Abstract
The carotid bodies (CBs) play a role as metabolic sensors being deeply involved in the genesis of dysmetabolic states. CB activity was shown to be increased in prediabetes and type 2 diabetes animal models and also in prediabetic patients. Furthermore, abolishment of CB activity, via carotid sinus nerve surgical resection, both prevents and reverses pathological metabolic disease features in animal models.
Herein, we review in a concise manner the pathways linking CB chemoreceptor dysfunction to the pathogenesis of metabolic diseases and describe the methods available to evaluate CB chemosensitivity, postulated to be directly related to metabolic dysfunction. Moreover, we describe the biomarkers used to diagnose prediabetes and introduce the CB, as a novel biomarker for its early screening. A final section is devoted to debate the applications of CB chemosensitivity evaluation, not only as a biomarker for early screening of prediabetes but also to identify subgroups of patients that will benefit from therapeutics directed to modulate CB activity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- ADA:
-
American Diabetes Association
- BMI:
-
Body mass index
- CB:
-
Carotid body
- CCA:
-
Common carotid artery
- CSN:
-
Carotid sinus nerve
- EASD:
-
European Association for the Study of Diabetes
- FINDRISC:
-
Finnish Diabetes Risk Score
- FiO2:
-
Oxygen fraction in inspired air
- HbA1c:
-
Glycated hemoglobin
- HF:
-
High fat
- HOMA:
-
Homeostatic model assessment
- HR:
-
Heart rate
- HVR:
-
Hypoxic ventilatory response
- IDF:
-
International Diabetes Federation
- IFG:
-
Impaired fasting glucose
- iGlu:
-
Interstitial glucose
- IGT:
-
Impaired glucose tolerance
- IL:
-
Interleukin
- NTS:
-
Nucleus of tractus solitarius
- OGTT:
-
Oral glucose tolerance test
- OSA:
-
Obstructive sleep apnea
- RR:
-
Respiratory rate
- SNS:
-
Sympathetic nervous system
- SpO2:
-
Peripheral oxygen saturation
- T2D:
-
Type 2 diabetes
- TNF-α:
-
Tumor necrosis factor alpha
- WHO:
-
World Health Organization
References
Alberti KGMM, Zimmet P, Shaw J. International Diabetes Federation: a consensus on type 2 diabetes prevention. Diabet Med. 2007;24:451–63. https://doi.org/10.1111/J.1464-5491.2007.02157.X.
Algoblan A, Alalfi M, Khan M. Mechanism linking diabetes mellitus and obesity. Diabetes Metab Syndr Obes Targets Ther. 2014;7:587. https://doi.org/10.2147/DMSO.S67400.
American Diabetes Association. Classification and diagnosis of diabetes: standards of medical care in diabetes – 2021. Diabetes Care. 2021;44:S15–33. https://doi.org/10.2337/DC21-S002.
Barbosa TC, Kaur J, Holwerda SW, et al. Insulin increases ventilation during euglycemia in humans. Am J Physiol Regul Integr Comp Physiol. 2018;315:84–9. https://doi.org/10.1152/ajpregu.00039.2018.-Evidence.
Barry E, Roberts S, Oke J, et al. Efficacy and effectiveness of screen and treat policies in prevention of type 2 diabetes: systematic review and meta-analysis of screening tests and interventions. BMJ. 2017;356. https://doi.org/10.1136/BMJ.I6538.
Bascom DA, Clement ID, Dorrington KL, Robbins PA. Effects of dopamine and domperidone on ventilation during isocapnic hypoxia in humans. Respir Physiol. 1991;85:319–28. https://doi.org/10.1016/0034-5687(91)90071-P.
Berger S, Polotsky VY. Leptin and leptin resistance in the pathogenesis of obstructive sleep apnea: a possible link to oxidative stress and cardiovascular complications. Oxidative Med Cell Longev. 2018;2018:1–8. https://doi.org/10.1155/2018/5137947.
Berne RM, Rubio R, Curnish RR. Release of adenosine from ischemic brain. Circ Res. 1974;35:262–71. https://doi.org/10.1161/01.RES.35.2.262.
Bin-Jaliah I, Maskell PD, Kumar P. Indirect sensing of insulin-induced hypoglycaemia by the carotid body in the rat. J Physiol. 2004;556:255–66. https://doi.org/10.1113/JPHYSIOL.2003.058321.
Blüher M, Mantzoros CS. From leptin to other adipokines in health and disease: facts and expectations at the beginning of the 21st century. Metabolism. 2015;64:131–45. https://doi.org/10.1016/J.METABOL.2014.10.016.
Booth A, Magnuson A, Fouts J, Foster MT. Adipose tissue: an endocrine organ playing a role in metabolic regulation. Horm Mol Biol Clin Investig. 2016;26:25–42. https://doi.org/10.1515/HMBCI-2015-0073.
Brito GC, Fonseca-Pinto R, Guarino MP, et al. CBView: merging data in metabolic diagnosis. Procedia Comput Sci. 2018;138:244–9. https://doi.org/10.1016/j.procs.2018.10.035.
Buijsse B, Simmons RK, Griffin SJ, Schulze MB. Risk assessment tools for identifying individuals at risk of developing type 2 diabetes. Epidemiol Rev. 2011;33:46–62. https://doi.org/10.1093/EPIREV/MXQ019.
Caballero-Eraso C, Shin M-K, Pho H, et al. Leptin acts in the carotid bodies to increase minute ventilation during wakefulness and sleep and augment the hypoxic ventilatory response. J Physiol. 2019;597:151–72. https://doi.org/10.1113/JP276900.
Chua TP, Coats AJS. The reproducibility and comparability of tests of the peripheral chemoreflex: comparing the transient hypoxic ventilatory drive test and the single-breath carbon dioxide response test in healthy subjects. Eur J Clin Investig. 1995;25:887–92. https://doi.org/10.1111/J.1365-2362.1995.TB01962.X.
Conde SV, Gonzalez C, Batuca JR, et al. An antagonistic interaction between A2B adenosine and D2 dopamine receptors modulates the function of rat carotid body chemoreceptor cells. J Neurochem. 2008;107:1369–81. https://doi.org/10.1111/J.1471-4159.2008.05704.X.
Conde SV, Monteiro EC. Hypoxia induces adenosine release from the rat carotid body. J Neurochem. 2004;89:1148–56. https://doi.org/10.1111/J.1471-4159.2004.02380.X.
Conde SV, Monteiro EC, Rigual R, et al. Hypoxic intensity: a determinant for the contribution of ATP and adenosine to the genesis of carotid body chemosensory activity. J Appl Physiol. 2012;112:2002–10. https://doi.org/10.1152/JAPPLPHYSIOL.01617.2011.
Conde SV, Monteiro EC, Sacramento JF. Purines and carotid body: new roles in pathological conditions. Front Pharmacol. 2017a;8:913. https://doi.org/10.3389/fphar.2017.00913.
Conde SV, Ribeiro MJ, Melo BF, et al. Insulin resistance: a new consequence of altered carotid body chemoreflex? J Physiol. 2017b;595:31–41. https://doi.org/10.1113/JP271684.
Conde SV, Sacramento JF, Guarino MP. Carotid body: a metabolic sensor implicated in insulin resistance. Physiol Genomics. 2018;50:208–14. https://doi.org/10.1152/PHYSIOLGENOMICS.00121.2017.
Conde SV, Sacramento JF, Guarino MP, et al. Carotid body, insulin, and metabolic diseases: unraveling the links. Front Physiol. 2014;5:418. https://doi.org/10.3389/fphys.2014.00418.
Conde SV, Sacramento JF, Martins FO. Immunity and the carotid body: implications for metabolic diseases. Bioelectron Med. 2020;61(6):1–20. https://doi.org/10.1186/S42234-020-00061-5.
Cosentino F, Grant PJ, Aboyans V, et al. The Task Force for diabetes, pre-diabetes, and cardiovascular diseases of the European Society of Cardiology (ESC) and the European Association for the Study of Diabetes (EASD). Eur Heart J. 2020;41:255–323. https://doi.org/10.1093/EURHEARTJ/EHZ486.
Cracchiolo M, Sacramento JF, Mazzoni A, et al. High frequency shift in carotid sinus nerve and sympathetic nerve activity in type 2 diabetic rat model *. In: 9th international IEEE/EMBS conference on neural engineering (NER). IEEE; 2019a. p. 498–501.
Cracchiolo M, Sacramento JF, Mazzoni A, et al. Decoding neural metabolic markers from the carotid sinus nerve in a type 2 diabetes model. IEEE Trans Neural Syst Rehabil Eng. 2019b;27:2034–43. https://doi.org/10.1109/TNSRE.2019.2942398.
Cramer JA, Wiggins RH, Fudim M, et al. Carotid body size on CTA: correlation with comorbidities. Clin Radiol. 2014;69:e33–6. https://doi.org/10.1016/J.CRAD.2013.08.016.
Cunha-Guimaraes JP, Guarino MP, Timóteo AT, et al. Carotid body chemosensitivity: early biomarker of dysmetabolism in humans. Eur J Endocrinol. 2020;182:549–57. https://doi.org/10.1530/EJE-19-0976.
Dejours P. Chemoreflexes in breathing. Physiol Rev. 1962;42:335–58. https://doi.org/10.1152/PHYSREV.1962.42.3.335.
Dejours P. Control of respiration by arterial chemoreceptors. Ann N Y Acad Sci. 1963;109:682–95. https://doi.org/10.1111/J.1749-6632.1963.TB13497.X.
Dorcely B, Katz K, Jagannathan R, et al. Novel biomarkers for prediabetes, diabetes, and associated complications. Diabetes Metab Syndr Obes Targets Ther. 2017;10:345–61. https://doi.org/10.2147/DMSO.S100074.
Eikelis N, Schlaich M, Aggarwal A, et al. Interactions between leptin and the human sympathetic nervous system. Hypertension. 2003;41:1072–9. https://doi.org/10.1161/01.HYP.0000066289.17754.49.
Ferrannini E, Gastaldelli A, Miyazaki Y, et al. β-Cell function in subjects spanning the range from normal glucose tolerance to overt diabetes: a new analysis. J Clin Endocrinol Metab. 2005;90:493–500. https://doi.org/10.1210/JC.2004-1133.
Gonzalez C, Agapito MT, Rocher A, et al. A revisit to O2 sensing and transduction in the carotid body chemoreceptors in the context of reactive oxygen species biology. Respir Physiol Neurobiol. 2010;174:317–30. https://doi.org/10.1016/j.resp.2010.09.002.
Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev. 1994;74:829–98. https://doi.org/10.1152/PHYSREV.1994.74.4.829.
Hostalek U. Global epidemiology of prediabetes – present and future perspectives. Clin Diabetes Endocrinol. 2019;51(5):1–5. https://doi.org/10.1186/S40842-019-0080-0.
Hu FB, Stampfer MJ, Haffner SM, et al. Elevated risk of cardiovascular disease prior to clinical diagnosis of type 2 diabetes. Diabetes Care. 2002;25:1129–34. https://doi.org/10.2337/DIACARE.25.7.1129.
International Diabetes Federation. IDF Diabetes Atlas. 10th ed; 2021. https://diabetesatlas.org/. Accessed on 03 March 2022
Joyner MJ, Limberg JK, Wehrwein EA, Johnson BD. Role of the carotid body chemoreceptors in glucose homeostasis and thermoregulation in humans. J Physiol. 2018;596:3079–85. https://doi.org/10.1113/JP274354.
Kåhlin J, Mkrtchian S, Ebberyd A, et al. The human carotid body releases acetylcholine, ATP and cytokines during hypoxia. Exp Physiol. 2014;99:1089–98. https://doi.org/10.1113/EXPPHYSIOL.2014.078873.
Khaodhiar L, Cummings S, Apovian CM. Treating diabetes and prediabetes by focusing on obesity management. Curr Diab Rep. 2009;9:348. https://doi.org/10.1007/S11892-009-0055-0.
Lahiri S, DeLaney RG. Relationship between carotid chemoreceptor activity and ventilation in the cat. Respir Physiol. 1975;24:267–86. https://doi.org/10.1016/0034-5687(75)90018-3.
Lam S-Y, Liu Y, Ng K-M, et al. Chronic intermittent hypoxia induces local inflammation of the rat carotid body via functional upregulation of proinflammatory cytokine pathways. Histochem Cell Biol. 2012;137:303–17. https://doi.org/10.1007/s00418-011-0900-5.
Lambert EA, Straznicky NE, Dixon JB, Lambert GW. Should the sympathetic nervous system be a target to improve cardiometabolic risk in obesity? Am J Physiol Heart Circ Physiol. 2015;309:H244–58. https://doi.org/10.1152/AJPHEART.00096.2015.
Lambert GW, Straznicky NE, Lambert EA, et al. Sympathetic nervous activation in obesity and the metabolic syndrome – causes, consequences and therapeutic implications. Pharmacol Ther. 2010;126:159–72. https://doi.org/10.1016/j.pharmthera.2010.02.002.
Limberg JK, Johnson BD, Holbein WW, et al. Interindividual variability in the dose-specific effect of dopamine on carotid chemoreceptor sensitivity to hypoxia. J Appl Physiol. 2016;120:138–47. https://doi.org/10.1152/JAPPLPHYSIOL.00723.2015.
Lindström J, Tuomilehto J. The diabetes risk score. Diabetes Care. 2003;26:725–31. https://doi.org/10.2337/DIACARE.26.3.725.
López-Barneo J. Oxygen sensing and stem cell activation in the hypoxic carotid body. Cell Tissue Res. 2018;3722(372):417–25. https://doi.org/10.1007/S00441-017-2783-9.
Marshall JM. Peripheral chemoreceptors and cardiovascular regulation. Physiol Rev. 1994;74:543–94. https://doi.org/10.1152/PHYSREV.1994.74.3.543.
Mata-Cases M, Artola S, Escalada J, et al. Consensus on the detection and management of prediabetes. Consensus and Clinical Guidelines Working Group of the Spanish Diabetes Society. Rev Clínica Española (English Ed). 2015;215:117–29. https://doi.org/10.1016/j.rceng.2014.10.001.
Matafome P, Seiça R. Function and dysfunction of adipose tissue. Adv Neurobiol. 2017;19:3–31. https://doi.org/10.1007/978-3-319-63260-5_1.
Mkrtchian S, Kåhlin J, Ebberyd A, et al. The human carotid body transcriptome with focus on oxygen sensing and inflammation – a comparative analysis. J Physiol. 2012;590:3807–19. https://doi.org/10.1113/jphysiol.2012.231084.
Monteiro E, Ribeiro J. Ventilatory effects of adenosine mediated by carotid body chemoreceptors in the rat. Naunyn Schmiedeberg’s Arch Pharmacol. 1987;335:143–8. https://doi.org/10.1007/BF00177715.
Moser G, Schrader J, Deussen A. Turnover of adenosine in plasma of human and dog blood. Am J Phys. 1989;256. https://doi.org/10.1152/AJPCELL.1989.256.4.C799.
Nair S, Gupta A, Fudim M, et al. CT angiography in the detection of carotid body enlargement in patients with hypertension and heart failure. Neuroradiology. 2013;55:1319–22. https://doi.org/10.1007/S00234-013-1273-3.
Niewinski P. Carotid body modulation in systolic heart failure from the clinical perspective. J Physiol. 2016;595:53–61. https://doi.org/10.1113/JP271692.
Niewinski P, Tubek S, Banasiak W, et al. Consequences of peripheral chemoreflex inhibition with low-dose dopamine in humans. J Physiol. 2014;592:1295–308. https://doi.org/10.1113/JPHYSIOL.2013.266858.
O’Donnell CP, Schaub CD, Haines AS, et al. Leptin prevents respiratory depression in obesity. Am J Respir Crit Care Med. 1999;159:1477–84. https://doi.org/10.1164/ajrccm.159.5.9809025.
Olea E, Ribeiro MJ, Gallego-Martin T, et al. The carotid body does not mediate the acute ventilatory effects of leptin. Adv Exp Med Biol. 2015;860:379–85. https://doi.org/10.1007/978-3-319-18440-1_43.
Olson DE, Zhu M, Long Q, et al. Increased cardiovascular disease, resource use, and costs before the clinical diagnosis of diabetes in veterans in the southeastern U.S. J Gen Intern Med. 2015;30:749–57. https://doi.org/10.1007/S11606-014-3075-7.
Ortega-Sáenz P, Pardal R, Levitsky K, et al. Cellular properties and chemosensory responses of the human carotid body. J Physiol. 2013;591:6157–73. https://doi.org/10.1113/JPHYSIOL.2013.263657.
Paleczny B, Siennicka A, Zacharski M, et al. Increased body fat is associated with potentiation of blood pressure response to hypoxia in healthy men: relations with insulin and leptin. Clin Auton Res. 2016;262(26):107–16. https://doi.org/10.1007/S10286-015-0338-2.
Pardal R, Ortega-Sáenz P, Durán R, López-Barneo J. Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell. 2007;131:364–77. https://doi.org/10.1016/j.cell.2007.07.043.
Paulweber B, Valensi P, Lindström J, et al. A European evidence-based guideline for the prevention of type 2 diabetes. Horm Metab Res. 2010;42:S3–S36. https://doi.org/10.1055/S-0029-1240928.
Pereda SA, Eckstein JW, Abboud FM. Cardiovascular responses to insulin in the absence of hypoglycemia. Am J Phys. 1962;202:249–52. https://doi.org/10.1152/AJPLEGACY.1962.202.2.249.
Pijacka W, Moraes DJA, Ratcliffe LEK, et al. Purinergic receptors in the carotid body as a new drug target for controlling hypertension. Nat Med. 2016;2210(22):1151–9. https://doi.org/10.1038/nm.4173.
Porzionato A, Macchi V, De Caro R, Di Giulio C. Inflammatory and immunomodulatory mechanisms in the carotid body. Respir Physiol Neurobiol. 2013;187:31–40. https://doi.org/10.1016/j.resp.2013.02.017.
Prabhakar NR. Carotid body chemoreflex: a driver of autonomic abnormalities in sleep apnoea. Exp Physiol. 2016;101:975–85. https://doi.org/10.1113/EP085624.
Quintero M, Olea E, Conde SV, et al. Age protects from harmful effects produced by chronic intermittent hypoxia. J Physiol. 2016;594:1773–90. https://doi.org/10.1113/JP270878.
Ribeiro MJ, Sacramento JF, Gallego-Martin T, et al. High fat diet blunts the effects of leptin on ventilation and on carotid body activity. J Physiol. 2018;596:3187–99. https://doi.org/10.1113/JP275362.
Ribeiro MJ, Sacramento JF, Gonzalez C, et al. Carotid body denervation prevents the development of insulin resistance and hypertension induced by Hypercaloric diets. Diabetes. 2013;62:2905–16. https://doi.org/10.2337/DB12-1463.
Ruud J, Steculorum SM, Brüning JC. Neuronal control of peripheral insulin sensitivity and glucose metabolism. Nat Commun. 2017;8:15259. https://doi.org/10.1038/ncomms15259.
Sacramento JF, Andrzejewski K, Melo BF, et al. Exploring the mediators that promote carotid body dysfunction in type 2 diabetes and obesity related syndromes. Int J Mol Sci. 2020;21:5545. https://doi.org/10.3390/IJMS21155545.
Sacramento JF, Chew DJ, Melo BF, et al. Bioelectronic modulation of carotid sinus nerve activity in the rat: a potential therapeutic approach for type 2 diabetes. Diabetologia. 2018;613(61):700–10. https://doi.org/10.1007/S00125-017-4533-7.
Sacramento JF, Olea E, Ribeiro MJ, et al. Contribution of adenosine and ATP to the carotid body chemosensory activity in ageing. J Physiol. 2019;597:4991–5008. https://doi.org/10.1113/JP274179.
Sacramento JF, Ribeiro MJ, Rodrigues T, et al. Functional abolition of carotid body activity restores insulin action and glucose homeostasis in rats: key roles for visceral adipose tissue and the liver. Diabetologia. 2017;60:158–68. https://doi.org/10.1007/S00125-016-4133-Y.
Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas, 9th edition. Diabetes Res Clin Pract. 2019;157:107843. https://doi.org/10.1016/j.diabres.2019.107843.
Dos Santos E, Sacramento JF, Melo BF, Conde SV. Carotid body dysfunction in diet-induced insulin resistance is associated with alterations in its morphology. Adv Exp Med Biol. 2018;1071:103–8. https://doi.org/10.1007/978-3-319-91137-3_13.
Schwarz PEH, Li J, Reimann M, et al. The Finnish Diabetes Risk Score is associated with insulin resistance and progression towards type 2 diabetes. J Clin Endocrinol Metab. 2009;94:920–6. https://doi.org/10.1210/JC.2007-2427.
Sequeira IR, Poppitt SD. HbA1c as a marker of prediabetes: a reliable screening tool or not. Insights Nutr Metab. 2017;1:21–29
Tabák AG, Herder C, Rathmann W, et al. Prediabetes: a high-risk state for diabetes development. Lancet. 2012;379:2279–90. https://doi.org/10.1016/S0140-6736(12)60283-9.
Tankersley CG, O’Donnell C, Daood MJ, et al. Leptin attenuates respiratory complications associated with the obese phenotype. J Appl Physiol. 1998;85:2261–9. https://doi.org/10.1152/JAPPL.1998.85.6.2261.
Tankova T, Chakarova N, Atanassova I, Dakovska L. Evaluation of the Finnish Diabetes Risk Score as a screening tool for impaired fasting glucose, impaired glucose tolerance and undetected diabetes. Diabetes Res Clin Pract. 2011;92:46–52. https://doi.org/10.1016/j.diabres.2010.12.020.
Thomas DD, Corkey BE, Istfan NW, Apovian CM. Hyperinsulinemia: an early indicator of metabolic dysfunction. J Endocr Soc. 2019;3:1727–47. https://doi.org/10.1210/js.2019-00065.
Thorp AA, Schlaich MP. Relevance of sympathetic nervous system activation in obesity and metabolic syndrome. J Diabetes Res. 2015;2015:1–11. https://doi.org/10.1155/2015/341583.
Tubek S, Niewinski P, Reczuch K, et al. Effects of selective carotid body stimulation with adenosine in conscious humans. J Physiol. 2016;594:6225–40. https://doi.org/10.1113/JP272109.
Tuso P. Prediabetes and lifestyle modification: time to prevent a preventable disease. Perm J. 2014;18:88–93. https://doi.org/10.7812/TPP/14-002.
Uematsu T, Kozawa O, Matsuno H, et al. Pharmacokinetics and tolerability of intravenous infusion of adenosine (SUNY4001) in healthy volunteers. Br J Clin Pharmacol. 2000;50:177–81. https://doi.org/10.1046/J.1365-2125.2000.00214.X.
Vera-Cruz P, Guerreiro F, Ribeiro MJ, et al. Hyperbaric oxygen therapy improves glucose homeostasis in type 2 diabetes patients: a likely involvement of the carotid bodies. Adv Exp Med Biol. 2015;860:221–5. https://doi.org/10.1007/978-3-319-18440-1_24.
Vidal ML, Luis CFJ, Chávez HRT, et al. Insulin in the carotid sinus increases suprahepatic and arterial glucose levels. Rev Cuba Invest Biomed. 2019;38:e102.
Ward DS, Voter WA, Karan S. The effects of hypo- and hyperglycaemia on the hypoxic ventilatory response in humans. J Physiol. 2007;582:859–69. https://doi.org/10.1113/JPHYSIOL.2007.130112.
Watt A, Reid P, Stephens M, Routledge P. Adenosine-induced respiratory stimulation in man depends on site of infusion. Evidence for an action on the carotid body? Br J Clin Pharmacol. 1987;23:486–90. https://doi.org/10.1111/J.1365-2125.1987.TB03081.X.
Watt A, Routledge P. Adenosine stimulates respiration in man. Br J Clin Pharmacol. 1985;20:503–6. https://doi.org/10.1111/J.1365-2125.1985.TB05108.X.
Waugh N, Shyangdan D, Taylor-Phillips S, et al. Screening for type 2 diabetes: a short report for the National Screening Committee. Health Technol Assess. 2013;17:1–89. https://doi.org/10.3310/HTA17350.
Wehrwein EA, Basu R, Basu A, et al. Hyperoxia blunts counterregulation during hypoglycaemia in humans: possible role for the carotid bodies? J Physiol. 2010;588:4593–601. https://doi.org/10.1113/JPHYSIOL.2010.197491.
Wehrwein EA, Limberg JK, Taylor JL, et al. Effect of bilateral carotid body resection on the counterregulatory response to hypoglycaemia in humans. Exp Physiol. 2015;100:69–78. https://doi.org/10.1113/EXPPHYSIOL.2014.083154.
Welch BT, Petersen-Jones HG, Eugene AR, et al. Impact of sleep disordered breathing on carotid body size. Respir Physiol Neurobiol. 2017;236:5–10. https://doi.org/10.1016/J.RESP.2016.10.013.
Welsh MJ, Heistad DD, Abboud FM. Depression of ventilation by dopamine in man. Evidence for an effect on the chemoreceptor reflex. J Clin Invest. 1978;61:708–13. https://doi.org/10.1172/JCI108983.
Wilson PWF, Meigs JB, Sullivan L, et al. Prediction of incident diabetes mellitus in middle-aged adults: the Framingham Offspring Study. Arch Intern Med. 2007;167:1068–74. https://doi.org/10.1001/ARCHINTE.167.10.1068.
Word Health Organization. Regional Office for Europe. Nutrition, overweight and obesity: factsheet on Sustainable Development Goals (SDGs): health targets. 2021.
World Health Organization. Definition and diagnosis of diabetes mellitus and intermediate hyperglycemia. 2006.
Yip WCY, Sequeira IR, Plank LD, Poppitt SD. Prevalence of pre-diabetes across ethnicities: a review of impaired fasting glucose (IFG) and impaired glucose tolerance (IGT) for classification of Dysglycaemia. Nutrients. 2017;9:1273. https://doi.org/10.3390/NU9111273.
Yuan F, Wang H, Feng J, et al. Leptin signaling in the carotid body regulates a hypoxic ventilatory response through altering TASK Channel expression. Front Physiol. 2018;9:249. https://doi.org/10.3389/fphys.2018.00249.
Zapata P, Larraín C, Reyes P, Fernández R. Immunosensory signalling by carotid body chemoreceptors. Respir Physiol Neurobiol. 2011;178:370–4. https://doi.org/10.1016/j.resp.2011.03.025.
Zimmet P, Alberti KGMM, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414:782–7. https://doi.org/10.1038/414782a.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 Springer Nature Switzerland AG
About this entry
Cite this entry
Conde, S.V., Lages, M., Guarino, M.P., Sacramento, J.F. (2022). Carotid Bodies:Use of Chemosensitivity as a Biomarker in Prediabetes. In: Patel, V.B., Preedy, V.R. (eds) Biomarkers in Diabetes. Biomarkers in Disease: Methods, Discoveries and Applications. Springer, Cham. https://doi.org/10.1007/978-3-030-81303-1_38-1
Download citation
DOI: https://doi.org/10.1007/978-3-030-81303-1_38-1
Received:
Accepted:
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-81303-1
Online ISBN: 978-3-030-81303-1
eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences