Inflammation-induced hyperalgesia: Effects of timing, dosage, and negative affect on somatic pain sensitivity in human experimental endotoxemia

Brain, Behavior, and Immunity

Volumn 41, Issue 1, 2014, Pages 46-54

  Wegner, Alexander ^a   Elsenbruch, Sigrid ^a   Maluck, Janina ^a   Grigoleit, Jan Sebastian ^a   Engler, Harald ^a   Jäger, Marcus ^a   Spreitzer, Ingo ^b   Schedlowski, Manfred ^a   Benson, Sven ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b PAUL EHRLICH INSTITUT   (Germany)

Author keywords

Anxiety; Cytokines; Endotoxin; Inflammation; Lipopolysaccharides; Mechanical pain sensitivity; Mood; Pain; Pressure pain thresholds; Sickness behavior

Indexed keywords

HYDROCORTISONE; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; PLACEBO; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; IL6 PROTEIN, HUMAN;

ADULT; ALERTNESS; ALLODYNIA; ANXIETY; ARTICLE; BODY TEMPERATURE; COLD SENSITIVITY; CONTROLLED STUDY; DELTOID MUSCLE; ERECTOR SPINAE MUSCLE; EXPERIMENTAL ENDOTOXEMIA; GASTROCNEMIUS MUSCLE; HOSPITAL ANXIETY AND DEPRESSION SCALE; HUMAN; HUMAN EXPERIMENT; HYDROCORTISONE BLOOD LEVEL; HYPERALGESIA; HYPOTHALAMUS HYPOPHYSIS SYSTEM; INFLAMMATION; MALE; MOOD; NOCICEPTION; NORMAL HUMAN; PAIN ASSESSMENT; PRESSURE PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL; STATE TRAIT ANXIETY INVENTORY; SUPRASPINATUS MUSCLE; ADVERSE EFFECTS; AFFECT; BLOOD; COLD; COMPARATIVE STUDY; COMPLICATION; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; ENDOTOXEMIA; FEVER; INTRAVENOUS DRUG ADMINISTRATION; MUSCULOSKELETAL PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PATHOPHYSIOLOGY; PHYSIOLOGY; PRESSURE; PSYCHOLOGY; YOUNG ADULT;

ADULT; AFFECT; ANXIETY; COLD TEMPERATURE; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; DOUBLE-BLIND METHOD; ENDOTOXEMIA; FEVER; HEALTHY VOLUNTEERS; HUMANS; HYDROCORTISONE; HYPERALGESIA; INJECTIONS, INTRAVENOUS; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; MUSCULOSKELETAL PAIN; PAIN MEASUREMENT; PAIN PERCEPTION; PAIN THRESHOLD; PRESSURE; YOUNG ADULT;

EID: 84924084798     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.05.001     Document Type: Article

References (47)

1. al'Absi M., Petersen K.L., Wittmers L.E. Adrenocortical and hemodynamic predictors of pain perception in men and women. Pain 2002, 96:197-204.
2. Alstergren P., Fredriksson L., Kopp S. Temporomandibular joint pressure pain threshold is systemically modulated in rheumatoid arthritis. J. Orofac. Pain 2008, 22(3):231-238.
3. Bahador M., Cross A.S. From therapy to experimental model: a hundred years of endotoxin administration to human subjects. J. Endotoxin Res. 2007, 13:251-279.
4. Baumgärtner U., Magerl W., Klein T. Neurogenic hyperalgesia versus painful hypoalgesia: two distinct mechanisms of neuropathic pain. Pain 2002, 96:141-151.
5. Benson S., Engler H., Schedlowski M., Elsenbruch S. Experimental endotoxemia as a model to study neuroimmune mechanisms in human visceral pain. Ann. N.Y. Acad. Sci. 2012, 1262:108-117.
6. Benson S., Kattoor J., Wegner A., Hammes F., Reidick D., Grigoleit J.S., Engler H., Oberbeck R., Schedlowski M., Elsenbruch S. Acute experimental endotoxemia induces visceral hypersensitivity and altered pain evaluation in healthy humans. Pain 2012, 153(4):794-799.
7. Bingham B., Ajit S.K., Blake D.R., Samad T.A. The molecular basis of pain and its clinical implications in rheumatology. Nat. Clin. Pract. Rheumatol. 2009, 5(1):28-37.
8. Carli G., Suman A.L., Biasi G., Marcolongo R. Reactivity to superficial and deep stimuli in patients with chronic musculoskeletal pain. Pain 2002, 100(3):259-269.
9. Dadabhoy D., Croffold L.J., Spaeth M., Russell I.J., Clauw D.J. Biology and therapy of fibromyalgia. Evidence-based biomarkers for fibromyalgia syndrome. Arthrit. Res. Ther. 2008, 10(4):211.
10. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9(1):46-56.
11. de Goeij M., van Eijk L.T., Vanelderen P., Wilder-Smith O.H., Vissers K.C., van der Hoeven J.G., Kox M., Scheffer G.J., Pickkers P. Systemic inflammation decreases pain thresholds in humans in vivo. PLoS One 2013, 8(12):e84159.
12. DellaGioia N., Hannestad J. A critical review of human endotoxin administration as an experimental paradigm of depression. Neurosci. Biobehav. Rev. 2010, 34(1):130-143.
13. Elsenbruch S. Abdominal pain in Irritable Bowel Syndrome: a review of putative psychological, neural and neuro-immune mechanisms. Brain Behav. Immun. 2011, 25(3):386-394.
14. Euteneuer F., Schwarz M.J., Hennings A., Riemer S., Stapf T., Selberdinger V., Rief W. Depression, cytokines and experimental pain: evidence for sex-related association pattern. J. Affect. Dis. 2011, 131(1-3):143-149.
15. Geiss A., Varadi E., Steinbach K., Bauer H.W., Anton F. Psychoneuroimmunological correlates of persisiting sciatic pain in patients who underwent discectomy. Neurosci. Lett. 1997, 237(2-3):65-68.
16. Goehler L.E., Lyte M., Gaykema R.P. Infection-induced viscerosensory signals from the gut enhance anxiety: implications for psychoneuroimmunology. Brain Behav. Immun. 2007, 21(6):721-726.
17. Graven-Nielsen T., Arendt-Nielsen L. Peripheral and central sensitization in musculoskeletal pain disorders: an experimental approach. Curr. Rheumatol. Rep. 2002, 4(4):313-321.
18. Grigoleit J.S., Kullmann J.S., Winkelhaus A., Engler H., Wegner A., Hammes F., Oberbeck R., Schedlowski M. Single-trial conditioning in a human taste-endotoxin paradigm induces conditioned odor aversion but not cytokine responses. Brain Behav. Immun. 2012, 26(2):234-238.
19. Grigoleit J.S., Kullmann J.S., Wolf O.T., Hammes F., Wegner A., Jablonowski S., Engler H., Gizewski E., Oberbeck R., Schedlowski M. Dose-dependent effects of endotoxin on neurobehavioral functions in humans. PLoS One 2011, 6(12):e28330.
20. Grigoleit J.S., Oberbeck J.R., Lichte P., Kobbe P., Wolf O.T., Montag T., del Rey A., Gizewski E.R., Engler H., Schedlowski M. Lipopolysaccharide-induced experimental immune activation does not impair memory functions in humans. Neurobiol. Learn. Mem. 2010, 94(4):561-567.
21. Herrmann-Lingen, C., Buss, U., Snaith, R., 2005. Hospital Anxiety and Depression Scale - German Version. Huber Verlag, Bern, Switzerland.
22. Houtveen J.H., Kavelaars A., Heijnen C.J., van Doornen L.J. Heterogeneous medically unexplained symptoms and immune function. Brain Behav. Immun. 2007, 21(8):1075-1082.
23. Hutchinson M.R., Buijs M., Tuke J., Kwok Y.H., Gentgall M., Williams D., Rolan P. Low-dose endotoxin potentiates capsaicin-induced pain in man: evidence for a pain neuroimmune connection. Brain Behav. Immun. 2013, 30:3-11.
24. Koch A., Zacharowski K., Boehm O., Stevens M., Lipfert P., von Giesen H.J., Wolf A., Freynhagen R. Nitric oxide and pro-inflammatory cytokines correlate with pain intensity in chronic pain patients. Inflamm. Res. 2007, 56(1):32-37.
25. Lacourt T., Houtveen J.H., van Dornen L.J.P. Experimental pressure-pain assessments: test-retest reliability, convergence and dimensionality. Scand. J. Pain 2012, 3:31-37.
26. Laursen B.S., Bajaj P., Olesen A.S., Delmar C., Arendt-Nielsen L. Health related quality of life and quantitative pain measurement in females with chronic non-malignant pain. Eur. J. Pain 2005, 9(3):267-275.
27. Miller R.J., Jung H., Bhangoo S.K., White F.A. Cytokine and chemokine regulation of sensory neuron function. Handb. Exp. Pharmacol. 2009, 194:417-449.
28. Mullington J., Korth C., Hermann D.M., Orth A., Galanos C., Holsboer F., Pollmacher T. Dose-dependent effects of endotoxin on human sleep. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2000, 278:R947-R955.
29. Nicrota L., Loram L.C., Watkins L.R., Hutchinson M.R. Toll-likereceptors in pain. Exp. Neurol. 2012, 234:316-329.
30. Oono Y., Baad-Hansen L., Wang K., Arendt-Nielsen L., Svensson P. Effect of conditioned pain modulation on trigeminal somatosensory function evaluated by quantitative sensory testing. Pain 2013, 154(12):2684-2690.
31. Parkitny L., McAuley J.H., Di Pietro F., Stanton T.R., O'Connell N.E., Marinus J., vanHilten J.J., Moseley G.L. Inflammation in complex regional pain syndrome: a systematic review and meta-analysis. Neurology 2013, 80(1):106-117.
32. Rolke R., Baron R., Maier C., Tolle T.R., Treede R.D., Beyer A., Binder A., Birbaumer N., Birklein F., Botefur I.C., Braune S., Flor H., Huge V., Klug R., Landwehrmeyer G.B., Magerl W., Maihofner C., Rolko C., Schaub C., Scherens A., Sprenger T., Valet M., Wasserka B. Quantitative sensory testing in the German Research Network on Neuropathic Pain (DFNS): standardized protocol and reference values. Pain 2006, 123(3):231-243.
33. Sandkuhler J. Models and mechanisms of hyperalgesia and allodynia. Physiol. Rev. 2009, 89:707-758.
34. Schafers M., Sorkin L. Effect of cytokines on neuronal excitability. Neurosci. Lett. 2008, 437(3):188-193.
35. Schedlowski M., Engler H., Grigoleit J.S. Endotoxin-induced experimental systemic inflammation in humans: a model to disentangle immune-to-brain communication. Brain Behav. Immun. 2014, 35(1):1-8.
36. Smith H.S., Harris R., Clauw D. Fibromyalgia: an afferent processing disorder leading to a complex pain generalized syndrome. Pain Phys. 2011, 14(2):E217-E245.
37. Spielberger C.D., Gorsuch R.L., Lushene R.E. Manual for the State-trait Anxiety Inventory 1970, Consulting Psychology Press, Palo Alto, CA.
38. Steyer R., Schwenkmezger P., Notz P., Eid M. Der Mehrdimensionale Befindlichkeitsfragebogen (MDBF) 1997, Hogrefe, Göttingen.
39. Stürmer T., Brenner H., Koenig W., Günther K.P. Severity and extent of osteoarthritis and low grade systemic inflammation as assessed by high sensitivity C reactive protein. Ann. Rheumat. Disord. 2004, 63(2):200-205.
40. Üceyler N., Häuser W., Sommer C. Systematic review with meta-analysis: cytokines in fibromyalgia syndrome. BMC Musculoskel. Disord. 2011, 28(12):245.
41. Üceyler N., Rogausch J.P., Toyka K.V., Sommer C. Differential expression of cytokines in painful and painless neuropathies. Neurology 2007, 69(1):42-49.
42. Vaegter H.B., Handberg ang G., Graven-Nielsen T. Similarities between exercise-induced hypoalgesia and conditioned pain modulation in humans. Pain 2014, 155(1):158-167.
43. Walker A.K., Kavelaars A., Heijnen C.J., Dantzer R. Neuroinflammation and comorbidity of pain and depression. Pharmacol. Rev. 2014, 66:80-101.
44. Wang X.S., Williams L.A., Krishnan S., Liao Z., Liu P., Mao L., Shi Q., Mobley G.M., Woodruff J.F., Cleeland C.S. Serum sTNF-R1, IL-6, and the development of fatigue in patients with gastrointestinal cancer undergoing chemoradiation therapy. Brain Behav. Immun. 2012, 26(5):699-705.
45. Watkins L.R., Hutchinson M.R., Milligan E.D., Maier S.F. "Listening" and "talking" to neurons: implications of immune activation for pain control and increasing the efficacy of opioids. Brain Res. Rev. 2007, 56:148-169.
46. Watkins L.R., Maier S.F. Immune regulation of central nervous system functions: from sickness responses to pathological pain. J. Intern. Med. 2005, 257(2):139-155.
47. Wiech K., Tracey I. The influence of negative emotions on pain: Behavioral effects and neural mechanisms. NeuroImage 2009, 47:987-994.