Autonomic and Vascular Responses during Reactive Hyperemia in Healthy Individuals and Patients with Sickle Cell Anemia
Abstract
:1. Introduction
2. Methods
2.1. General Description
2.2. Exclusion Criteria
2.3. Physiological Recording
2.4. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Voskaridou, E.; Christoulas, D.; Terpos, E. Sickle-cell disease and the heart: Review of the current literature. Br. J. Haematol. 2012, 157, 664–673. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1365-2141.2012.09143.x (accessed on 25 December 2022). [CrossRef]
- Couque, N.; Girard, D.; Ducrocq, R.; Boizeau, P.; Haouari, Z.; Missud, F.; Holvoet, L.; Ithier, G.; Belloy, M.; Odièvre, M.-H.; et al. Improvement of medical care in a cohort of newborns with sickle-cell disease in North Paris: Impact of national guidelines. Br. J. Haematol. 2016, 173, 927–937. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1111/bjh.14015 (accessed on 25 December 2022). [CrossRef]
- Ware, R.E.; Montalembert, M.; Tshilolo, L.; Abboud, M.R. Sickle cell disease. Lancet 2017, 390, 311–323. [Google Scholar] [CrossRef]
- Cataldo, G.; Rajput, S.; Gupta, K.; Simone, D.A. Sensitization of nociceptive spinal neurons contributes to pain in a transgenic model of sickle cell disease. Pain 2015, 156, 722–730. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4366346/ (accessed on 25 December 2022). [CrossRef] [PubMed] [Green Version]
- Coates, T.D.; Chalacheva, P.; Zeltzer, L.; Khoo, M.C.K. Autonomic nervous system involvement in sickle cell disease. Clin. Hemorheol. Microcirc. 2018, 68, 251–262. Available online: https://content.iospress.com/articles/clinical-hemorheology-and-microcirculation/ch189011 (accessed on 25 December 2022). [CrossRef]
- Belhassen, L.; Pelle, G.; Sediame, S.; Bachir, D.; Carville, C.; Bucherer, C.; Lacombe, C.; Galacteros, F.; Adnot, S. Endothelial dysfunction in patients with sickle cell disease is related to selective impairment of shear stress–mediated vasodilation. Blood 2001, 97, 1584–1589. [Google Scholar] [CrossRef]
- Charlot, K.; Moeckesch, B.; Jumet, S.; Romana, M.; Waltz, X.; Divialle-Doumdo, L.; Hardy-Dessources, M.-D.; Petras, M.; Tressières, B.; Pichon, A.; et al. Physical activity level is not a determinant of autonomic nervous system activity and clinical severity in children/adolescents with sickle cell anemia: A pilot study. Pediatr. Blood Cancer 2015, 62, 1962–1967. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1002/pbc.25604 (accessed on 25 December 2022). [CrossRef]
- Charlot, K.; Hierso, R.; Lemonne, N.; Romana, M.; Tressières, B.; Lalanne-Mistrih, M.L.; Etienne-Julan, M.; Tarer, V.; Ferracci, S.; Hardy-Dessources, M.; et al. Changes in autonomic nervous activity during vaso-occlusive crisis in patients with sickle cell anaemia. Br. J. Haematol. 2017, 177, 484–486. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1111/bjh.14064 (accessed on 25 December 2022). [CrossRef] [Green Version]
- Inamo, J.; Connes, P.; Barthélémy, J.C.; Dan, V.; Coates, T.; Loko, G. Pulmonary hypertension does not affect the autonomic nervous system dysfunction of sickle cell disease. Am. J. Hematol. 2009, 84, 311–312. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1002/ajh.21377 (accessed on 25 December 2022). [CrossRef] [PubMed]
- Pearson, S.R.; Alkon, A.; Treadwell, M.; Wolff, B.; Quirolo, K.; Boyce, W.T. Autonomic reactivity and clinical severity in children with sickle cell disease. Clin. Auton. Res. 2005, 15, 400–407. [Google Scholar] [CrossRef] [PubMed]
- Mestre, J.C.R.; Hernández, A.; Agramonte, O.; Hernández, P. Cardiovascular autonomic dysfunction in sickle cell anemia: A possible risk factor for sudden death? Clin. Auton. Res. 1997, 7, 121–125. [Google Scholar] [CrossRef] [PubMed]
- Alexy, T.; Sangkatumvong, S.; Connes, P.; Pais, E.; Tripette, J.; Barthelemy, J.C.; Fisher, T.; Meiselman, H.; Khoo, M.; Coates, T. Sickle cell disease: Selected aspects of pathophysiology. Clin. Hemorheol. Microcirc. 2010, 44, 155–166. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2910781/ (accessed on 25 December 2022). [CrossRef] [PubMed]
- Sangkatumvong, S.; Coates, T.D.; Khoo, M.C. Abnormal autonomic cardiac response to transient hypoxia in sickle cell anemia. Physiol. Meas. 2008, 29, 655–668. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2956125/ (accessed on 25 December 2022). [CrossRef] [Green Version]
- Nebor, D.; Bowers, A.; Hardy-Dessources, M.D.; Knight-Madden, J.; Romana, M.; Reid, H.; Barthelemy, J.-C.; Cumming, V.; Hue, O.; Elion, J.; et al. Frequency of pain crises in sickle cell anemia and its relationship with the sympatho-vagal balance, blood viscosity and inflammation. Haematologica 2011, 96, 1589–1594. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3208675/ (accessed on 25 December 2022). [CrossRef] [PubMed]
- Serhiyenko, V.A.; Serhiyenko, A.A. Cardiac autonomic neuropathy: Risk factors, diagnosis and treatment. World J. Diabetes 2018, 9, 1–24. Available online: http://www.wjgnet.com/1948-9358/full/v9/i1/1.htm (accessed on 23 February 2022). [CrossRef]
- Spallone, V.; Ziegler, D.; Freeman, R.; Bernardi, L.; Frontoni, S.; Pop-Busui, R.; Stevens, M.; Kempler, P.; Hilsted, J.; Tesfaye, S.; et al. Cardiovascular autonomic neuropathy in diabetes: Clinical impact, assessment, diagnosis, and management. Diabetes Metab. Res. Rev. 2011, 27, 639–653. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1002/dmrr.1239 (accessed on 23 February 2022). [CrossRef] [Green Version]
- Zhang, Z.; Ma, Y.; Fu, L.; Li, L.; Liu, J.; Peng, H.; Jiang, H. Combination of Composite Autonomic Symptom Score 31 and Heart Rate Variability for Diagnosis of Cardiovascular Autonomic Neuropathy in People with Type 2 Diabetes. J. Diabetes Res. 2020, 2020, 5316769. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7648703/ (accessed on 23 February 2022). [CrossRef]
- Bulte, C.S.E.; Keet, S.W.M.; Boer, C.; Bouwman, R.A. Level of agreement between heart rate variability and pulse rate variability in healthy individuals. Eur. J. Anaesthesiol. 2010, 28, 34–3827. Available online: https://journals.lww.com/ejanaesthesiology/Fulltext/2011/01000/Level_of_agreement_between_heart_rate_variability.8.aspx (accessed on 25 December 2022). [CrossRef] [Green Version]
- Gil, E.; Orini, M.; Bailón, R.; Vergara, J.M.; Mainardi, L.; Laguna, P. Photoplethysmography pulse rate variability as a surrogate measurement of heart rate variability during non-stationary conditions. Physiol. Meas. 2010, 31, 1271. [Google Scholar] [CrossRef]
- Lu, G.; Yang, F.; Taylor, J.A.; Stein, J.F. A comparison of photoplethysmography and ECG recording to analyse heart rate variability in healthy subjects. J. Med. Eng. Technol. 2009, 33, 634–641. [Google Scholar] [CrossRef]
- Schäfer, A.; Vagedes, J. How accurate is pulse rate variability as an estimate of heart rate variability?: A review on studies comparing photoplethysmographic technology with an electrocardiogram. Int. J. Cardiol. 2013, 166, 15–29. Available online: https://www.internationaljournalofcardiology.com/article/S0167-5273(12)00326-9/fulltext (accessed on 25 December 2022). [CrossRef] [PubMed]
- Posada-Quintero, H.F.; Delisle-Rodríguez, D.; Cuadra-Sanz, M.B.; de la Vara-Prieto, R.R.F. Evaluation of pulse rate variability obtained by the pulse onsets of the photoplethysmographic signal. Physiol. Meas. 2013, 34, 179. [Google Scholar] [CrossRef]
- Kandhai-Ragunath, J.J.; Jørstad, H.T.; de Man, F.H.; Peters, R.J.; vonBirgelen, C. Approaches for non-invasive assessment of endothelial function: Focus on peripheral arterial tonometry. Neth. Heart J. 2013, 21, 214–218. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3636344/ (accessed on 23 February 2022). [CrossRef] [PubMed] [Green Version]
- Shimada, S.; Todoki, K.; Omori, Y.; Toyama, T.; Matsuo, M.; Wada-Takahashi, S.; Takahashi, S.-S.; Lee, M.-C. Contribution of nitrergic nerve in canine gingival reactive hyperemia. J. Clin. Biochem. Nutr. 2015, 56, 98–104. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4345180/ (accessed on 22 February 2022). [CrossRef] [PubMed] [Green Version]
- Krishnan, A.; Lucassen, E.B.; Hogeman, C.; Blaha, C.; Leuenberger, U.A. Effects of Limb Posture on Reactive Hyperemia. Eur. J. Appl. Physiol. 2011, 111, 1415–1420. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3285391/ (accessed on 22 February 2022). [CrossRef] [Green Version]
- Schreuder, T.H.A.; Green, D.J.; Hopman, M.T.E.; Thijssen, D.H.J. Acute impact of retrograde shear rate on brachial and superficial femoral artery flow-mediated dilation in humans. Physiol. Rep. 2014, 2, e00193. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3967676/ (accessed on 22 February 2022). [CrossRef]
- Short, K.R.; Blackett, P.R.; Gardner, A.W.; Copeland, K.C. Vascular health in children and adolescents: Effects of obesity and diabetes. Vasc. Health Risk Manag. 2009, 5, 973–990. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2788602/ (accessed on 22 February 2022).
- Simón, C.A.P.; Allen, P.D.J. Nuevos modelos conceptual y matemático para el contorno de la onda de volumen de pulso arterial. Rev. Cuba. Investig. Bioméd. 2011, 30, 487–500. Available online: http://scielo.sld.cu/pdf/ibi/v30n4/ibi07411.pdf (accessed on 25 December 2022).
- Malik, M. Heart rate variability: Standards of measurement, physiological interpretation, and clinical use: Task force of the European Society of Cardiology and the North American Society for Pacing and Electrophysiology. Circulation 1996, 93, 1043–1065. [Google Scholar] [CrossRef]
- Torres-Leyva, M.; Carrazana-Escalona, R.; Ormigó-Polo, L.E.; Ricardo-Ferro, B.T.; López-Galán, E.; Ortiz-Alcolea, L.; Sánchez-Hechavarría, M.E. Cardiovascular autonomic response during the Cuban dynamic weight-bearing test. CorSalud 2019, 11, 1–10. Available online: http://www.revcorsalud.sld.cu/index.php/cors/article/view/342/842 (accessed on 25 December 2022).
- Khaleel, M.; Puliyel, M.; Shah, P.; Sunwoo, J.; Kato, R.M.; Chalacheva, P.; Thuptimdang, W.; Detterich, J.; Wood, J.C.; Tsao, J.; et al. Individuals with sickle cell disease have a significantly greater vasoconstriction response to thermal pain than controls and have significant vasoconstriction in response to anticipation of pain. Am. J. Hematol. 2017, 92, 1137–1145. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5880319/ (accessed on 25 December 2022). [CrossRef] [PubMed] [Green Version]
- Hedreville, M.; Charlot, K.; Waltz, X.; Sinnapah, S.; Lemonne, N.; Etienne-Julan, M.; Soter, V.; Hue, O.; Hardy-Dessources, M.-D.; Barthélémy, J.-C.; et al. Acute Moderate Exercise Does Not Further Alter the Autonomic Nervous System Activity in Patients with Sickle Cell Anemia. PLoS ONE 2014, 9, e95563. Available online: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0095563 (accessed on 25 December 2022). [CrossRef] [PubMed]
- López-Galán, E.; Andreu-Heredia, A.; Carrazana-Escalona, R.; Querts-Menéndez, O.; García-Naranjo, J.C.; Lazo-Herrera, L.A.; Muñoz-Bustos, G.A.; Albarrán-Torres, F.A.; Sánchez-Hechavarría, M.E. La activación precoz del reflejo simpático cardiovascular es independiente del tiempo de oclusión durante la hiperemia reactiva. CorSalud 2022, 14, 164–172. Available online: https://revcorsalud.sld.cu/index.php/cors/article/view/754 (accessed on 25 December 2022).
- Boushel, R. Muscle metaboreflex control of the circulation during exercise. Acta Physiol. 2010, 199, 367–383. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1111/j.1748-1716.2010.02133.x (accessed on 25 December 2022). [CrossRef] [PubMed]
- Kaur, J.; Spranger, M.D.; Hammond, R.L.; Krishnan, A.C.; Alvarez, A.; Augustyniak, R.A.; O’Leary, D.S. Muscle metaboreflex activation during dynamic exercise evokes epinephrine release resulting in β2-mediated vasodilation. Am. J. Physiol.-Heart Circ. Physiol. 2015, 308, H524–H529. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4346770/ (accessed on 25 December 2022). [CrossRef] [PubMed] [Green Version]
- Ai, J.; Epstein, P.N.; Gozal, D.; Yang, B.; Wurster, R.; Cheng, Z.J. Morphology and topography of nucleus ambiguus projections to cardiac ganglia in rats and mice. Neuroscience 2007, 149, 845–860. Available online: https://www.sciencedirect.com/science/article/pii/S0306452207009530 (accessed on 25 December 2022). [CrossRef] [PubMed]
- Lin, M.; Ai, J.; Li, L.; Huang, C.; Chapleau, M.W.; Liu, R.; Gozal, D.; Wead, W.B.; Wurster, R.D.; Cheng, Z. Structural remodeling of nucleus ambiguus projections to cardiac ganglia following chronic intermittent hypoxia in C57BL/6J mice. J. Comp. Neurol. 2008, 509, 103–117. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1002/cne.21732 (accessed on 25 December 2022). [CrossRef]
- Ahmed, S.; Siddiqui, A.K.; Sadiq, A.; Shahid, R.K.; Patel, D.V.; Russo, L.A. Echocardiographic abnormalities in sickle cell disease. Am. J. Hematol. 2004, 76, 195–198. Available online: https://onlinelibrary.wiley.com/doi/abs/10.1002/ajh.20118 (accessed on 30 January 2023). [CrossRef]
- Sangkatumvong, S.; Khoo, M.C.K.; Kato, R.; Detterich, J.A.; Bush, A.; Keens, T.G.; Meiselman, H.J.; Wood, J.C.; Coates, T.D. Peripheral Vasoconstriction and Abnormal Parasympathetic Response to Sighs and Transient Hypoxia in Sickle Cell Disease. Am. J. Respir. Crit. Care Med. 2011, 184, 474–481. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3175540/ (accessed on 25 December 2022). [CrossRef] [Green Version]
- Thijssen, D.; Atkinson, C.; Ono, K.; Sprung, S.; Spence, A.; Pugh, C.; Green, D. Sympathetic nervous system activation, arterial shear rate, and flow-mediated dilation. J. Appl. Physiol. 2014, 116, 1300–1307. Available online: https://journals.physiology.org/doi/full/10.1152/japplphysiol.00110.2014?rfr_dat=cr_pub++0pubmed&url_ver=Z39.88-2003&rfr_id=ori%3Arid%3Acrossref.org (accessed on 25 December 2022). [CrossRef] [Green Version]
- Yoshida, M.; Tomiyama, H.; Shiina, K.; Odaira, M.; Yamashina, A. The difference of the influence of autonomic nervous activation caused by reactive hyperemia on two different endothelial function tests. Eur. Heart J. 2013, 34 (Suppl. S1), P1436. [Google Scholar] [CrossRef] [Green Version]
- Selvaraj, N.; Jaryal, A.K.; Santhosh, J.; Anand, S.; Deepak, K.K. Monitoring of reactive hyperemia using photoplethysmographic pulse amplitude and transit time. J. Clin. Monit. Comput. 2009, 23, 315–322. [Google Scholar] [CrossRef]
- Blum, A.; Yeganeh, S.; Peleg, A.; Vigder, F.; Kryuger, K.; Khatib, A.; Khazim, K.; Dauerman, H. Endothelial Function in Patients with Sickle Cell Anemia during and After Sickle Cell Crises. J. Thromb. Thrombolysis 2005, 19, 83–86. [Google Scholar] [CrossRef] [PubMed]
- Ansari, J.; Gavins, F.N.E. Ischemia-Reperfusion Injury in Sickle Cell Disease: From Basics to Therapeutics. Am. J. Pathol. 2019, 189, 706–718. Available online: https://ajp.amjpathol.org/article/S0002-9440(18)30622-9/fulltext (accessed on 25 December 2022). [CrossRef] [PubMed] [Green Version]
AA (n = 18) | SS (n = 24) | p | |
---|---|---|---|
Sex, male/female | 7/11 | 10/14 | 0.856 |
Weight, kg | 71.9 ± 9.27 | 53.25 ± 14.20 | <0.001 |
BMI | 26.47 ± 3.86 | 24.46 ± 7.76 | 0.077 |
Age | 44.5 ± 11.6 | 43.29 ± 11.31 | 0.737 |
Height, cm | 160 ± 0.07 | 150 ± 0.18 | 0.005 |
SBP, mmHg | 121.66 ± 6.18 | 114.58 ± 15.03 | 0.068 |
DBP, mmHg | 81.11 ± 6.76 | 73.75 ± 11.34 | 0.019 |
MBP, mmHg | 94.62 ± 6.06 | 87.36 ± 11.67 | 0.021 |
HR, beats/min | 78.17 ± 4.82 | 75.46 ± 8.46 | 0.311 |
Hb, g/L | - | 76.71 ± 18.46 | - |
Ht | - | 0.24 ± 0.059 | - |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
López-Galán, E.; Vitón-Castillo, A.A.; Carrazana-Escalona, R.; Planas-Rodriguez, M.; Fernández-García, A.A.; Cutiño-Clavel, I.; Pascau-Simon, A.; Connes, P.; Sánchez-Hechavarría, M.E.; Muñoz-Bustos, G.A. Autonomic and Vascular Responses during Reactive Hyperemia in Healthy Individuals and Patients with Sickle Cell Anemia. Medicina 2023, 59, 1141. https://doi.org/10.3390/medicina59061141
López-Galán E, Vitón-Castillo AA, Carrazana-Escalona R, Planas-Rodriguez M, Fernández-García AA, Cutiño-Clavel I, Pascau-Simon A, Connes P, Sánchez-Hechavarría ME, Muñoz-Bustos GA. Autonomic and Vascular Responses during Reactive Hyperemia in Healthy Individuals and Patients with Sickle Cell Anemia. Medicina. 2023; 59(6):1141. https://doi.org/10.3390/medicina59061141
Chicago/Turabian StyleLópez-Galán, Erislandis, Adrián Alejandro Vitón-Castillo, Ramón Carrazana-Escalona, Maylet Planas-Rodriguez, Adolfo Arsenio Fernández-García, Ileana Cutiño-Clavel, Alexander Pascau-Simon, Philippe Connes, Miguel Enrique Sánchez-Hechavarría, and Gustavo Alejandro Muñoz-Bustos. 2023. "Autonomic and Vascular Responses during Reactive Hyperemia in Healthy Individuals and Patients with Sickle Cell Anemia" Medicina 59, no. 6: 1141. https://doi.org/10.3390/medicina59061141