The Vagus Nerve Can Predict and Possibly Modulate Non-Communicable Chronic Diseases: Introducing a Neuroimmunological Paradigm to Public Health
Abstract
:1. The Problem
2. Oxidative Stress and Chronic Diseases
3. Inflammation and Chronic Diseases
4. Excessive Sympathetic Nervous System Activity and Chronic Diseases
5. Introducing Neuro-Immunology and Neuro-Modulation to Public Health
6. Epidemiological Path: Vagal Nerve Activity Predicts Risk and prognosis of Chronic Diseases
7. Biological Path: The Vagus Nerve Inhibits Oxidative Stress, Inflammation and Sympathetic Activity
8. Behavioral Path: Effects of Vagal Activity on Lifestyle Risk Factors of Chronic Diseases
9. Implications for Prevention and Treatment: Activating the Vagal Nerve for Health
10. Note of Caution
11. Summary
Funding
Conflicts of Interest
References
- GBD 2016 Causes of Death Collaborators. Global, regional, and national age-sex specific mortality for 264 causes of death, 1980–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 2017, 390, 1151–1210. [Google Scholar] [CrossRef]
- GBD 2015 Risk Factors Collaborators. Global, regional, and national comparative risk assessment of 79 behavioural, environmental and occupational, and metabolic risks or clusters of risks, 1990–2015: A systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016, 388, 1659–1724. [Google Scholar] [CrossRef]
- Lelieveld, J.; Evans, J.S.; Fnais, M.; Giannadaki, D.; Pozzer, A. The contribution of outdoor air pollution sources to premature mortality on a global scale. Nature 2015, 525, 367–371. [Google Scholar] [CrossRef] [PubMed]
- Kruk, J. Physical activity in the prevention of the most frequent chronic diseases: An analysis of the recent evidence. Asian Pac. J. Cancer Prev. 2007, 8, 325–338. [Google Scholar] [PubMed]
- NCD Risk Factor Collaboration (NCD-RisC). Africa Working Group. Trends in obesity and diabetes across Africa from 1980 to 2014: An analysis of pooled population-based studies. Int. J. Epidemiol. 2017, 46, 1421–1432. [Google Scholar] [CrossRef] [PubMed]
- Moran, A.E.; Forouzanfar, M.H.; Roth, G.A.; Mensah, G.A.; Ezzati, M.; Flaxman, A.; Murray, C.J.; Naghavi, M. The global burden of ischemic heart disease in 1990 and 2010: The Global Burden of Disease 2010 study. Circulation 2014, 129, 1493–1501. [Google Scholar] [CrossRef] [PubMed]
- Park, H.M.; Woo, H.; Jung, S.J.; Jung, K.W.; Shin, H.R.; Shin, A. Colorectal cancer incidence in 5 Asian countries by subsite: An analysis of Cancer Incidence in Five Continents (1998–2007). Cancer Epidemiol. 2016, 45, 65–70. [Google Scholar] [CrossRef] [PubMed]
- Daubisse-Marliac, L.; Delafosse, P.; Boitard, J.B.; Poncet, F.; Grosclaude, P.; Colonna, M. Breast cancer incidence and time trend in France from 1990 to 2007: A population-based study from two French cancer registries. Ann. Oncol. 2011, 22, 329–334. [Google Scholar] [CrossRef] [PubMed]
- GBD 2016 DALYs and HALE Collaborators. Global, regional, and national disability-adjusted life-years (DALYs) for 333 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet 2017, 390, 1260–1344. [Google Scholar] [CrossRef]
- López-Campos, J.L.; Tan, W.; Soriano, J.B. Global burden of COPD. Respirology 2016, 21, 14–23. [Google Scholar] [CrossRef] [PubMed]
- Gidron, Y.; Perry, H.; Glennie, M. The Vagus may inform the brain about sub-clinical tumours and modulate them: An Hypothesis. Lancet Oncol. 2005, 6, 245–248. [Google Scholar] [CrossRef]
- De Couck, M.; Mravec, B.; Gidron, Y. You may need the vagus nerve to understand pathophysiology and to treat diseases. Clin. Sci. 2012, 122, 323–328. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bourdrel, T.; Bind, M.A.; Béjot, Y.; Morel, O.; Argacha, J.F. Cardiovascular effects of air pollution. Arch. Cardiovasc. Dis. 2017, 110, 634–642. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Øvrevik, J.; Refsnes, M.; Låg, M.; Brinchmann, B.C.; Schwarze, P.E.; Holme, J.A. Triggering Mechanisms and Inflammatory Effects of Combustion Exhaust Particles with Implication for Carcinogenesis. Basic Clin. Pharmacol. Toxicol. 2017, 121, 55–62. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, H.; Kwong, J.C.; Copes, R.; Hystad, P.; van Donkelaar, A.; Tu, K.; Brook, J.R.; Goldberg, M.S.; Martin, R.V.; Murray, B.J.; et al. Exposure to ambient air pollution and the incidence of dementia: A population-based cohort study. Environ. Int. 2017, 108, 271–277. [Google Scholar] [CrossRef] [PubMed]
- Takaki, J. Associations of job stress indicators with oxidative biomarkers in Japanese men and women. Int. J. Environ. Res. Public Health 2013, 10, 6662–6671. [Google Scholar] [CrossRef] [PubMed]
- Blackburn, E.H.; Epel, E.S. Telomeres and adversity: Too toxic to ignore. Nature 2012, 490, 169–171. [Google Scholar] [CrossRef] [PubMed]
- Dean, S.G.; Zhang, C.; Gao, J.; Roy, S.; Shinkle, J.; Sabarinathan, M.; Argos, M.; Tong, L.; Ahmed, A.; Islam, M.T.; et al. The association between telomere length and mortality in Bangladesh. Aging 2017, 9, 1537–1548. [Google Scholar] [CrossRef] [PubMed]
- Pikarsky, E.; Porat, R.M.; Stein, I.; Abramovitch, R.; Amit, S.; Kasem, S.; Gutkovich-Pyest, E.; Urieli-Shoval, S.; Galun, E.; Ben-Neriah, Y. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004, 431, 461–466. [Google Scholar] [CrossRef] [PubMed]
- Mantovani, A.; Allavena, P.; Sica, A.; Balkwill, F. Cancer-related inflammation. Nature 2008, 454, 436–444. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Voronov, E.; Shouval, D.S.; Krelin, Y.; Cagnano, E.; Benharroch, D.; Iwakura, Y.; Dinarello, C.A.; Apte, R.N. IL-1 is required for tumour invasiveness and angiogenesis. Proc. Natl. Acad. Sci. USA 2003, 100, 2645–2650. [Google Scholar] [CrossRef] [PubMed]
- Ross, R. Atherosclerosis is an inflammatory disease. Am. Heart J. 1999, 138, S419–S420. [Google Scholar] [CrossRef]
- Gidron, Y.; Kupper, N.; Kwaijtaal, M.; Winter, J.; Denollet, J. Vagus-brain communication in atherosclerosis-related inflammation: A neuroimmunomodulation perspective of CAD. Atherosclerosis 2007, 195, e1–e9. [Google Scholar] [CrossRef] [PubMed]
- Su, B.; Liu, T.; Fan, H.; Chen, F.; Ding, H.; Wu, Z.; Wang, H.; Hou, S. Inflammatory Markers and the Risk of Chronic Obstructive Pulmonary Disease: A Systematic Review and Meta-Analysis. PLoS ONE 2016, 11, e0150586. [Google Scholar] [CrossRef] [PubMed]
- Shoelson, S.E.; Lee, J.; Goldfine, A.B. Inflammation and insulin resistance. J. Clin. Investig. 2006, 116, 1793–1801. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maes, M.; Song, C.; Lin, A.; de Jongh, R.; van Gastel, A.; Kenis, G.; Bosmans, E.; de Meester, I.; Benoy, I.; Neels, H.; et al. The effects of psychological stress on humans: Increased production of pro-inflammatory cytokines and a Th1-like response in stress-induced anxiety. Cytokine 1998, 10, 313–318. [Google Scholar] [CrossRef] [PubMed]
- Remme, W.J. The sympathetic nervous system and ischaemic heart disease. Eur. Heart J. 1998, 19, F62–F71. [Google Scholar] [PubMed]
- Entschladen, F.; Drell, T.L.; Lang, K.; Joseph, J.; Zaenker, K.S. Tumour-cell migration, invasion, and metastasis: Navigation by neurotransmitters. Lancet Oncol. 2004, 5, 254–258. [Google Scholar] [CrossRef]
- Andreas, S.; Haarmann, H.; Klarner, S.; Hasenfuss, G.; Raupach, T. Increased sympathetic nerve activity in COPD is associated with morbidity and mortality. Lung 2014, 192, 235–241. [Google Scholar] [CrossRef] [PubMed]
- Yufu, K.; Okada, N.; Ebata, Y.; Murozono, Y.; Shinohara, T.; Nakagawa, M.; Takahashi, N. Plasma norepinephrine is an independent predictor of adverse cerebral and cardiovascular events in type 2 diabetic patients without structural heart disease. J. Cardiol. 2014, 64, 225–230. [Google Scholar] [CrossRef] [PubMed]
- Wojciechowska, J.; Krajewski, W.; Bolanowski, M.; Kręcicki, T.; Zatoński, T. Diabetes and Cancer: A Review of Current Knowledge. Exp. Clin. Endocrinol. Diabetes 2016, 124, 263–275. [Google Scholar] [CrossRef] [PubMed]
- Idris, M.A.; Dollard, M.F.; Winefield, A.H. The effect of globalization on employee psychological health and job satisfaction in Malaysian workplaces. J. Occup. Health 2011, 53, 447–454. [Google Scholar] [CrossRef] [PubMed]
- Evans, G.W.; Carrère, S. Traffic congestion, perceived control, and psychophysiological stress among urban bus drivers. J. Appl. Psychol. 1991, 76, 658–663. [Google Scholar] [CrossRef] [PubMed]
- Dadgar, I.; Norström, T. Short-term and long-term effects of GDP on traffic deaths in 18 OECD countries, 1960–2011. J. Epidemiol. Community Health 2017, 71, 146–153. [Google Scholar] [CrossRef] [PubMed]
- Kuo, T.B.; Lai, C.J.; Huang, Y.T.; Yang, C.C. Regression analysis between heart rate variability and baroreflex-related vagus nerve activity in rats. J. Cardiovasc. Electrophysiol. 2005, 16, 864–869. [Google Scholar] [CrossRef] [PubMed]
- Weber, C.S.; Thayer, J.F.; Rudat, M.; Wirtz, P.H.; Zimmermann-Viehoff, F.; Thomas, A.; Perschel, F.H.; Arck, P.C.; Deter, H.C. Low vagal tone is associated with impaired post stress recovery of cardiovascular, endocrine, and immune markers. Eur. J. Appl. Physiol. 2010, 109, 201–211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ohira, H.; Matsunaga, M.; Osumi, T.; Fukuyama, S.; Shinoda, J.; Yamada, J.; Gidron, Y. Vagal nerve activity as a moderator of brain-immune relationships. J. Neuroimmunol. 2013, 260, 28–36. [Google Scholar] [CrossRef] [PubMed]
- Licht, C.M.; Vreeburg, S.A.; van Reedt Dortland, A.K.; Giltay, E.J.; Hoogendijk, W.J.; DeRijk, R.H.; Vogelzangs, N.; Zitman, F.G.; de Geus, E.J.; Penninx, B.W. Increased sympathetic and decreased parasympathetic activity rather than changes in hypothalamic-pituitary-adrenal axis activity is associated with metabolic abnormalities. J. Clin. Endocrinol. Metab. 2010, 95, 2458–2466. [Google Scholar] [CrossRef] [PubMed]
- Dekker, J.M.; Schouten, E.G.; Klootwijk, P.; Pool, J.; Swenne, C.A.; Kromhout, D. Heart rate variability from short electrocardiographic recordings predicts mortality from all causes in middle-aged and elderly men. The Zutphen Study. Am. J. Epidemiol. 1997, 145, 899–908. [Google Scholar] [CrossRef] [PubMed]
- Buccelletti, E.; Gilardi, E.; Scaini, E.; Galiuto, L.; Persiani, R.; Biondi, A.; Basile, F.; Silveri, N.G. Heart rate variability and myocardial infarction: Systematic literature review and metanalysis. Eur. Rev. Med. Pharmacol. Sci. 2009, 13, 299–307. [Google Scholar]
- Zhou, X.; Ma, Z.; Zhang, L.; Zhou, S.; Wang, J.; Wang, B.; Fu, W. Heart rate variability in the prediction of survival in patients with cancer: A systematic review and meta-analysis. J. Psychosom. Res. 2016, 89, 20–25. [Google Scholar] [CrossRef] [PubMed]
- De Couck, M.D.; Maréchal, R.; Moorthamers, S.; Laethem, J.-L.V.; Gidron, Y. Vagal nerve activity predicts overall survival in metastatic pancreatic cancer, mediated by inflammation. Cancer Epidemiol. 2016, 40, 47–51. [Google Scholar] [CrossRef] [PubMed]
- Perugini, R.A.; Li, Y.; Rosenthal, L.; Gallagher-Dorval, K.; Kelly, J.J.; Czerniach, D.R. Reduced heart rate variability correlates with insulin resistance but not with measures of obesity in population undergoing laparoscopic Roux-en-Y gastric bypass. Surg. Obes. Relat. Dis. 2010, 6, 237–241. [Google Scholar] [CrossRef] [PubMed]
- Bissinger, A.; Ruxer, J.; Ahmed, R.B.; Lubinski, A. Heart rate turbulence in patients with poorly controlled diabetes mellitus type 2. Arch. Med. Sci. 2014, 10, 1073–1077. [Google Scholar] [CrossRef] [PubMed]
- Handa, R.; Poanta, L.; Rusu, D.; Albu, A. The role of heart rate variability in assessing the evolution of patients with chronic obstructive pulmonary disease. Rom. J. Intern. Med. 2012, 50, 83–88. [Google Scholar] [PubMed]
- Tsutsumi, T.; Ide, T.; Yamato, M.; Kudou, W.; Andou, M.; Hirooka, Y.; Utsumi, H.; Tsutsui, H.; Sunagawa, K. Modulation of the myocardial redox state by vagal nerve stimulation after experimental myocardial infarction. Cardiovasc. Res. 2008, 77, 713–721. [Google Scholar] [CrossRef] [PubMed]
- Bezerra, O.C.; França, C.M.; Rocha, J.A.; Neves, G.A.; Souza, P.R.M.; Teixeira Gomes, M.; Malfitano, C.; Loleiro, T.C.A.; Dourado, P.M.; Llesuy, S.; et al. Cholinergic stimulation improves oxidative stress and inflammation in experimental myocardial infarction. Sci. Rep. 2017, 7, 13687. [Google Scholar] [CrossRef] [PubMed]
- Ek, M.; Kurosawa, M.; Lundeberg, T.; Ericsson, A. Activation of vagal afferents after intravenous injection of interleukin-1beta: Role of endogenous prostaglandins. J. Neurosci. 1998, 18, 9471–9479. [Google Scholar] [CrossRef] [PubMed]
- Tracey, K.J. Reflex control of immunity. Nat. Rev. Immunol. 2009, 9, 418–428. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rosas-Ballina, M.; Olofsson, P.S.; Ochani, M.; Valdés-Ferrer, S.I.; Levine, Y.A.; Reardon, C.; Tusche, M.W.; Pavlov, V.A.; Andersson, U.; Chavan, S.; et al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 2011, 334, 98–101. [Google Scholar] [CrossRef] [PubMed]
- Saku, K.; Kishi, T.; Sakamoto, K.; Hosokawa, K.; Sakamoto, T.; Murayama, Y.; Kakino, T.; Ikeda, M.; Ide, T.; Sunagawa, K. Afferent vagal nerve stimulation resets baroreflex neural arc and inhibits sympathetic nerve activity. Physiol. Rep. 2014, 2, e12136. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Feliciano, L.; Henning, R.J. Vagal nerve stimulation releases vasoactive intestinal peptide which significantly increases coronary artery blood flow. Cardiovasc. Res. 1998, 40, 45–55. [Google Scholar] [CrossRef] [Green Version]
- Vaupel, P.; Mayer, A. Hypoxia in cancer: Significance and impact on clinical outcome. Cancer Metastasis Rev. 2007, 26, 225–239. [Google Scholar] [CrossRef] [PubMed]
- McGarry, T.; Biniecka, M.; Veale, D.J.; Fearon, U. Hypoxia, oxidative stress and inflammation. Free Radic. Biol. Med. 2018, 125, 15–24. [Google Scholar] [CrossRef] [PubMed]
- Bodin, F.; McIntyre, K.M.; Schwartz, J.E.; McKinley, P.S.; Cardetti, C.; Shapiro, P.A.; Gorenstein, E.; Sloan, R.P. The Association of Cigarette Smoking with High-Frequency Heart Rate Variability: An Ecological Momentary Assessment Study. Psychosom. Med. 2017, 79, 1045–1050. [Google Scholar] [CrossRef] [PubMed]
- Holzman, J.B.; Bridgett, D.J. Heart rate variability indices as bio-markers of top-down self-regulatory mechanisms: A meta-analytic review. Neurosci. Biobehav. Rev. 2017, 74, 233–255. [Google Scholar] [CrossRef] [PubMed]
- Riggs, N.R.; Huh, J.; Chou, C.P.; Spruijt-Metz, D.; Pentz, M.A. Executive function and latent classes of childhood obesity risk. J. Behav. Med. 2012, 35, 642–650. [Google Scholar] [CrossRef] [PubMed]
- Hall, P.A.; Fong, G.T.; Epp, L.J.; Elias, L.J. Executive function moderates the intention-behavior link for physical activity and dietary behavior. Psychol. Health 2008, 23, 309–326. [Google Scholar] [CrossRef] [PubMed]
- Kraus, T.; Hösl, K.; Kiess, O.; Schanze, A.; Kornhuber, J.; Forster, C. BOLD fMRI deactivation of limbic and temporal brain structures and mood enhancing effect by transcutaneous vagus nerve stimulation. J. Neural Transm. 2007, 114, 1485–1493. [Google Scholar] [CrossRef] [PubMed]
- Badran, B.W.; Dowdle, L.T.; Mithoefer, O.J.; LaBate, N.T.; Coatsworth, J.; Brown, J.C.; DeVries, W.H.; Austelle, C.W.; McTeague, L.M.; George, M.S. Neurophysiologic effects of transcutaneous auricular vagus nerve stimulation (taVNS) via electrical stimulation of the tragus: A concurrent taVNS/fMRI study and review. Brain Stimul. 2018, 11, 492–500. [Google Scholar] [CrossRef] [PubMed]
- Ziomber, A.; Juszczak, K.; Kaszuba-Zwoinska, J.; Machowska, A.; Zaraska, K.; Gil, K.; Thor, P. Magnetically induced vagus nerve stimulation and feeding behavior in rats. J. Physiol. Pharmacol. 2009, 60, 71–77. [Google Scholar] [PubMed]
- Meule, A.; Freund, R.; Skirde, A.K.; Vögele, C.; Kübler, A. Heart rate variability biofeedback reduces food cravings in high food cravers. Appl. Psychophysiol. Biofeedback 2012, 37, 241–251. [Google Scholar] [CrossRef] [PubMed]
- Maier, S.U.; Hare, T.A. Higher heart-rate variability is associated with ventromedial prefrontal cortex activity and increased resistance to temptation in dietary self-control challenges. J. Neurosci. 2017, 37, 446–455. [Google Scholar] [CrossRef] [PubMed]
- Martinmäki, K.; Rusko, H. Time-frequency analysis of heart rate variability during immediate recovery from low and high intensity exercise. Eur. J. Appl. Physiol. 2008, 102, 353–360. [Google Scholar] [CrossRef] [PubMed]
- Silberstein, S.D.; Mechtler, L.L.; Kudrow, D.B.; Calhoun, A.H.; McClure, C.; Saper, J.R.; Liebler, E.J.; Rubenstein Engel, E.; Tepper, S.J.; ACT1 Study Group. Non-Invasive Vagus Nerve Stimulation for the ACute Treatment of Cluster Headache: Findings from the Randomized, Double-Blind, Sham-Controlled ACT1 Study. Headache 2016, 56, 1317–1332. [Google Scholar] [CrossRef] [PubMed]
- Lerman, I.; Hauger, R.; Sorkin, L.; Proudfoot, J.; Davis, B.; Huang, A.; Lam, K.; Simon, B.; Baker, D.G. Noninvasive Transcutaneous Vagus Nerve Stimulation Decreases Whole Blood Culture-Derived Cytokines and Chemokines: A Randomized, Blinded, Healthy Control Pilot Trial. Neuromodulation 2016, 19, 283–290. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hein, E.; Nowak, M.; Kiess, O.; Biermann, T.; Bayerlein, K.; Kornhuber, J.; Kraus, T. Auricular transcutaneous electrical nerve stimulation in depressed patients: A randomized controlled pilot study. J. Neural Transm. 2013, 120, 821–827. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.; Zhai, X.; Li, S.; McCabe, M.F.; Wang, X.; Rong, P. Transcutaneous vagus nerve stimulation induces tidal melatonin secretion and has an antidiabetic effect in Zucker fatty rats. PLoS ONE 2015, 10, e0124195. [Google Scholar] [CrossRef] [PubMed]
- Nolan, R.P.; Floras, J.S.; Ahmed, L.; Harvey, P.J.; Hiscock, N.; Hendrickx, H.; Talbot, D. Behavioural modification of the cholinergic anti-inflammatory response to C-reactive protein in patients with hypertension. J. Intern. Med. 2012, 272, 161–169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- De Couck, M.; de Leeuw, I.; Blase, K.M.; Reiman, E.; van Acker, L.; Gidron, Y. Effects of HRV-biofeedback on the tumor marker CEA in patients with metastatic colon cancer: A controlled pilot study. Manuscript under review.
- Tyagi, A.; Cohen, M. Yoga and heart rate variability: A comprehensive review of the literature. Int. J. Yoga 2016, 9, 97–113. [Google Scholar] [PubMed]
- Miller, I.S.; Didier, S.; Murray, D.W.; Turner, T.H.; Issaivanan, M.; Ruggieri, R.; Al-Abed, Y.; Symons, M. Semapimod sensitizes glioblastoma tumors to ionizing radiation by targeting microglia. PLoS ONE 2014, 9, e95885. [Google Scholar] [CrossRef] [PubMed]
- Arimura, T.; Saku, K.; Kakino, T.; Nishikawa, T.; Tohyama, T.; Sakamoto, T.; Sakamoto, K.; Kishi, T.; Ide, T.; Sunagawa, K. Intravenous electrical vagal nerve stimulation prior to coronary reperfusion in a canine ischemia-reperfusion model markedly reduces infarct size and prevents subsequent heart failure. Int. J. Cardiol. 2017, 227, 704–710. [Google Scholar] [CrossRef] [PubMed]
- Khodaparast, N.; Hays, S.A.; Sloan, A.M.; Fayyaz, T.; Hulsey, D.R.; Rennaker, R.L., II; Kilgard, M.P. Vagus nerve stimulation delivered during motor rehabilitation improves recovery in a rat model of stroke. Neurorehabil. Neural Repair 2014, 28, 698–706. [Google Scholar] [CrossRef] [PubMed]
- Malbert, C.H.; Picq, C.; Divoux, J.L.; Henry, C.; Horowitz, M. Obesity-associated alterations in glucose metabolism are reversed by chronic bilateral stimulation of the abdominal vagus verve. Diabetes 2017, 66, 848–857. [Google Scholar] [CrossRef] [PubMed]
- Pettersson, A.; Nilsson, L.; Nylund, G.; Khorram-Manesh, A.; Nordgren, S.; Delbro, D.S. Is acetylcholine an autocrine/paracrine growth factor via the nicotinic alpha7-receptor subtype in the human colon cancer cell line HT-29? Eur. J. Pharmacol. 2009, 609, 27–33. [Google Scholar] [CrossRef] [PubMed]
- Friedman, J.R.; Richbart, S.D.; Merritt, J.C.; Brown, K.C.; Nolan, N.A.; Akers, A.T.; Lau, J.K.; Robateau, Z.R.; Miles, S.L.; Dasgupta, P. Acetylcholine signaling system in progression of lung cancers. Pharmacol. Ther. 2018. [Google Scholar] [CrossRef] [PubMed]
- Mehlsen, J.; Kaijer, M.N.; Mehlsen, A.B. Autonomic and electrocardiographic changes in cardioinhibitory syncope. Europace 2008, 10, 91–95. [Google Scholar] [CrossRef] [PubMed]
- Park, S.K.; Tucker, K.L.; O’Neill, M.S.; Sparrow, D.; Vokonas, P.S.; Hu, H.; Schwartz, J. Fruit, vegetable, and fish consumption and heart rate variability: The Veterans Administration Normative Aging Study. Am. J. Clin. Nutr. 2009, 89, 778–786. [Google Scholar] [CrossRef] [PubMed]
- Gidron, Y.; Davidson, K.; Bata, I. The short-term effects of a hostility-reduction intervention on male coronary heart disease patients. Health Psychol. 1999, 18, 416–420. [Google Scholar] [CrossRef] [PubMed]
© 2018 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 (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Gidron, Y.; Deschepper, R.; De Couck, M.; Thayer, J.F.; Velkeniers, B. The Vagus Nerve Can Predict and Possibly Modulate Non-Communicable Chronic Diseases: Introducing a Neuroimmunological Paradigm to Public Health. J. Clin. Med. 2018, 7, 371. https://doi.org/10.3390/jcm7100371
Gidron Y, Deschepper R, De Couck M, Thayer JF, Velkeniers B. The Vagus Nerve Can Predict and Possibly Modulate Non-Communicable Chronic Diseases: Introducing a Neuroimmunological Paradigm to Public Health. Journal of Clinical Medicine. 2018; 7(10):371. https://doi.org/10.3390/jcm7100371
Chicago/Turabian StyleGidron, Yori, Reginald Deschepper, Marijke De Couck, Julian F. Thayer, and Brigitte Velkeniers. 2018. "The Vagus Nerve Can Predict and Possibly Modulate Non-Communicable Chronic Diseases: Introducing a Neuroimmunological Paradigm to Public Health" Journal of Clinical Medicine 7, no. 10: 371. https://doi.org/10.3390/jcm7100371
APA StyleGidron, Y., Deschepper, R., De Couck, M., Thayer, J. F., & Velkeniers, B. (2018). The Vagus Nerve Can Predict and Possibly Modulate Non-Communicable Chronic Diseases: Introducing a Neuroimmunological Paradigm to Public Health. Journal of Clinical Medicine, 7(10), 371. https://doi.org/10.3390/jcm7100371