Autonomic and respiratory consequences of altered chemoreflex function: clinical and therapeutic implications in cardiovascular diseases.


Journal

European journal of heart failure
ISSN: 1879-0844
Titre abrégé: Eur J Heart Fail
Pays: England
ID NLM: 100887595

Informations de publication

Date de publication:
May 2023
Historique:
revised: 10 02 2023
received: 14 09 2022
accepted: 26 02 2023
medline: 19 6 2023
pubmed: 13 3 2023
entrez: 12 3 2023
Statut: ppublish

Résumé

The importance of chemoreflex function for cardiovascular health is increasingly recognized in clinical practice. The physiological function of the chemoreflex is to constantly adjust ventilation and circulatory control to match respiratory gases to metabolism. This is achieved in a highly integrated fashion with the baroreflex and the ergoreflex. The functionality of chemoreceptors is altered in cardiovascular diseases, causing unstable ventilation and apnoeas and promoting sympathovagal imbalance, and it is associated with arrhythmias and fatal cardiorespiratory events. In the last few years, opportunities to desensitize hyperactive chemoreceptors have emerged as potential options for treatment of hypertension and heart failure. This review summarizes up to date evidence of chemoreflex physiology/pathophysiology, highlighting the clinical significance of chemoreflex dysfunction, and lists the latest proof of concept studies based on modulation of the chemoreflex as a novel target in cardiovascular diseases.

Identifiants

pubmed: 36907827
doi: 10.1002/ejhf.2819
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

642-656

Informations de copyright

© 2023 European Society of Cardiology.

Références

Guyenet PG. Regulation of breathing and autonomic outflows by chemoreceptors. Compr Physiol. 2014;4:1511-62.
Javaheri S. Determinants of carbon dioxide tension. In: Gennari FJ, Adrogue HJ, Gall JH, Madias NE, editors. Acid-base disorders and their treatment. 1st ed. Boca Raton: Taylor and Francis; 2006. p. 47-77.
Toledo C, Andrade DC, Lucero C, Schultz HD, Marcus N, Retamal M, et al. Contribution of peripheral and central chemoreceptors to sympatho-excitation in heart failure. J Physiol. 2017;595:43-51.
Sainju RK, Dragon DN, Winnike HB, Nashelsky MB, Granner MA, Gehlbach BK, et al. Ventilatory response to CO2 in patients with epilepsy. Epilepsia. 2019;60:508-17.
Giannoni A, Mirizzi G, Aimo A, Emdin M, Passino C. Peripheral reflex feedbacks in chronic heart failure: is it time for a direct treatment? World J Cardiol. 2015;7:824-8.
Iturriaga R. Carotid body ablation: a new target to address central autonomic dysfunction. Curr Hypertens Rep. 2018;20:53.
Nabbout R, Mistry A, Zuberi S, Villeneuve N, Gil-Nagel A, Sanchez-Carpintero R, et al. Fenfluramine for treatment-resistant seizures in patients with dravet syndrome receiving stiripentol-inclusive regimens: a randomized clinical trial. JAMA Neurol. 2020;77:300-8.
Heymans C, Bouckaert J. Sinus caroticus and respiratory reflexes: I. Cerebral blood flow and respiration. Adrenaline apnoea. J Physiol. 1930;69:254-66.
Kumar P, Bin-Jaliah I. Adequate stimuli of the carotid body: more than an oxygen sensor? Respir Physiol Neurobiol. 2007;157:12-21.
Nattie E, Julius H, Comroe J. distinguished lecture: central chemoreception: then. . . and now. J Appl Physiol. 1985;2011:1-8.
Zera T, Moraes DJA, Da Silva MP, Fisher JP, Paton JFR. The logic of carotid body connectivity to the brain. Physiology. 2019;34:264-82.
Edelman NH, Epstein PE, Lahiri S, Cherniack NS. Ventilatory responses to transient hypoxia and hypercapnia in man. Respir Physiol. 1973;17:302-14.
Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev. 1994;74:829-98.
Blain GM, Smith CA, Henderson KS, Dempsey JA. Contribution of the carotid body chemoreceptors to eupneic ventilation in the intact, unanesthetized dog. J Appl Physiol (1985). 2009;106:1564-73.
Hodges MR, Forster HV. Respiratory neuroplasticity following carotid body denervation: central and peripheral adaptations. Neural Regen Res. 2012;7:1073-9.
Keir D, Duffin J, Millar P, Floras J. Simultaneous assessment of central and peripheral chemoreflex regulation of muscle sympathetic nerve activity and ventilation in healthy young men. J Physiol. 2019;597:3281-96.
Sayegh ALC, Fan JL, Vianna LC, Dawes M, Paton JFR, Fisher JP. Sex differences in the sympathetic neurocirculatory responses to chemoreflex activation. J Physiol. 2022;600:2669-89.
Gentile F, Borrelli C, Sciarrone P, Buoncristiani F, Spiesshoefer J, Bramanti F, et al. Central apneas are more detrimental in female than in male patients with heart failure. J Am Heart Assoc. 2022;11:e024103.
Cui Z, Fisher JA, Duffin J. Central-peripheral respiratory chemoreflex interaction in humans. Respir Physiol Neurobiol. 2012;180:126-31.
Heistad D, Abboud FM, Mark AL, Schmid PG. Effect of baroreceptor activity on ventilatory response to chemoreceptor stimulation. J Appl Physiol. 1975;39:411-6.
Mancia G. Influence of carotid baroreceptors on vascular responses to carotid chemoreceptor stimulation in the dog. Circ Res. 1975;36:270-6.
Somers VK, Mark AL, Abboud FM. Interaction of baroreceptor and chemoreceptor reflex control of sympathetic nerve activity in normal humans. J Clin Invest. 1991;87:1953-7.
Halliwill JR, Morgan BJ, Charkoudian N. Peripheral chemoreflex and baroreflex interactions in cardiovascular regulation in humans. J Physiol. 2003;552:295-302.
Schmidt H, Francis DP, Rauchhaus M, Werdan K, Piepoli MF. Chemo- and ergoreflexes in health, disease and ageing. Int J Cardiol. 2005;98:369-78.
Chua TP, Ponikowski P, Harrington D, Anker SD, Webb-Peploe K, Clark AL, et al. Clinical correlates and prognostic significance of the ventilatory response to exercise in chronic heart failure. J Am Coll Cardiol. 1997;29:1585-90.
Lykidis CK, Kumar P, Balanos GM. The respiratory responses to the combined activation of the muscle metaboreflex and the ventilatory chemoreflex. Adv Exp Med Biol. 2009;648:281-7.
Torres-Torrelo H, Ortega-Sáenz P, Gao L, López-Barneo J. Lactate sensing mechanisms in arterial chemoreceptor cells. Nat Commun. 2021;12:4166.
Trzebski A, Tafil M, Zoltowski M, Przybylski J. Increased sensitivity of the arterial chemoreceptor drive in young men with mild hypertension. Cardiovasc Res. 1982;16:163-72.
