Spinal cord injury-induced immune deficiency syndrome enhances infection susceptibility dependent on lesion level

Brain

Volumn 139, Issue 3, 2016, Pages 692-707

  Brommer, Benedikt ^a,b   Engel, Odilo ^a   Kopp, Marcel A ^a   Watzlawick, Ralf ^a   Müller, Susanne ^a   Prüss, Harald ^a,c   Chen, Yuying ^d   DeVivo, Michael J ^d   Finkenstaedt, Felix W ^a   Dirnagl, Ulrich ^a,c   Liebscher, Thomas ^e   Meisel, Andreas ^a   Schwab, Jan M ^a,f  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d University of Alabama at Birmingham   (United States)

^e Trauma Hospital Berlin   (Germany)

^f THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Mechanisms; Myelopathy; Neuroinflammation; Rehabilitation; Spinal cord injury

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; COHORT ANALYSIS; CONTROLLED STUDY; DENERVATION; EXPERIMENTAL PNEUMONIA; EXPERIMENTAL SPINAL CORD INJURY; HUMAN; IMMUNE DEFICIENCY; INFECTION RISK; INFECTION SENSITIVITY; MAJOR CLINICAL STUDY; MALE; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PNEUMOCOCCAL INFECTION; POSTGANGLIONIC NERVE; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; RISK FACTOR; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; SPINAL CORD INJURY INDUCED IMMUNE DEFICIENCY SYNDROME; SPLEEN; SYMPATHETIC INNERVATION; THORACIC SPINAL CORD; ANIMAL; C57BL MOUSE; COMPLICATION; DISEASE PREDISPOSITION; IMMUNOLOGIC DEFICIENCY SYNDROMES; INJURIES; PATHOLOGY; THORACIC VERTEBRA;

ANIMALS; DISEASE SUSCEPTIBILITY; IMMUNOLOGIC DEFICIENCY SYNDROMES; MALE; MICE; MICE, INBRED C57BL; SPINAL CORD INJURIES; THORACIC VERTEBRAE;

EID: 84964587194     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awv375     Document Type: Article

References (48)

1. Ankeny DP, Lucin KM, Sanders VM, McGaughy VM, Popovich PG. Spinal cord injury triggers systemic autoimmunity: evidence for chronic B lymphocyte activation and lupus-like autoantibody synthesis. J Neurochem 2006;99:1073-87.
2. Bellinger DL, Millar BA, Perez S, Carter J, Wood C, ThyagaRajan S, et al. Sympathetic modulation of immunity: relevance to disease. Cell Immunol 2008;252:27-56.
3. Berlly M, Shem K. Respiratory management during the first five days after spinal cord injury. J Spinal Cord Med 2007;30:309-18.
4. Campagnolo DI, Bartlett JA, Keller SE, Sanchez W, Oza R. Impaired phagocytosis of Staphylococcus aureus in complete tetraplegics. Am J Phys Med Rehabil 1997;76:276-80.
5. Candiani G, Abbondi M, Borgonovi M, Williams R. Experimental lobar pneumonia due to penicillin-susceptible and penicillin-resistant Streptococcus pneumoniae in immunocompetent and neutropenic rats: efficacy of penicillin and teicoplanin treatment. J Antimicrob Chemother 1997;39:199-207.
6. Cruse JM, Lewis RE, Bishop GR, Kliesch WF, Gaitan E. Neuroendocrine-immune interactions associated with loss and restoration of immune system function in spinal cord injury and stroke patients. Immunol Res 1992;11:104-16.
7. Dembowsky K, Czachurski J, Amendt K, Seller H. Tonic descending inhibition of the spinal somato-sympathetic reflex from the lower brain stem. J Auton Nerv Syst 1980;2:157-82.
8. Desborough JP. The stress response to trauma and surgery. Br J Anaesth 2000;85:109-17.
9. DeVivo MJ, Black KJ, Stover SL. Causes of death during the first 12 years after spinal cord injury. Arch Phys Med Rehabil 1993;74:248-54.
10. DeVivo MJ, Go BK, Jackson AB. Overview of the national spinal cord injury statistical center database. J Spinal Cord Med 2002;25:335-8.
11. DeVivo MJ, Kartus PL, Stover SL, Rutt RD, Fine PR. Cause of death for patients with spinal cord injuries. Arch Intern Med 1989;149:1761-6.
12. Elenkov IJ, Wilder RL, Chrousos GP, Vizi ES. The sympathetic nerve - an integrative interface between two supersystems: the brain and the immune system. Pharmacol Rev 2000;52:595-638.
13. Elm von E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007;370:1453-7.
14. Failli V, Kopp MA, Gericke C, Martus P, Klingbeil S, Brommer B, et al. Functional neurological recovery after spinal cord injury is impaired in patients with infections. Brain 2012;135:3238-50.
15. ∗Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods 2007;39:175-91.
16. Fawcett JW, Curt A, Steeves JD, Coleman WP, Tuszynski MH, Lammertse D, et al. Guidelines for the conduct of clinical trials for spinal cord injury as developed by the ICCP panel: spontaneous recovery after spinal cord injury and statistical power needed for therapeutic clinical trials. Spinal Cord 2007;45:190-205.
17. Felten DL, Ackerman KD, Wiegand SJ, Felten SY. Noradrenergic sympathetic innervation of the spleen: I. Nerve fibers associate with lymphocytes and macrophages in specific compartments of the splenic white pulp. J Neurosci Res 1987;18:28-36.
18. Furlan JC, Krassioukov AV, Fehlings MG. Hematologic abnormalities within the first week after acute isolated traumatic cervical spinal cord injury: a case-control cohort study. Spine 2006;31:2674-83.
19. Held KS, Steward O, Blanc C, Lane TE. Impaired immune responses following spinal cord injury lead to reduced ability to control viral infection. Exp Neurol 2010;226:242-53.
20. Hetze S, Engel O, Römer C, Mueller S, Dirnagl U, Meisel C, et al. Superiority of preventive antibiotic treatment compared with standard treatment of poststroke pneumonia in experimental stroke: a bed to bench approach. J Cereb Blood Flow Metabol 2013;33:846-54.
21. Hoffmann S, Malzahn U, Harms H, Koennecke H-C, Berger K, Kalic M, et al. Development of a clinical score (A2DS2) to predict pneumonia in acute ischemic stroke. Stroke 2012;43:2617-23.
22. Ibarra A, Jiménez A, Cortes C, Correa D. Influence of the intensity, level and phase of spinal cord injury on the proliferation of T cells and T-cell-dependent antibody reactions in rats. Spinal Cord 2007;45:380-6.
23. Irwin MR, Cole SW. Reciprocal regulation of the neural and innate immune systems. Nat Rev Immunol 2011;11:625-32.
24. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010;8:e1000412.
25. Lacks S, Hotchkiss RD. A study of the genetic material determining an enzyme activity in Pneumococcus. Biochim Biophys Acta 1960;39:508-18.
26. Lane MA. Spinal respiratory motoneurons and interneurons. Respir Physiol Neurobiol 2011;179:3-13.
27. Lucin KM, Sanders VM, Jones TB, Malarkey WB, Popovich PG. Impaired antibody synthesis after spinal cord injury is level dependent and is due to sympathetic nervous system dysregulation. Exp Neurol 2007;207:75-84.
28. Lucin KM, Sanders VM, Popovich PG. Stress hormones collaborate to induce lymphocyte apoptosis after high level spinal cord injury. J Neurochem 2009;110:1409-21.
29. MacDonald KD, Chang H-YS, Mitzner W. An improved simple method of mouse lung intubation. J Appl Physiol 2009;106:984-7.
30. Maiorov DN, Weaver LC, Krassioukov AV. Relationship between sympathetic activity and arterial pressure in conscious spinal rats. Am J Physiol 1997;272:H625-31.
31. Marino RJ, Barros T, Biering-Sorensen F, Burns SP, Donovan WH, Graves DE, et al. International standards for neurological classification of spinal cord injury. J Spinal Cord Med 2003;26(Suppl 1):S50-6.
32. Meisel C, Schwab JM, Prass K, Meisel A, Dirnagl U. Central nervous system injury-induced immune deficiency syndrome. Nat Rev Neurosci 2005;6:775-86.
33. Prass K, Braun JS, Dirnagl U, Meisel C, Meisel A. Stroke propagates bacterial aspiration to pneumonia in a model of cerebral ischemia. Stroke 2006;37:2607-12.
34. Prass K, Meisel C, Hoflich C, Braun JS, Halle E, Wolf T, et al. Strokeinduced immunodeficiency promotes spontaneous bacterial infections and is mediated by sympathetic activation reversal by poststroke T helper cell type 1-like immunostimulation. J Exp Med 2003;198:725-36.
35. Previnaire JG, Soler JM, Masri El W, Denys P. Assessment of the sympathetic level of lesion in patients with spinal cord injury. Spinal Cord 2009;47:122-7.
36. Richards JS, Go BK, Rutt RD, Lazarus PB. Spinal cord injury: clinical outcomes from the model systems. 1995 edn. Gaithersburg, MD: Aspen Publishers; 1995.
37. Riegger T, Conrad S, Liu K, Schluesener HJ, Adibzahdeh M, Schwab JM. Spinal cord injury-induced immune depression syndrome (SCI-IDS). Eur J Neurosci 2007;25:1743-7.
38. Riegger T, Conrad S, Schluesener HJ, Kaps H-P, Badke A, Baron C, et al. Immune depression syndrome following human spinal cord injury (SCI): a pilot study. Neuroscience 2009;158:1194-9.
39. Shavelle RM, DeVivo MJ, Brooks JC, Strauss DJ, Paculdo DR. Improvements in long-term survival after spinal cord injury? Arch Phys Med Rehabil 2015;96:645-51.
40. Steinman L. Elaborate interactions between the immune and nervous systems. Nat Immunol 2004;5:575-81.
41. Stover SL, DeVivo MJ, Go BK. History, implementation, and current status of the National Spinal Cord Injury Database. Arch Phys Med Rehabil 1999;80:1365-71.
42. Sullivan GM, Feinn R. Using effect size- or why the P value is not enough. J Grad Med Educ 2012;4:279-82.
43. Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009;325:612-16.
44. Taylor RF, Schramm LP. Differential effects of spinal transection on sympathetic nerve activities in rats. Am J Physiol 1987;253:R611-8.
45. Tracey KJ. Reflex control of immunity. Nat Rev Immunol 2009;9:418-28.
46. Wallin BG, Stjernberg L. Sympathetic activity in man after spinal cord injury. Outflow to skin below the lesion. Brain 1984;107(Pt 1):183-98.
47. Zajarías-Fainsod D, Carrillo-Ruiz J, Mestre H, Grijalva I, Madrazo I, Ibarra A. Autoreactivity against myelin basic protein in patients with chronic paraplegia. Eur Spine J 2012;21:964-70.
48. Zhang Y, Guan Z, Reader B, Shawler T, Mandrekar-Colucci S, Huang K, et al. Autonomic dysreflexia causes chronic immune suppression after spinal cord injury. J Neurosci 2013;33:12970-81.