Autonomic dysfunctions in patients with inflammatory bowel disease in clinical remission
Abstract
Introduction and objective The autonomic nervous system, especially the parasympathetic system, has been reported to modulate the immune response in chronic inflammatory disorders. Autonomic dysfunctions have been reported earlier in patients with inflammatory bowel disease; however, the results have been conflicting. We therefore evaluated autonomic functions in patients with inflammatory bowel disease (IBD) in clinical remission.Patients and methods Heart rate variability, a marker of autonomic functions, which included time-domain, frequency-domain, and nonlinear indices (Poincaré plot) was assessed using Nevrokard, version 6.4.0 Slovenia, in 118 patients with IBD (ulcerative colitis [UC] 62, and Crohn's disease [CD] 56) and 58 healthy controls.Results There was no difference in mean of R-R intervals in patients with UC, CD, and healthy controls. Frequency domain indices (absolute values of total power, high-frequency power, and low-frequency power) were lower in patients with UC and CD vs. healthy controls. High-frequency (HFnu) (expressed in normalized units) was significantly lower in UC compared to healthy controls. There was no significant difference in the low-frequency (LFnu) and LF/HF ratio in UC, CD, and healthy controls. Amongst the Poincaré plot indices, while standard deviation of the instantaneous R-R interval variability (SD1nu) was lower in UC and CD vs. healthy controls, there was no significant difference in the long-term R-R interval variability (SD2nu).Conclusions Patients with inflammatory bowel disease have lower autonomic functions. Patients with UC have significantly lower parasympathetic function in comparison to those with CD and healthy controls. These autonomic dysfunctions in patients with IBD may have a bearing on the pathogenesis of IBD.
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Patients with UC have markedly lower autonomic functions compared to those with CD and healthy controls.
“Another study showed that patients with UC have markedly lower autonomic functions in comparison to those with CD and healthy controls (35).”
From Stress triggers flare of inflammatory bowel disease in children and adults (2019) · cites this paper as [35]
Cites
Heart Rate Variability: Standards of Measurement, Physiological Interpretation, and Clinical Use
Electrophysiology, T. F. O. T. E. S. O. C. T. N. A. (1996) · Circulation · doi:10.1161/01.cir.93.5.1043 · Cited by 17,159 · see citing works
Heart rate variability: Standards of measurement, physiological interpretation, and clinical use
Malik, M., Bigger, J. T., Camm, A. J., Kleiger, R. E., Malliani, A., Moss, A. J., & Schwartz, P. J. (1996) · European Heart Journal · doi:10.1093/oxfordjournals.eurheartj.a014868 · Cited by 15,289 · see citing works
Practical Statistics for Medical Research.
Walter, S., & Altman, D. G. (1992) · Biometrics · doi:10.2307/2532320 · Cited by 11,665 · see citing works
Practical Statistics for Medical Research
Altman, D. G. (1990) · doi:10.1201/9780429258589 · Cited by 10,668 · see citing works
Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin
Borovikova, L. V., Ivanova, S., Zhang, M., Yang, H., Botchkina, G. I., Watkins, L. R., Wang, H., Abumrad, N., Eaton, J. W., & Tracey, K. J. (2000) · Nature · doi:10.1038/35013070 · Cited by 4,211 · see citing works
Tracey, K. J. (2002) · Nature · doi:10.1038/nature01321 · Cited by 3,728 · see citing works
Silverberg, M. S., Satsangi, J., Ahmad, T., Arnott, I. D., Bernstein, C. N., Brant, S. R., Caprilli, R., Colombel, J., Gasché, C., Geboes, K., et al. (2005) · Canadian Journal of Gastroenterology · doi:10.1155/2005/269076 · Cited by 3,408 · see citing works
Nicotinic acetylcholine receptor α7 subunit is an essential regulator of inflammation
Wang, H., Yu, M., Ochani, M., Amella, C. A., Tanovic, M., Susarla, S., Li, J. H., Wang, H., Yang, H., Ulloa, L., et al. (2003) · Nature · doi:10.1038/nature01339 · Cited by 3,228 · see citing works
Development of a Crohn's Disease Activity Index
Best, W. R., Becktel, J. M., Singleton, J. W., & Kern, F. (1976) · Gastroenterology · doi:10.1016/s0016-5085(76)80163-1 · Cited by 3,152 · see citing works
Development of a Crohn's disease activity index. National Cooperative Crohn's Disease Study.
Best, W. R., Becktel, J. M., Singleton, J. W., & Kern, F. (1976) · PubMed · Cited by 3,147 · see citing works
Cortisone in Ulcerative Colitis
Truelove, S. C., & Witts, L. J. (1955) · BMJ · doi:10.1136/bmj.2.4947.1041 · Cited by 2,793 · see citing works
Elenkov, I. J., Wilder, R. L., Chrousos, G. P., & Vizi, E. S. (2000) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01470-4 · Cited by 2,252 · see citing works
de Jonge, W. J., van der Zanden, E. P., The, F. O., Bijlsma, M. F., van Westerloo, D. J., Bennink, R. J., Berthoud, H.-R., Uematsu, S., Akira, S., van den Wijngaard, R. M., et al. (2005) · Nature Immunology · doi:10.1038/ni1229 · Cited by 1,074 · see citing works
Pagani, M., Montano, N., Porta, A., Malliani, A., Abboud, F. M., Birkett, C. L., & Somers, V. K. (1997) · Circulation · doi:10.1161/01.cir.95.6.1441 · Cited by 876 · see citing works
Quantitative beat-to-beat analysis of heart rate dynamics during exercise
Tulppo, M. P., Mäkikallio, T. H., Takala, T., Seppänen, T., & Huikuri, H. V. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.1.h244 · Cited by 813 · see citing works
The Natural History of Diabetic Autonomic Neuropathy
Ewing, D. J., Campbell, I. W., & Clarke, B. F. (1980) · QJM · doi:10.1093/oxfordjournals.qjmed.a067610 · Cited by 745 · see citing works
Pharmacological stimulation of the cholinergic antiinflammatory pathway
Bernik, T. R., Friedman, S. G., Ochani, M., DiRaimo, R., Ulloa, L., Yang, H., Sudan, S., Czura, C. J., Ivanova, S. M., & Tracey, K. J. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20011714 · Cited by 529 · see citing works
Ghia, J., Blennerhassett, P. A., Kumar–Ondiveeran, H., Verdu, E. F., & Collins, S. M. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.08.016 · Cited by 404 · see citing works
Matsunaga, K., Klein, T., Friedman, H. P., & Yamamoto, Y. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.11.6518 · Cited by 225 · see citing works
Magro, F., Vieira‐Coelho, M. A., Fraga, S., Serrão, P., Veloso, F. T., Ribeiro, T., & Soares-da-Silva, P. (2002) · Digestive Diseases and Sciences · doi:10.1023/a:1013256629600 · Cited by 206 · see citing works
Heart rate variability in patients with rheumatoid arthritis
Evrengül, H., Dursunoglu, D., Cobankara, V., Polat, B., Seleci, D., Kabukçu, S., Kaftan, A., Semiz, E., & Kilic, M. (2004) · Rheumatology International · doi:10.1007/s00296-003-0357-5 · Cited by 159 · see citing works
Sex specific alterations in autonomic function among patients with irritable bowel syndrome
Tillisch, K., Mayer, E. A., Labus, J. S., Stains, J., Chang, L., & Naliboff, B. D. (2005) · Gut · doi:10.1136/gut.2004.058685 · Cited by 156 · see citing works
Effects of chemical sympathectomy and sensory nerve ablation on experimental colitis in the rat
McCafferty, D., Wallace, J. L., & Sharkey, K. A. (1997) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1997.272.2.g272 · Cited by 152 · see citing works
Focal white-matter lesions in brain of patients with inflammatory bowel disease
Andus, T., Roth, M., Kullmann, F., Caesar, I., Gross, V., Feuerbach, S., Schölmerich, J., Geißler, A., & Held, P. (1995) · The Lancet · doi:10.1016/s0140-6736(95)90013-6 · Cited by 126 · see citing works
The protective effect of the vagus nerve in a murine model of chronic relapsing colitis
Ghia, J., Blennerhassett, P. A., El–Sharkawy, R. T., & Collins, S. M. (2007) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00240.2007 · Cited by 123 · see citing works
Kyösola, K. T., Penttilä, O., & Salaspuro, M. P. (1977) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365527709180942 · Cited by 106 · see citing works
Sympathetic overactivity in active ulcerative colitis: effects of clonidine
Furlan, R., Ardizzone, S., Palazzolo, L., Rimoldi, A., Perego, F., Barbic, F., Bevilacqua, M. T., Vago, L., Porro, G. B., & Malliani, A. (2005) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00442.2005 · Cited by 106 · see citing works
Differentiation Between Crohnʼs Disease and Other Inflammatory Conditions by Electron Microscopy
Dvořàk, A. M., & Silen, W. (1985) · Annals of Surgery · doi:10.1097/00000658-198501000-00008 · Cited by 80 · see citing works
Makharia, G. K., Sachdev, V., Gupta, R., Lal, S., & Pandey, R. M. (2006) · Digestive Diseases and Sciences · doi:10.1007/s10620-006-9527-0 · Cited by 76 · see citing works
Self-citationHoworka, K., Pumprla, J., & Schabmann, A. (1998) · Journal of the Autonomic Nervous System · doi:10.1016/s0165-1838(98)00015-0 · Cited by 71 · see citing works
Laser Doppler flowmetry as a measure of extrinsic colonic innervation in functional bowel disease
Emmanuel, A. V., & Kamm, M. A. (2000) · Gut · doi:10.1136/gut.46.2.212 · Cited by 70 · see citing works
Straub, R. H., Antoniou, E., Zeuner, M., Groß, V., Schölmerich, J., & Andus, T. (1997) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(97)00150-1 · Cited by 67 · see citing works
Ganguli, S. C., Kamath, M. V., Redmond, K., Chen, Y., Irvine, E. J., Collins, S. M., & Tougas, G. H. (2007) · Neurogastroenterology & Motility · doi:10.1111/j.1365-2982.2007.00987.x · Cited by 57 · see citing works
Benjamin, J., Makharia, G. K., Ahuja, V., Kalaivani, M., & Joshi, Y. K. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.1399 · Cited by 55 · see citing works
Self-citationHeart rate variability in human immunodeficiency virus-positive individuals
Mittal, C. M., Wig, N., Mishra, S., & Deepak, K. K. (2003) · International Journal of Cardiology · doi:10.1016/j.ijcard.2003.02.002 · Cited by 53 · see citing works
Self-citationEffect of chronic nicotine administration on trinitrobenzene sulphonic acid-induced colitis
Eliakim, R., Karmeli, F., Rachmilewitz, D., et al. (1998) · European Journal of Gastroenterology & Hepatology · doi:10.1097/00042737-199812000-00006 · Cited by 46 · see citing works
Autonomic cardiovascular regulation in quiescent ulcerative colitis and Crohn's disease
Coruzzi, P., Castiglioni, P., Parati, G., Brambilla, V., Brambilla, L., Gualerzi, M., Cademartiri, F., Franzè, A., Angelis, G. D., Rienzo, M. D., et al. (2007) · European Journal of Clinical Investigation · doi:10.1111/j.1365-2362.2007.01887.x · Cited by 35 · see citing works
Subclinical sympathetic neuropathy appears early in the course of Crohn's disease
Ohlsson, B., Sundkvist, G., & Lindgren, S. C. (2007) · BMC Gastroenterology · doi:10.1186/1471-230x-7-33 · Cited by 31 · see citing works
Mouzas, I., Pallis, A. G., KOCHIADAKIS, G. E., Marketou, M. E., CHLOUVERAKIS, G. I., Melissas, J., Vardas, P. E., & Kouroumalis, E. (2002) · Digestive and Liver Disease · doi:10.1016/s1590-8658(02)80070-6 · Cited by 30 · see citing works
Sympathetic hyperactivity in patients with ulcerative colitis
Maule, S. V., Pierangeli, G., Cevoli, S., Grimaldi, D., Gionchetti, P., Barbara, G., Rizzello, F., Stanghellini, V., Corinaldesi, R., Campieri, M., et al. (2007) · Clinical Autonomic Research · doi:10.1007/s10286-007-0425-0 · Cited by 25 · see citing works
Studies of rectal mucosal catecholamines in ulcerative colitis.
Penttilä, O., Kyösola, K. T., Klinge, E., et al. (1975) · PubMed · Cited by 18 · see citing works
Nemoto, H., Iguchi, H., Ichikawa, Y., et al. (2004) · The Neurologist · doi:10.1097/01.nrl.0000126590.16002.39 · Cited by 16 · see citing works
Severe neurological complications of ulcerative colitis
Druschky, A., Heckmann, J. G., Druschky, K., et al. (2002) · Journal of Clinical Neuroscience · doi:10.1054/jocn.2001.0972 · Cited by 15 · see citing works
Non-invasive cardiac evaluation in patients with systemic lupus erythematosus.
Wranicz, J. K., Cygankiewicz, I., Zielińska, M., et al. (2001) · PubMed · Cited by 11 · see citing works
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Olofsson, P. S., Rosas‐Ballina, M., Levine, Y. A., & Tracey, K. J. (2012) · Immunological Reviews · doi:10.1111/j.1600-065x.2012.01138.x · Cited by 393 · see citing works
Pellissier, S., Dantzer, C., Canini, F., Mathieu, N., & Bonaz, B. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.10.004 · Cited by 198 · see citing works
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Sun, Y., Li, L., Xie, R., Wang, B., Jiang, K., & Cao, H. (2019) · Frontiers in Pediatrics · doi:10.3389/fped.2019.00432 · Cited by 171 · see citing works
Sadowski, A., Dunlap, C., Lacombe, A., & Hanes, D. (2021) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000275 · Cited by 38 · see citing works
“Of the primary outcomes of interest, SDNN (34,42,49,50,55,56), the natural log of SDNN (42), RMSSD (34,42,48–50,53,55,56,58), and pNN50 (34,49,50,53,55) were presented.”
BackgroundInfluential
- Authors
- Sharma, P., Makharia, G. K., Ahuja, V., Dwivedi, S. N., & Deepak, K. K.
- Affiliations
- All India Institute of Medical Sciences (IN)
- Corresponding author
- Deepak, Kishore Kumar
- Venue
- Digestive Diseases and Sciences
- Published
- 2008-08-19
- Volume
- 54
- Issue
- 4
- Pages
- 853-861
- ISSN
- 0163-2116 (ISSN-L)
- 1573-2568
- OpenAlex
- W1979550688
- Cited by
- 64
- References
- 45
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 1 · 2020: 5 · 2019: 2 · 2018: 8 · 2017: 3 · 2016: 4 · 2015: 5 · 2014: 5 · 2013: 3 · 2012: 4
- FWCI
- 2.68
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Digestive Diseases and Sciences (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- inflammatory bowel disease, autonomic dysfunction, heart rate variability, parasympathetic function, ulcerative colitis, Crohn's disease, clinical remission, Poincaré plot, RR interval variability, autonomic nervous system
- MeSH terms
- Adult, Colitis, Ulcerative, Crohn Disease, Cross-Sectional Studies, Female, Heart Rate, Humans, Male, Middle Aged, Time Factors, Case-Control Studies, Nonlinear Dynamics, Autonomic Pathways, Young Adult
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