Siński M, Lewandowski J, Przybylski J, Bidiuk J, Abramczyk P, Ciarka A, et al. Tonic activity of carotid body chemoreceptors contributes to the increased sympathetic drive in essential hypertension. Hypertens Res. 2012;35:487-91.
Floras JS. Hypertension and sleep apnea. Can J Cardiol. 2015;31:889-97.
Fukuda Y, Sato A, Trzebski A. Carotid chemoreceptor discharge responses to hypoxia and hypercapnia in normotensive and spontaneously hypertensive rats. J Auton Nerv Syst. 1987;19:1-11.
Del Rio R, Moya EA, Iturriaga R. Carotid body and cardiorespiratory alterations in intermittent hypoxia: the oxidative link. Eur Respir J. 2010;36:143-50.
Taylor KS, Millar PJ, Murai H, Haruki N, Kimmerly DS, Bradley TD, et al. Cortical autonomic network gray matter and sympathetic nerve activity in obstructive sleep apnea. Sleep. 2018;41:zsx208.
Giannoni A, Emdin M, Bramanti F, Iudice G, Francis DP, Barsotti A, et al. Combined increased chemosensitivity to hypoxia and hypercapnia as a prognosticator in heart failure. J Am Coll Cardiol. 2009;53:1975-80.
Chua TP, Ponikowski P, Webb-Peploe K, Harrington D, Anker SD, Piepoli M, et al. Clinical characteristics of chronic heart failure patients with an augmented peripheral chemoreflex. Eur Heart J. 1997;18:480-6.
Javaheri S. A mechanism of central sleep apnea in patients with heart failure. N Engl J Med. 1999;341:949-54.
Niewinski P, Engelman ZJ, Fudim M, Tubek S, Paleczny B, Jankowska EA, et al. Clinical predictors and hemodynamic consequences of elevated peripheral chemosensitivity in optimally treated men with chronic systolic heart failure. J Card Fail. 2013;19:408-15.
Giannoni A, Emdin M, Passino C. Cheyne-Stokes respiration, chemoreflex, and ticagrelor-related dyspnea. N Engl J Med. 2016;375:1004-6.
Giannoni A, Borrelli C, Gentile F, Mirizzi G, Coceani M, Paradossi U, et al. Central apnoeas and ticagrelor-related dyspnoea in patients with acute coronary syndrome. Eur Heart J Cardiovasc Pharmacother. 2021;7:180-8.
Plum F, Brown HW. Neurogenic factors in periodic breathing. Trans Am Neurol Assoc. 1961;86:39-42.
Seiler A, Camilo M, Korostovtseva L, Haynes AG, Brill A-K, Horvath T, et al. Prevalence of sleep-disordered breathing after stroke and TIA: a meta-analysis. Neurology. 2019;92:e648-54.
Paton JY, Swaminathan S, Sargent CW, Keens TG. Hypoxic and hypercapnic ventilatory responses in awake children with congenital central hypoventilation syndrome. Am Rev Respir Dis. 1989;140:368-72.
Lin Z, Chen ML, Keens TG, Ward SLD, Khoo MCK. Noninvasive assessment of cardiovascular autonomic control in congenital central hypoventilation syndrome. Conf Proc IEEE Eng Med Biol Soc. 2004;2004:3870-3.
Javaheri S, Colangelo G, Lacey W, Gartside PS. Chronic hypercapnia in obstructive sleep apnea-hypopnea syndrome. Sleep. 1994;17:416-23.
Li A, Roy SH, Nattie EE. An augmented CO2 chemoreflex and overactive orexin system are linked with hypertension in young and adult spontaneously hypertensive rats. J Physiol. 2016;594:4967-80.
Guyenet PG, Stornetta RL, Holloway BB, Souza GMPR, Abbott SBG. Rostral ventrolateral medulla and hypertension. Hypertension. 2018;72:559-66.
Pijacka W, McBryde FD, Marvar PJ, Lincevicius GS, Abdala AP, Woodward L, et al. Carotid sinus denervation ameliorates renovascular hypertension in adult Wistar rats. J Physiol. 2016;594:6255-66.
Narkiewicz K, Ratcliffe LEK, Hart EC, Briant LJB, Chrostowska M, Wolf J, et al. Unilateral carotid body resection in resistant hypertension: a safety and feasibility trial. JACC Basic Transl Sci. 2016;1:313-24.
Pijacka W, Moraes DJA, Ratcliffe LEK, Nightingale AK, Hart EC, Da Silva MP, et al. Purinergic receptors in the carotid body as a new drug target for controlling hypertension. Nat Med. 2016;22:1151-9.
Jackson KL, Dampney BW, Moretti J-L, Stevenson ER, Davern PJ, Carrive P, et al. Contribution of orexin to the neurogenic hypertension in BPH/2J mice. Hypertension. 2016;67:959-69.
Sun H, Palcza J, Card D, Gipson A, Rosenberg R, Kryger M, et al. Effects of suvorexant, an orexin receptor antagonist, on respiration during sleep in patients with obstructive sleep apnea. J Clin Sleep Med. 2016;12:9-17.
White DP. Pharmacologic approaches to the treatment of obstructive sleep apnea. Sleep Med Clin. 2016;11:203-12.
Tan ZY, Lu Y, Whiteis CA, Simms AE, Paton JFR, Chapleau MW, et al. Chemoreceptor hypersensitivity, sympathetic excitation, and overexpression of ASIC and TASK channels before the onset of hypertension in SHR. Circ Res. 2010;106:536-45.
