might also ameliorate vascular regulation [35] at various levels, from sympathetic control to oxidative stress.”
BackgroundKozàkovà, M., Morizzo, C., Bianchi, C., Filippi, M. D., Miccoli, R., Paterni, M., Bello, V. D., & Palombo, C. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-2028 · Cited by 29
“A higher HR in T2DM patients with inadequate glycemic control as well as the independent association between HR and carotid stiffness (Table 2) might reflect changes in baroreflex sensitivity that have been shown to be related to both T2DM and arterial stiffness (19, 20).”
BackgroundKanaley, J. A., Goulopoulou, S., Franklin, R. M., Baynard, T., Holmstrup, M. E., Carhart, R. L., Weinstock, R. S., & Fernhall, B. (2009) · International Journal of Obesity · doi:10.1038/ijo.2009.145 · Cited by 29
Al-Mhanna, S. B., Alghannam, A. F., Alkhamees, N. H., Sheeha, B. H. B., Omar, N., Albalawi, H., Gülü, M., Canlı, U., Afolabi, H. A., Abubakar, B. D., et al. (2025) · PeerJ · doi:10.7717/peerj.19537 · Cited by 27
Treadmill gait training improves baroreflex sensitivity in Parkinson’s disease
Ganesan, M., Pal, P. K., Gupta, A., & Sathyaprabha, T. N. (2014) · Clinical Autonomic Research · doi:10.1007/s10286-014-0236-z · Cited by 27
Piras, A., Persiani, M., Damiani, N., Perazzolo, M., & Raffi, M. (2014) · European Journal of Applied Physiology · doi:10.1007/s00421-014-3057-9 · Cited by 28
“These changes in blood pressure may be associated with changes in its autonomic regulative function as both blood pressure and cardiovascular autonomic function can be improved with exercise training (Pagani et al. 1988; Loimaala et al. 2003; Timmers et al. 2004; Shin et al. 2014).”
Exercise frequency and arterial compliance in non-diabetic and type 1 diabetic individuals
Mason, N. J., Jenkins, A. J., Best, J. D., & Rowley, K. (2006) · European Journal of Cardiovascular Prevention & Rehabilitation · doi:10.1097/01.hjr.0000216546.07432.b2 · Cited by 27
Manjunath, N., Vinutha, H., & Raghavendra, B. (2015) · Indian Journal of Endocrinology and Metabolism · doi:10.4103/2230-8210.163194 · Cited by 26
“In a previous study, exercise for 12 months did not show any change in the time domain as well as frequency domain measures in 24 h HRV recording.[21] In contrast, in healthy individuals, increase in HRV and vagal tone has been observed following yoga practice in several studies.”
BackgroundCseh, D., Climie, R. E., Offredo, L., Guibout, C., Thomas, F., Zanoli, L., Danchin, N., Sharman, J. E., Laurent, S., Jouven, X., et al. (2020) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.120.314102 · Cited by 25
Bönhof, G. J., Herder, C., & Ziegler, D. (2021) · Current Diabetes Reviews · doi:10.2174/1573399817666210412123740 · Cited by 25
Pfeifer, L. O., Nardi, A. T. D., da Silva, L. X. N., Botton, C. E., do Nascimento, D. M., Teodoro, J. L., Schaan, B. D., & Umpierre, D. (2022) · Sports Medicine - Open · doi:10.1186/s40798-022-00422-1 · Cited by 31
“[51] Combined 2 65 to 75% VO2max; 70 to 80% 1RM ≥ 30 52 Verity et al.”
BackgroundInfluentialDeep breathing improves blunted baroreflex sensitivity even after 30 years of type 1 diabetes
the FinnDiane Study Group, Rosengård‐Bärlund, M., Bernardi, L., Holmqvist, J., Debarbieri, G., Mäntysaari, M., af Björkesten, C.-G., Forsblom, C. M., & Groop, P. (2011) · Diabetologia · doi:10.1007/s00125-011-2164-y · Cited by 25
“Early autonomic abnormalities also seem to be favourably influenced by physical exercise in type 2 diabetes [17, 18], again suggesting that these abnormalities can be partly corrected in diabetes.”
BackgroundPrescribing Exercise for Individuals with Type 2 Diabetes: Recommendations and Precautions
Colberg, S. R., & Sigal, R. J. (2011) · The Physician and Sportsmedicine · doi:10.3810/psm.2011.05.1909 · Cited by 25
Kang, S., Woo, J., Shin, K. O., Kim, D., Lee, H., Kim, Y. J., & Yeo, N. H. (2009) · Europe PMC (PubMed Central) · Cited by 24
Subramanian, S. K., Sharma, V. K., Arunachalam, V., Rajendran, R., & Archana Gaur, T. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.01043 · Cited by 40
Mild‐to‐moderate intensity exercise improves cardiac autonomic drive in type 2 diabetes
Goit, R. K., Paudel, B. H., Khadka, R., Roy, R. K., & Shrewastwa, M. K. (2014) · Journal of Diabetes Investigation · doi:10.1111/jdi.12238 · Cited by 23
“However, Loimaala et al.25 reported no differences in the time domain or frequency domain HRV measures even after 12 months of training.”
BackgroundHamasaki, H. (2023) · Healthcare · doi:10.3390/healthcare11192668 · Cited by 24
“(2003) [23] Finland Randomized, controlled, parallel-group trial 12 months 50 male patients with T2D, 1 dropout Intervention group: Age: 53.”
BackgroundInfluentialEffect of supervised integrated exercise on heart rate variability in type 2 diabetes mellitus.
Bhagyalakshmi, K., Haleagrahara, N., Anupama, B., Ramesh, B., Prabha, A., Murthy, N., & Avabratha, S. (2007) · PubMed · Cited by 23
Adam, M., Imboden, M., Schaffner, E., Boes, E., Kronenberg, F., Pons, M., Bettschart, R. W., Barthélemy, J., Schindler, C., & Probst-Hensch, N. M. (2016) · International Journal of Cardiology · doi:10.1016/j.ijcard.2016.11.049 · Cited by 23
Colberg, S. R., & Vinik, A. I. (2014) · The Physician and Sportsmedicine · doi:10.3810/psm.2014.02.2043 · Cited by 23
Sanches, Í. C., Conti, F. F., Bernardes, N., Brito, J. D. O., Galdini, E. G., Cavaglieri, C. R., Irigoyen, M. C., & Angelis, K. D. (2015) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00883.2014 · Cited by 25
“In this context, several clinical and experimental studies have demonstrated the positive role of exercise training on the baroreflex sensitivity in patients with diabetes (20), postmenopausal women (16), or ovariectomized diabetic female rats (33), as observed after aerobic or combined exercise training in the presen…”
BackgroundImpaired myocardial function in newly onset Type 2 diabetes associates with arterial stiffness☆
Loimaala, A., Groundstroem, K., Majahalme, S. K., Nenonen, A., & VUORI, I. M. (2005) · European Journal of Echocardiography · doi:10.1016/j.euje.2005.07.001 · Cited by 21
Self-citationMostarda, C. T., Rodrigues, B., de Moraes, O. A., Moraes-Silva, I. C., de Arruda, P. P. R. F., Cardoso, R., Scapini, K. B., dos Santos, F., Angelis, K. D., & Irigoyen, M. C. (2014) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2013.12.005 · Cited by 21
“Cardiac autonomic neuropathy in diabetic patients has also been associated with cardiac arrhythmias and sudden death (De Angelis, Irigoyen, & Morris, 2009; Loimaala et al., 2003; Vinik, Erbas, & Casellini, 2013).”
BackgroundCardiopulmonary Rehabilitation Enhances Heart Rate Recovery in Patients With COPD
Georgiopoulou, V. V., Dimopoulos, S. K., Sakellariou, D., Papazachou, O., Gerovasili, V., Tasoulis, A., Agapitou, V., Vogiatzis, I., Roussos, C., & Nanas, S. (2012) · Respiratory Care · doi:10.4187/respcare.01485 · Cited by 20
Colberg, S. R., Sigal, R. J., Fernhall, B., Regensteiner, J. G., Blissmer, B. J., Rubin, R. R., Chasan‐Taber, L., Albright, A. L., & Braun, B. (2010) · Cited by 20
Efeitos fisiológicos do treinamento físico em pacientes portadores de diabetes tipo 1
Angelis, K. D., da Pureza, D. Y., Flores, L. J. F., Rodrigues, B., Melo, K., Schaan, B. D., & Irigoyen, M. C. (2006) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/s0004-27302006000600005 · Cited by 19
Esposito, P. B., Mereu, R., Barbieri, G. D., Rampino, T., Toro, A. D., Groop, P., Canton, A. D., & Bernardi, L. (2015) · Acta Diabetologica · doi:10.1007/s00592-015-0765-5 · Cited by 20
Lehnen, A. M. (2013) · Journal of Diabetes & Metabolism · doi:10.4172/2155-6156.s10-002 · Cited by 19
“Aerobic [16] and/or resistance exercise training [17] are known to improve insulin sensitivity and have other beneficial effects on blood pressure, heart rate, heart rate variability, and chemoreceptor and arterial baroreceptor reflex sensitivity [18,19].”
BackgroundSchneider, V. M., Frank, P., Fuchs, S. C. P. C., & Ferrari, R. (2021) · Experimental Gerontology · doi:10.1016/j.exger.2021.111549 · Cited by 17
Metadata
- Authors
- Loimaala, A., Huikuri, H. V., Kööbi, T., Rinne, M., Nenonen, A., & Vuori, I.
- Affiliations
- South Karelia Central Hospital (FI)
- Oulu University Hospital (FI)
- Tampere University Hospital, Department of Clinical Physiology, Tampere, Finland
- Urho Kaleva Kekkonen Institute (FI)
- Tampere University Hospital (FI)
- Venue
- Diabetes
- Publisher
- American Diabetes Association
- Published
- 2003-07-01
- Volume
- 52
- Issue
- 7
- Pages
- 1837-1842
- ISSN
- 0012-1797 (ISSN-L)
- 1939-327X
- OpenAlex
- W2140739356
- Cited by
- 207
- References
- 36
- Citations by year
- 2026: 6 · 2025: 4 · 2024: 7 · 2023: 8 · 2022: 6 · 2021: 8 · 2020: 5 · 2019: 7 · 2018: 6 · 2017: 7 · 2016: 6 · 2015: 9 · 2014: 18 · 2013: 8 · 2012: 15
- FWCI
- 4.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Diabetes (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Tays
- Pirkanmaan Rahasto
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Physiology (medical) › Cardiovascular and exercise physiology
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Physical Activity and Health
- Keywords
- type 2 diabetes, baroreflex sensitivity, exercise training, heart rate variability, endurance training, resistance training, autonomic regulation, glycemic control, VO2max, hemodynamics, pulse wave velocity, sudden cardiac death risk
- MeSH terms
- Blood Pressure, Diabetes Mellitus, Type 2, Diet, Diabetic, Heart Rate, Hemodynamics, Glycated Hemoglobin, Humans, Hypoglycemic Agents, Male, Middle Aged, Oxygen Consumption, Physical Fitness, Vascular Resistance, Exercise, Body Mass Index, Baroreflex
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