Vagus nerve stimulation: A new bioelectronics approach to treat rheumatoid arthritis?

Best Practice and Research: Clinical Rheumatology

Volumn 28, Issue 4, 2014, Pages 625-635

  Koopman, F A ^a   Schuurman, P R ^a   Vervoordeldonk, M J ^a   Tak, P P ^a,b,c  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b GLAXOSMITHKLINE   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cholinergic anti inflammatory pathway; Rheumatoid arthritis; Vagus nerve stimulation

Indexed keywords

BUNGAROTOXIN RECEPTOR; CHOLINERGIC RECEPTOR STIMULATING AGENT; NICOTINE; SHORT HAIRPIN RNA;

ANTIINFLAMMATORY ACTIVITY; CHOLINERGIC SYSTEM; CYTOKINE PRODUCTION; DEPRESSION; DISEASE ACTIVITY; DISEASE EXACERBATION; EPILEPSY; EXPERIMENTAL ARTHRITIS; FIBROBLAST; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; RHEUMATOID ARTHRITIS; SYNOVIOCYTE; VAGOTOMY; VAGUS NERVE STIMULATION; ANIMAL; ARTHRITIS, RHEUMATOID; INFLAMMATION; METABOLISM; PROCEDURES;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; ARTHRITIS, RHEUMATOID; HUMANS; INFLAMMATION; VAGUS NERVE STIMULATION;

EID: 84925879871     PISSN: 15216942     EISSN: 15321770     Source Type: Journal    
DOI: 10.1016/j.berh.2014.10.015     Document Type: Review

References (73)

1. McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011;365:2205-19. http://dx.doi.org/10.7748/phc2011.11.21.9.29.c8797.
2. Smolen JS, Landewe R, Breedveld FC, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update. Ann Rheum Dis 2014;73:492-509. http://dx.doi.org/10.1136/annrheumdis-2013-204573. annrheumdis-2013-204573 [pii].
3. Bianchi M, Ulrich P, Bloom O, et al. An inhibitor of macrophage arginine transport and nitric oxide production (CNI-1493) prevents acute inflammation and endotoxin lethality. Mol Med 1995;1:254-66.
4. Watkins LR, Goehler LE, Relton JK, et al. Blockade of interleukin-1 induced hyperthermia by subdiaphragmatic vagotomy: evidence for vagal mediation of immune-brain communication. Neurosci Lett 1995;183:27-31.
5. Borovikova LV, Ivanova S, Nardi D, et al. Role of vagus nerve signaling in CNI-1493-mediated suppression of acute inflammation. Auton Neurosci 2000;85:141-7. http://dx.doi.org/10.1016/S1566-0702(00)00233-2. S1566-0702(00) 00233-2 [pii].
6. Borovikova LV, Ivanova S, Zhang M, et al. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000;405:458-62. http://dx.doi.org/10.1038/35013070.
7. Parrish WR, Rosas-Ballina M, Gallowitsch-Puerta M, et al. Modulation of TNF release by choline requires alpha7 subunit nicotinic acetylcholine receptor-mediated signaling. Mol Med 2008;14:567-74. http://dx.doi.org/10.2119/2008-00079. Parrish.
8. Wang H, Yu M, Ochani M, et al. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003;421:384-8. http://dx.doi.org/10.1038/nature01339. nature01339 [pii].
9. Gigliotti JC, Huang L, Ye H, et al. Ultrasound prevents renal ischemia-reperfusion injury by stimulating the splenic cholinergic anti-inflammatory pathway. J Am Soc Nephrol 2013;24:1451-60. http://dx.doi.org/10.1681/ASN.2013010084. ASN.2013010084 [pii].
10. Huston JM, Ochani M, Rosas-Ballina M, et al. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J Exp Med 2006;203:1623-8. http://dx.doi.org/10.1084/jem.20052362. jem. 20052362 [pii].
11. Huston JM, Rosas-Ballina M, Xue X, et al. Cholinergic neural signals to the spleen down-regulate leukocyte trafficking via CD11b. J Immunol 2009;183:552-9. http://dx.doi.org/10.4049/jimmunol.0802684. 183/1/552 [pii].
12. Ji H, Rabbi MF, Labis B, et al. Central cholinergic activation of a vagus nerve-to-spleen circuit alleviates experimental colitis. Mucosal Immunol 2014;7:335-47. http://dx.doi.org/10.1038/mi.2013.52. mi201352 [pii].
13. Olofsson PS, Katz DA, Rosas-Ballina M, et al. alpha7 nicotinic acetylcholine receptor (alpha7nAChR) expression in bone marrow-derived non-T cells is required for the inflammatory reflex. Mol Med 2012;18:539-43. http://dx.doi.org/10.2119/molmed.2011.00405. molmed.2011.00405 [pii].
14. Rosas-Ballina M, Olofsson PS, Ochani M, et al. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 2011;334:98-101. http://dx.doi.org/10.1126/science.1209985. science.1209985 [pii].
15. Grimsholm O, Rantapaa-Dahlqvist S, Dalen T, et al. Unexpected finding of a marked non-neuronal cholinergic system in human knee joint synovial tissue. Neurosci Lett 2008;442:128-33. http://dx.doi.org/10.1016/j.neulet.2008.06.082. S0304-3940(08)00890-2 [pii].
16. Schubert J, Beckmann J, Hartmann S, et al. Expression of the non-neuronal cholinergic system in human knee synovial tissue from patients with rheumatoid arthritis and osteoarthritis. Life Sci 2012;91:1048-52. http://dx.doi.org/10.1016/j. lfs.2012.04.032. S0024-3205(12)00222-6 [pii].
17. Koopman FA, Stoof SP, Straub RH, et al. Restoring the balance of the autonomic nervous system as an innovative approach to the treatment of rheumatoid arthritis. Mol Med 2011;17:937-48. http://dx.doi.org/10.2119/molmed.2011.00065. molmed.2011.00065 [pii].
18. Bai A, Guo Y, Lu N. The effect of the cholinergic anti-inflammatory pathway on experimental colitis. Scand J Immunol 2007;66:538-45. http://dx.doi.org/10.1111/j.1365-3083.2007.02011.x. SJI2011 [pii].
19. Mabley J, Gordon S, Pacher P. Nicotine exerts an anti-inflammatory effect in a murine model of acute lung injury. Inflammation 2011;34:231-7. http://dx.doi.org/10.1007/s10753-010-9228-x.
20. The F, Cailotto C, van d V, et al. Central activation of the cholinergic anti-inflammatory pathway reduces surgical inflammation in experimental post-operative ileus. Br J Pharmacol 2011;163:1007-16. http://dx.doi.org/10.1111/j.1476- 5381.2011.01296.x.
21. van Westerloo DJ, Giebelen IA, Florquin S, et al. The vagus nerve and nicotinic receptors modulate experimental pancreatitis severity in mice. Gastroenterology 2006;130:1822-30. http://dx.doi.org/10.1053/j.gastro.2006.02.022. S0016-5085(06)00285-X [pii].
22. Van Maanen MA, Lebre MC, van der Poll T, et al. Stimulation of nicotinic acetylcholine receptors attenuates collageninduced arthritis in mice. Arthritis Rheum 2009;60:114-22. http://dx.doi.org/10.1002/art.24177.
23. Li T, Zuo X, Zhou Y, et al. The vagus nerve and nicotinic receptors involve inhibition of HMGB1 release and early proinflammatory cytokines function in collagen-induced arthritis. J Clin Immunol 2010;30:213-20. http://dx.doi.org/10.1007/s10875-009-9346-0.
24. Hu Y, Liu R, Li J, et al. Attenuation of collagen-induced arthritis in rat by nicotinic Alpha7 receptor partial agonist GTS-21. Biomed Res Int 2014. http://dx.doi.org/10.1155/2014/325875. 325875.
25. Van Maanen MA, Stoof SP, LaRosa GJ, et al. Role of the cholinergic nervous system in rheumatoid arthritis: aggravation of arthritis in nicotinic acetylcholine receptor alpha7 subunit gene knockout mice. Ann Rheum Dis 2010;69:1717-23. http://dx.doi.org/10.1136/ard.2009.118554. ard.2009.118554 [pii].
26. de Jonge WJ, Ulloa L. The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol 2007;151:915-29. http://dx.doi.org/10.1038/sj.bjp.0707264. 0707264 [pii].
27. Van Maanen MA, Stoof SP, van der Zanden EP, et al. The alpha7 nicotinic acetylcholine receptor on fibroblast-like synoviocytes and in synovial tissue from rheumatoid arthritis patients: a possible role for a key neurotransmitter in synovial inflammation. Arthritis Rheum 2009;60:1272-81. http://dx.doi.org/10.1002/art.24470.
28. Waldburger JM, Boyle DL, Pavlov VA, et al. Acetylcholine regulation of synoviocyte cytokine expression by the alpha7 nicotinic receptor. Arthritis Rheum 2008;58:3439-49. http://dx.doi.org/10.1002/art.23987.
29. Zhou Y, Zuo X, Li Y, et al. Nicotine inhibits tumor necrosis factor-alpha induced IL-6 and IL-8 secretion in fibroblast-like synoviocytes from patients with rheumatoid arthritis. Rheumatol Int 2012;32:97-104. http://dx.doi.org/10.1007/s00296- 010-1549-4.
30. Rosas-Ballina M, Goldstein RS, Gallowitsch-Puerta M, et al. The selective alpha7 agonist GTS-21 attenuates cytokine production in human whole blood and human monocytes activated by ligands for TLR2, TLR3, TLR4, TLR9, and RAGE. Mol Med 2009;15:195-202. http://dx.doi.org/10.2119/molmed.2009.00039.
31. Zhang P, Han D, Tang T, et al. Inhibition of the development of collagen-induced arthritis in Wistar rats through vagus nerve suspension: a 3-month observation. Inflamm Res 2008;57:322-8. http://dx.doi.org/10.1007/s00011-008- 8070-1.
32. Levine YA, Koopman FA, Faltys M, et al. Neurostimulation of the cholinergic anti-inflammatory pathway ameliorates disease in rat collagen-induced arthritis. PLoS One 2014;9:e104530. http://dx.doi.org/10.1371/journal.pone.0104530. PONE-D-14-09205 [pii].
33. de Hair MJ, Landewe RB, van de Sande MG, et al. Smoking and overweight determine the likelihood of developing rheumatoid arthritis. Ann Rheum Dis 2013;72:1654-8. http://dx.doi.org/10.1136/annrheumdis-2012-202254. annrheumdis- 2012-202254 [pii].
34. Carlens C, Hergens MP, Grunewald J, et al. Smoking, use of moist snuff, and risk of chronic inflammatory diseases. Am J Respir Crit Care Med 2010;181:1217-22. http://dx.doi.org/10.1164/rccm.200909-1338OC. 200909-1338OC [pii].
35. Klareskog L, Malmstrom V, Lundberg K, et al. Smoking, citrullination and genetic variability in the immunopathogenesis of rheumatoid arthritis. Semin Immunol 2011;23:92-8. http://dx.doi.org/10.1016/j.smim.2011.01.014. S1044-5323(11) 00015-7 [pii].
36. Fisher MC, Hochberg MC, El-Taha M, et al. Smoking, smoking cessation, and disease activity in a large cohort of patients with rheumatoid arthritis. J Rheumatol 2012;39:904-9. http://dx.doi.org/10.3899/jrheum.110852. jrheum. 110852 [pii].
37. Papadopoulos NG, Alamanos Y, Voulgari PV, et al. Does cigarette smoking influence disease expression, activity and severity in early rheumatoid arthritis patients? Clin Exp Rheumatol 2005;23:861-6. 1724 [pii].
38. Soderlin MK, Petersson IF, Bergman S, et al. Smoking at onset of rheumatoid arthritis (RA) and its effect on disease activity and functional status: experiences from BARFOT, a long-term observational study on early RA. Scand J Rheumatol 2011; 40:249-55. http://dx.doi.org/10.3109/03009742.2010.541495.
39. Harrison BJ, Silman AJ, Wiles NJ, et al. The association of cigarette smoking with disease outcome in patients with early inflammatory polyarthritis. Arthritis Rheum 2001;44:323-30. http://dx.doi.org/10.1002/1529-0131(200102)44.2323::AID-ANR493.0.CO;2-C
40. Lu B, Rho YH, Cui J, et al. Associations of smoking and alcohol consumption with disease activity and functional status in rheumatoid arthritis. J Rheumatol 2014;41:24-30. http://dx.doi.org/10.3899/jrheum.130074. jrheum.130074 [pii].
41. Vesperini V, Lukas C, Fautrel B, et al. Association of tobacco exposure and reduction of radiographic progression in early rheumatoid arthritis: results from a French multicenter cohort. Arthritis Care Res (Hoboken) 2013;65:1899-906. http://dx.doi.org/10.1002/acr.22057.
42. Westhoff G, Rau R, Zink A. Rheumatoid arthritis patients who smoke have a higher need for DMARDs and feel worse, but they do not have more joint damage than non-smokers of the same serological group. Rheumatology (Oxford) 2008;47: 849-54. http://dx.doi.org/10.1093/rheumatology/ken057. ken057 [pii].
43. Canhao H, Rodrigues AM, Mourao AF, et al. Comparative effectiveness and predictors of response to tumour necrosis factor inhibitor therapies in rheumatoid arthritis. Rheumatology (Oxford) 2012;51:2020-6. http://dx.doi.org/10.1093/rheumatology/kes184. kes184 [pii].
44. Rojas-Serrano J, Perez LL, Garcia CG, et al. Current smoking status is associated to a non-ACR 50 response in early rheumatoid arthritis. A cohort study. Clin Rheumatol 2011;30:1589-93. http://dx.doi.org/10.1007/s10067-011-1775-5.
45. Soderlin MK, Petersson IF, Geborek P. The effect of smoking on response and drug survival in rheumatoid arthritis patients treated with their first anti-TNF drug. Scand J Rheumatol 2012;41:1-9. http://dx.doi.org/10.3109/03009742.2011. 599073.
46. Andersson ML, Bergman S, Soderlin MK. The effect of snuff (smokeless tobacco) on disease activity and function in rheumatoid arthritis: experiences from the Better Anti-Rheumatic FarmacOTherapy, a longitudinal multicenter study on early rheumatoid arthritis. J Clin Rheumatol 2013;19:14-8. http://dx.doi.org/10.1097/RHU.0b013e31828214ed. 00124743- 201301000-00003 [pii].
47. Jiang X, Alfredsson L, Klareskog L, et al. Smokeless tobacco (moist snuff) use and the risk of developing rheumatoid arthritis: results from the Swedish Epidemiological Investigation of Rheumatoid Arthritis (EIRA) case-control study. Arthritis Care Res (Hoboken) 2014. http://dx.doi.org/10.1002/acr.22325.
48. Martin-Martinez MA, Gonzalez-Juanatey C, Castaneda S, et al. Recommendations for the management of cardiovascular risk in patients with rheumatoid arthritis: scientific evidence and expert opinion. Semin Arthritis Rheum 2014. http://dx. doi.org/10.1016/j.semarthrit.2014.01.002. S0049-0172(14)00003-1 [pii].
49. Albano SA, Santana-Sahagun E, Weisman MH. Cigarette smoking and rheumatoid arthritis. Semin Arthritis Rheum 2001; 31:146-59. http://dx.doi.org/10.1053/sarh.2001.27719. S0049-0172(01)56332-5 [pii].
50. Camm AJ, Malik M. Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation 1996;93:1043-65.
51. Aydemir M, Yazisiz V, Basarici I, et al. Cardiac autonomic profile in rheumatoid arthritis and systemic lupus erythematosus. Lupus 2010;19:255-61. http://dx.doi.org/10.1177/0961203309351540. 0961203309351540 [pii].
52. Bruchfeld A, Goldstein RS, Chavan S, et al. Whole blood cytokine attenuation by cholinergic agonists ex vivo and relationship to vagus nerve activity in rheumatoid arthritis. J Intern Med 2010;268:94-101. http://dx.doi.org/10.1111/j.1365- 2796.2010.02226.x. JIM2226 [pii].
53. Evrengul H, Dursunoglu D, Cobankara V, et al. Heart rate variability in patients with rheumatoid arthritis. Rheumatol Int 2004;24:198-202. http://dx.doi.org/10.1007/s00296-003-0357-5.
54. Borman P, Gokoglu F, Kocaoglu S, et al. The autonomic dysfunction in patients with ankylosing spondylitis: a clinical and electrophysiological study. Clin Rheumatol 2008;27:1267-73. http://dx.doi.org/10.1007/s10067-008-0906-0.
55. Sharma P, Makharia GK, Ahuja V, et al. Autonomic dysfunctions in patients with inflammatory bowel disease in clinical remission. Dig Dis Sci 2009;54:853-61. http://dx.doi.org/10.1007/s10620-008-0424-6.
56. Routledge FS, Campbell TS, McFetridge-Durdle JA, et al. Improvements in heart rate variability with exercise therapy. Can J Cardiol 2010;26:303-12.
57. Khattab K, Khattab AA, Ortak J, et al. Iyengar yoga increases cardiac parasympathetic nervous modulation among healthy yoga practitioners. Evid Based Complement Altern Med 2007;4:511-7. http://dx.doi.org/10.1093/ecam/nem087.
58. Nesvold A, Fagerland MW, Davanger S, et al. Increased heart rate variability during nondirective meditation. Eur J Prev Cardiol 2012;19:773-80. http://dx.doi.org/10.1177/1741826711414625. 1741826711414625 [pii].
59. Kulur AB, Haleagrahara N, Adhikary P, et al. Effect of diaphragmatic breathing on heart rate variability in ischemic heart disease with diabetes. Arq Bras Cardiol 2009;92:423-7. 457. S0066-782X2009000600008 [pii].
60. Chung JW, Yan VC, Zhang H. Effect of acupuncture on heart rate variability: a systematic review. Evid Based Complement Altern Med 2014. http://dx.doi.org/10.1155/2014/819871. 819871.
61. Holman AJ, Ng E. Heart rate variability predicts anti-tumor necrosis factor therapy response for inflammatory arthritis. Auton Neurosci 2008;143:58-67. http://dx.doi.org/10.1016/j.autneu.2008.05.005. S1566-0702(08)00071-4 [pii].
62. Scherrmann J, Hoppe C, Kral T, et al. Vagus nerve stimulation: clinical experience in a large patient series. J Clin Neurophysiol 2001;18:408-14.
63. O'Reardon JP, Cristancho P, Peshek AD. Vagus nerve stimulation (VNS) and treatment of depression: to the Brainstem and beyond. Psychiatry (Edgmont) 2006;3:54-63.
64. Greg Browne. Cyberonics announces 100, 000th patient implant of VNS Therapy®. 2012.
65. Ben-Menachem E. Vagus nerve stimulation, side effects, and long-term safety. J Clin Neurophysiol 2001;18:415-8.
66. DeGiorgio CM, Thompson J, Lewis P, et al. Vagus nerve stimulation: analysis of device parameters in 154 patients during the long-term XE5 study. Epilepsia 2001;42:1017-20. epi08101 [pii].
67. Felson DT, Anderson JJ, Boers M, et al. American College of Rheumatology. Preliminary definition of improvement in rheumatoid arthritis. Arthritis Rheum 1995;38:727-35.
68. NCT01552941. Clinical trial registration - safety and efficacy vagal nerve stimulation in patients with rheumatoid arthritis. 2013.
69. Koopman FA, Miljko S, Grazio S, et al. Pilot study of stimulation of the cholinergic anti-inflammatory pathway with an implantable vagus nerve stimulation device in patients with rheumatoid arthritis. Arthritis Rheum 2012;64(Suppl.).
70. Anonymous. VNS Therapy® System Physician's Manual - chapter: MRI with the VNS Therapy® System. 2014.
71. Sperling W, Reulbach U, Kornhuber J. Clinical benefits and cost effectiveness of vagus nerve stimulation in a long-term treatment of patients with major depression. Pharmacopsychiatry 2009;42:85-8. http://dx.doi.org/10.1055/s-0028- 1103294.
72. Schabert VF, Watson C, Joseph GJ, et al. Costs of tumor necrosis factor blockers per treated patient using real-world drug data in a managed care population. J Manag Care Pharm 2013;19:621-30. 2013(19)8: 621-630 [pii].
73. Tak PP, Kalden JR. Advances in rheumatology: new targeted therapeutics. Arthritis Res Ther 2011;13(Suppl. 1):S5. http://dx.doi.org/10.1186/1478-6354-13-S1-S5. 1478-6354-13-S1-S5 [pii].