Conde SV, Monteiro EC, Sacramento JF. Purines and carotid body: new roles in pathological conditions. Front Pharmacol. 2017;8:913.
Javaheri S, Barbe F, Campos-Rodriguez F, Dempsey JA, Khayat R, Javaheri S, et al. Sleep apnea: types, mechanisms, and clinical cardiovascular consequences. J Am Coll Cardiol. 2017;69:841-58.
Javaheri S, Gay PC. To die, to sleep - to sleep, perchance to dream… without hypertension: dreams of the visionary christian guilleminault revisited. J Clin Sleep Med. 2019;15:1189-90.
Farré N, Farré R, Gozal D. Sleep apnea morbidity: a consequence of microbial-immune cross-talk? Chest. 2018;154:754-9.
Larkin EK, Patel SR, Goodloe RJ, Li Y, Zhu X, Gray-McGuire C, et al. A candidate gene study of obstructive sleep apnea in European Americans and African Americans. Am J Respir Crit Care Med. 2010;182:947-53.
Giannoni A, Gentile F, Buoncristiani F, Borrelli C, Sciarrone P, Spiesshoefer J, et al. Chemoreflex and baroreflex sensitivity hold a strong prognostic value in chronic heart failure. JACC Heart Fail. 2022;10:662-76.
Ponikowski P, Chua TP, Anker SD, Francis DP, Doehner W, Banasiak W, et al. Peripheral chemoreceptor hypersensitivity: an ominous sign in patients with chronic heart failure. Circulation. 2001;104:544-9.
Marcus NJ, Del Rio R, Schultz EP, Xia XH, Schultz HD. Carotid body denervation improves autonomic and cardiac function and attenuates disordered breathing in congestive heart failure. J Physiol. 2014;592:391-408.
Del Rio R, Marcus NJ, Schultz HD. Carotid chemoreceptor ablation improves survival in heart failure: rescuing autonomic control of cardiorespiratory function. J Am Coll Cardiol. 2013;62:2422-30.
Niewinski P, Janczak D, Rucinski A, Tubek S, Engelman ZJ, Piesiak P, et al. Carotid body resection for sympathetic modulation in systolic heart failure: results from first-in-man study. Eur J Heart Fail. 2017;19:391-400.
Lorenzi-Filho G, Rankin F, Bies I, Douglas Bradley T. Effects of inhaled carbon dioxide and oxygen on cheyne-stokes respiration in patients with heart failure. Am J Respir Crit Care Med. 1999;159:1490-8.
Borrelli C, Aimo A, Mirizzi G, Passino C, Vergaro G, Emdin M, et al. How to take arms against central apneas in heart failure. Expert Rev Cardiovasc Ther. 2017;15:743-55.
Giannoni A, Baruah R, Willson K, Mebrate Y, Mayet J, Emdin M, et al. Real-time dynamic carbon dioxide administration: a novel treatment strategy for stabilization of periodic breathing with potential application to central sleep apnea. J Am Coll Cardiol. 2010;56:1832-7.
Sacramento JF, Gonzalez C, Gonzalez-Martin MC, Conde SV. Adenosine receptor blockade by caffeine inhibits carotid sinus nerve chemosensory activity in chronic intermittent hypoxic animals. Adv Exp Med Biol. 2015;860:133-7.
Tubek S, Niewinski P, Reczuch K, Janczak D, Rucinski A, Paleczny B, et al. Effects of selective carotid body stimulation with adenosine in conscious humans. J Physiol. 2016;594:6225-40.
Notarius CF, Atchison DJ, Rongen GA, Floras JS. Effect of adenosine receptor blockade with caffeine on sympathetic response to handgrip exercise in heart failure. Am J Physiol Heart Circ Physiol. 2001;281:H1312-8.
Zurek M, Corrà U, Piepoli MF, Binder RK, Saner H, Schmid JP. Exercise training reverses exertional oscillatory ventilation in heart failure patients. Eur Respir J. 2012;40:1238-44.
Spicuzza L, Gabutti A, Porta C, Montano N, Bernardi L. Yoga and chemoreflex response to hypoxia and hypercapnia. Lancet. 2000;356:1495-6.
Taylor NC, Li A, Nattie EE. Medullary serotonergic neurones modulate the ventilatory response to hypercapnia, but not hypoxia in conscious rats. J Physiol. 2005;566:543-57.
Messier ML, Li A, Nattie EE. Inhibition of medullary raphé serotonergic neurons has age-dependent effects on the CO2 response in newborn piglets. J Appl Physiol. 2004;96:1909-19.
Yamauchi M, Dostal J, Kimura H, Strohl KP. Effects of buspirone on posthypoxic ventilatory behavior in the C57BL/6J and A/J mouse strains. J Appl Physiol. 2008;105:518-26.
Giannoni A, Borrelli C, Mirizzi G, Richerson GB, Emdin M, Passino C. Benefit of buspirone on chemoreflex and central apnoeas in heart failure: a randomized controlled crossover trial. Eur J Heart Fail. 2021;23:312-20.
Marcus NJ, Del Rio R, Ding Y, Schultz HD. KLF2 mediates enhanced chemoreflex sensitivity, disordered breathing and autonomic dysregulation in heart failure. J Physiol. 2018;596:3171-85.
Schultz HD, Marcus NJ, Del Rio R. Role of the carotid body chemoreflex in the pathophysiology of heart failure: a perspective from animal studies. Adv Exp Med Biol. 2015;860:167-85.
Schultz HD, Li YL, Ding Y. Arterial chemoreceptors and sympathetic nerve activity: implications for hypertension and heart failure. Hypertension. 2007;50:6-13.
Brown CV, Boulet LM, Vermeulen TD, Sands SA, Wilson RJA, Ayas NT, et al. Angiotensin II-type I receptor antagonism does not influence the chemoreceptor reflex or hypoxia-induced central sleep apnea in men. Front Neurosci. 2020;14:382.
Rongen GA, Senn BL, Ando S, Notarius CF, Stone JA, Floras JS. Comparison of hemodynamic and sympathoneural responses to adenosine and lower body negative pressure in man. Can J Physiol Pharmacol. 1997;75:128-34.
Javaheri S, Parker TJ, Liming JD, Corbett WS, Nishiyama H, Wexler L, et al. Sleep apnea in 81 ambulatory male patients with stable heart failure. Types and their prevalences, consequences, and presentations. Circulation. 1998;97:2154-9.
Dempsey JA, Smith CA, Blain GM, Xie A, Gong Y, Teodorescu M. Role of central/peripheral chemoreceptors and their interdependence in the pathophysiology of sleep apnea. Adv Exp Med Biol. 2012;758:343-9.
Yamada K, Asanoi H, Ueno H, Joho S, Takagawa J, Kameyama T, et al. Role of central sympathoexcitation in enhanced hypercapnic chemosensitivity in patients with heart failure. Am Heart J. 2004;148:964-70.
Ding Y, Li YL, Zimmerman MC, Schultz HD. Elevated mitochondrial superoxide contributes to enhanced chemoreflex in heart failure rabbits. Am J Physiol Regul Integr Comp Physiol. 2010;298:R303-11.
Chenuel BJ, Smith CA, Skatrud JB, Henderson KS, Dempsey JA. Increased propensity for apnea in response to acute elevations in left atrial pressure during sleep in the dog. J Appl Physiol. 2006;101:76-83.
Duffin J. The chemoreflex control of breathing and its measurement. Can J Anaesth. 1990;37:933-42.
Duffin J. Measuring the respiratory chemoreflexes in humans. Respir Physiol Neurobiol. 2011;177:71-9.
McClean PA, Phillipson EA, Martinez D, Zamel N. Single breath of CO2 as a clinical test of the peripheral chemoreflex. J Appl Physiol. 1988;64:84-9.
Jennett S, McKay FC, Moss VA. The human ventilatory response to stimulation by transient hypoxia. J Physiol. 1981;315:339-51.
Haldane J, Smith JL. The physiological effects of air vitiated by respiration. J Pathol Bacteriol. 1892;1:168-86.
Read DJ. A clinical method for assessing the ventilatory response to carbon dioxide. Australas Ann Med. 1967;16:20-32.
Duffin J. Measuring the ventilatory response to hypoxia. J Physiol. 2007;584:285-93.
Giannoni A, Emdin M, Poletti R, Bramanti F, Prontera C, Piepoli M, et al. Clinical significance of chemosensitivity in chronic heart failure: influence on neurohormonal derangement, Cheyne-Stokes respiration and arrhythmias. Clin Sci. 2008;114:489-97.
Nielsen M, Smith H. Studies on the regulation of respiration in acute hypoxia; with a appendix on respiratory control during prolonged hypoxia. Acta Physiol Scand. 1952;24:293-313.
Paton JFR, Ratcliffe L, Hering D, Wolf J, Sobotka PA, Narkiewicz K. Revelations about carotid body function through its pathological role in resistant hypertension. Curr Hypertens Rep. 2013;15:273-80.
Niewinski P, Tubek S, Banasiak W, Paton JFR, Ponikowski P. Consequences of peripheral chemoreflex inhibition with low-dose dopamine in humans. J Physiol. 2014;592:1295-308.
Mozer MT, Holbein WW, Joyner MJ, Curry TB, Limberg JK. Reductions in carotid chemoreceptor activity with low-dose dopamine improves baroreflex control of heart rate during hypoxia in humans. Physiol Rep. 2016;4:e12859.
Somers VK, Mark AL, Abboud FM. Potentiation of sympathetic nerve responses to hypoxia in borderline hypertensive subjects. Hypertension. 1988;11:608-12.
Paton JFR, Sobotka PA, Fudim M, Engelman ZJ, Engleman ZJ, Hart ECJ, et al. The carotid body as a therapeutic target for the treatment of sympathetically mediated diseases. Hypertension. 2013;61:5-13.
Younes M, Ostrowski M, Thompson W, Leslie C, Shewchuk W. Chemical control stability in patients with obstructive sleep apnea. Am J Respir Crit Care Med. 2001;163:1181-90.
White DP. Pathogenesis of obstructive and central sleep apnea. Am J Respir Crit Care Med. 2005;172:1363-70.
Leung RST. Sleep-disordered breathing: autonomic mechanisms and arrhythmias. Prog Cardiovasc Dis. 2009;51:324-38.
Mansukhani MP, Wang S, Somers VK. Chemoreflex physiology and implications for sleep apnoea: insights from studies in humans. Exp Physiol. 2015;100:130-5.
Francis DP, Willson K, Davies LC, Coats AJ, Piepoli M. Quantitative general theory for periodic breathing in chronic heart failure and its clinical implications. Circulation. 2000;102:2214-21.
Giannoni A, Gentile F, Navari A, Borrelli C, Mirizzi G, Catapano G, et al. Contribution of the lung to the genesis of Cheyne-Stokes respiration in heart failure: plant gain beyond chemoreflex gain and circulation time. J Am Heart Assoc. 2019;8:e012419.
Giannoni A, Gentile F, Sciarrone P, Borrelli C, Pasero G, Mirizzi G, et al. Upright Cheyne-Stokes respiration in patients with heart failure. J Am Coll Cardiol. 2020;75:2934-46.
Javaheri S, Dempsey JA. Central sleep apnea. Compr Physiol. 2013;3:141-63.
Hall MJ, Xie A, Rutherford R, Ando S, Floras JS, Bradley TD. Cycle length of periodic breathing in patients with and without heart failure. Am J Respir Crit Care Med. 1996;154:376-81.
Oldenburg O, Wellmann B, Buchholz A, Bitter T, Fox H, Thiem U, et al. Nocturnal hypoxaemia is associated with increased mortality in stable heart failure patients. Eur Heart J. 2016;37:1695-703.
Emdin M, Mirizzi G, Giannoni A, Poletti R, Iudice G, Bramanti F, et al. Prognostic significance of central apneas throughout a 24-hour period in patients with heart failure. J Am Coll Cardiol. 2017;70:1351-64.
Borrelli C, Gentile F, Sciarrone P, Mirizzi G, Vergaro G, Ghionzoli N, et al. Central and obstructive apneas in heart failure with reduced, mid-range and preserved ejection fraction. Front Cardiovasc Med. 2019;6:125.
Buchanan GF, Richerson GB. Role of chemoreceptors in mediating dyspnea. Respir Physiol Neurobiol. 2009;167:9-19.
Chua TP, Clark AL, Amadi AA, Coats AJ. Relation between chemosensitivity and the ventilatory response to exercise in chronic heart failure. J Am Coll Cardiol. 1996;27:650-7.
Arzt M, Harth M, Luchner A, Muders F, Holmer SR, Blumberg FC, et al. Enhanced ventilatory response to exercise in patients with chronic heart failure and central sleep apnea. Circulation. 2003;107:1998-2003.
Chua TP, Ponikowski PP, Harrington D, Chambers J, Coats AJ. Contribution of peripheral chemoreceptors to ventilation and the effects of their suppression on exercise tolerance in chronic heart failure. Heart. 1996;76:483-9.
Chua TP, Harrington D, Ponikowski P, Webb-Peploe K, Poole-Wilson PA, Coats AJ. Effects of dihydrocodeine on chemosensitivity and exercise tolerance in patients with chronic heart failure. J Am Coll Cardiol. 1997;29:147-52.
Murphy RM, Shah RV, Malhotra R, Pappagianopoulos PP, Hough SS, Systrom DM, et al. Exercise oscillatory ventilation in systolic heart failure: an indicator of impaired hemodynamic response to exercise. Circulation. 2011;124:1442-51.
Ponikowski P, Chua TP, Piepoli M, Ondusova D, Webb-Peploe K, Harrington D, et al. Augmented peripheral chemosensitivity as a potential input to baroreflex impairment and autonomic imbalance in chronic heart failure. Circulation. 1997;96:2586-94.
Francis DP, Davies LC, Willson K, Ponikowski P, Coats AJ, Piepoli M. Very-low-frequency oscillations in heart rate and blood pressure in periodic breathing: role of the cardiovascular limb of the hypoxic chemoreflex. Clin Sci (Lond). 2000;99:125-32.
Joyner MJ. Preclinical and clinical evaluation of autonomic function in humans. J Physiol. 2016;594:4009-13.
Xing DT, May CN, Booth LC, Ramchandra R. Tonic arterial chemoreceptor activity contributes to cardiac sympathetic activation in mild ovine heart failure. Exp Physiol. 2014;99:1031-41.
Sun SY, Wang W, Zucker IH, Schultz HD. Enhanced peripheral chemoreflex function in conscious rabbits with pacing-induced heart failure. J Appl Physiol. 1999;86:1264-72.
Giannoni A, Raglianti V, Mirizzi G, Taddei C, Del Franco A, Iudice G, et al. Influence of central apneas and chemoreflex activation on pulmonary artery pressure in chronic heart failure. Int J Cardiol. 2016;202:200-6.
Giannoni A, Raglianti V, Taddei C, Borrelli C, Chubuchny V, Vergaro G, et al. Cheyne-Stokes respiration related oscillations in cardiopulmonary hemodynamics in patients with heart failure. Int J Cardiol. 2019;289:76-82.
Ottaviani MM, Wright L, Dawood T, Macefield VG. In vivo recordings from the human vagus nerve using ultrasound-guided microneurography. J Physiol. 2020;598:3569-76.
McBryde FD, Abdala AP, Hendy EB, Pijacka W, Marvar P, Moraes DJA, et al. The carotid body as a putative therapeutic target for the treatment of neurogenic hypertension. Nat Commun. 2013;4:2395.
Mirizzi G, Giannoni A, Ripoli A, Iudice G, Bramanti F, Emdin M, et al. Prediction of the chemoreflex gain by common clinical variables in heart failure. PLoS One. 2016;11:e0153510.
Sutton FD, Zwillich CW, Creagh CE, Pierson DJ, Weil JV. Progesterone for outpatient treatment of Pickwickian syndrome. Ann Intern Med. 1975;83:476-9.
Javaheri S, Guerra L. Effects of domperidone and medroxyprogesterone acetate on ventilation in man. Respir Physiol. 1990;81:359-70.
Javaheri S, Brown LK, Khayat RN. Update on apneas of heart failure with reduced ejection fraction: emphasis on the physiology of treatment: Part 2: central sleep apnea. Chest. 2020;157:1637-46.
Contini M, Apostolo A, Cattadori G, Paolillo S, Iorio A, Bertella E, et al. Multiparametric comparison of CARvedilol, vs. NEbivolol, vs. BIsoprolol in moderate heart failure: the CARNEBI trial. Int J Cardiol. 2013;168:2314-40.
Agostoni P, Contini M, Magini A, Apostolo A, Cattadori G, Bussotti M, et al. Carvedilol reduces exercise-induced hyperventilation: a benefit in normoxia and a problem with hypoxia. Eur J Heart Fail. 2006;8:729-35.
Li YL, Xia XH, Zheng H, Gao L, Li YF, Liu D, et al. Angiotensin II enhances carotid body chemoreflex control of sympathetic outflow in chronic heart failure rabbits. Cardiovasc Res. 2006;71:129-38.
Cundrle I Jr, Johnson BD, Rea RF, Scott CG, Somers VK, Olson LJ. Modulation of ventilatory reflex control by cardiac resynchronization therapy. J Card Fail. 2015;21:367-73.
Mezzani A, Pistono M, Agostoni P, Giordano A, Gnemmi M, Imparato A, et al. Exercise gas exchange in continuous-flow left ventricular assist device recipients. PLoS One. 2018;13:e0187112.
Apostolo A, Paolillo S, Contini M, Vignati C, Tarzia V, Campodonico J, et al. Comprehensive effects of left ventricular assist device speed changes on alveolar gas exchange, sleep ventilatory pattern, and exercise performance. J Heart Lung Transplant. 2018;37:1361-71.
Ciarka A, Cuylits N, Vachiery JL, Lamotte M, Degaute JP, Naeije R, et al. Increased peripheral chemoreceptors sensitivity and exercise ventilation in heart transplant recipients. Circulation. 2006;113:252-7.
Bitter T, Westerheide N, Hossain MS, Lehmann R, Prinz C, Kleemeyer A, et al. Complex sleep apnoea in congestive heart failure. Thorax. 2011;66:402-7.
Costanzo MR, Ponikowski P, Javaheri S, Augostini R, Goldberg L, Holcomb R, et al. Transvenous neurostimulation for central sleep apnoea: a randomised controlled trial. Lancet. 2016;388:974-82.
Imadojemu VA, Mawji Z, Kunselman A, Gray KS, Hogeman CS, Leuenberger UA. Sympathetic chemoreflex responses in obstructive sleep apnea and effects of continuous positive airway pressure therapy. Chest. 2007;131:1406-13.
Spicuzza L, Bernardi L, Balsamo R, Ciancio N, Polosa R, Di Maria G. Effect of treatment with nasal continuous positive airway pressure on ventilatory response to hypoxia and hypercapnia in patients with sleep apnea syndrome. Chest. 2006;130:774-9.
Fontana M, Emdin M, Giannoni A, Iudice G, Baruah R, Passino C. Effect of acetazolamide on chemosensitivity, Cheyne-Stokes respiration, and response to effort in patients with heart failure. Am J Cardiol. 2011;107:1675-80.
Giannoni A, Passino C, Mirizzi G, Del Franco A, Aimo A, Emdin M. Treating chemoreflex in heart failure: modulation or demolition? J Physiol. 2014;592:1903-4.
Niewinski P, Janczak D, Rucinski A, Tubek S, Engelman ZJ, Jazwiec P, et al. Dissociation between blood pressure and heart rate response to hypoxia after bilateral carotid body removal in men with systolic heart failure. Exp Physiol. 2014;99:552-61.
Javaheri S, Parker TJ, Wexler L, Liming JD, Lindower P, Roselle GA. Effect of theophylline on sleep-disordered breathing in heart failure. N Engl J Med. 1996;335:562-7.
Javaheri S, Guerra L. Lung function, hypoxic and hypercapnic ventilatory responses, and respiratory muscle strength in normal subjects taking oral theophylline. Thorax. 1990;45:743-7.
Del Rio R, Marcus NJ, Schultz HD. Inhibition of hydrogen sulfide restores normal breathing stability and improves autonomic control during experimental heart failure. J Appl Physiol. 2013;114:1141-50.
Haack KKV, Marcus NJ, Del Rio R, Zucker IH, Schultz HD. Simvastatin treatment attenuates increased respiratory variability and apnea/hypopnea index in rats with chronic heart failure. Hypertension. 2014;63:1041-9.
Javaheri A, Rader DJ, Javaheri S. Statin therapy in heart failure: is it time for a second look? Hypertension. 2014;63:909-10.
Zeitler EP, Abraham WT. Novel devices in heart failure: BAT, atrial shunts, and phrenic nerve stimulation. JACC Heart Fail. 2020;8:251-64.
Heusser K, Thöne A, Lipp A, Menne J, Beige J, Reuter H, et al. Efficacy of electrical baroreflex activation is independent of peripheral chemoreceptor modulation. Hypertension. 2020;75:257-64.

Auteurs

Alberto Giannoni (A)

Health Science Interdisciplinary Center, Scuola Superiore Sant'Anna, Pisa, Italy.
Fondazione Toscana G. Monasterio, Pisa, Italy.

Chiara Borrelli (C)

Fondazione Toscana G. Monasterio, Pisa, Italy.

Francesco Gentile (F)

Health Science Interdisciplinary Center, Scuola Superiore Sant'Anna, Pisa, Italy.

Paolo Sciarrone (P)

Fondazione Toscana G. Monasterio, Pisa, Italy.

Jens Spießhöfer (J)

Health Science Interdisciplinary Center, Scuola Superiore Sant'Anna, Pisa, Italy.
University of Aachen, Aachen, Germany.

Massimo Piepoli (M)

IRCCS Policlinico San Donato, Milano, Italy.

George B Richerson (GB)

Department of Neurology, University of Iowa, Iowa City, IA, USA.

John S Floras (JS)

Division of Cardiology, Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada.

Andrew J S Coats (AJS)

Heart Research Institute, Sydney, Australia.

Shahrokh Javaheri (S)

Division of Pulmonary and Sleep Medicine, Bethesda North Hospital, Cincinnati, Ohio, Division of Pulmonary, Critical Care and Sleep Medicine, University of Cincinnati, Cincinnati, Ohio, and Division of Cardiology, The Ohio State University, Columbus, OH, USA.

Michele Emdin (M)

Health Science Interdisciplinary Center, Scuola Superiore Sant'Anna, Pisa, Italy.
Fondazione Toscana G. Monasterio, Pisa, Italy.

Claudio Passino (C)

Health Science Interdisciplinary Center, Scuola Superiore Sant'Anna, Pisa, Italy.
Fondazione Toscana G. Monasterio, Pisa, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH