Comparison of pruritus and sensory qualities induced by capsaicin, histamine and cowhage.


Journal

Journal of the European Academy of Dermatology and Venereology : JEADV
ISSN: 1468-3083
Titre abrégé: J Eur Acad Dermatol Venereol
Pays: England
ID NLM: 9216037

Informations de publication

Date de publication:
Sep 2019
Historique:
received: 22 01 2019
accepted: 29 05 2019
pubmed: 15 6 2019
medline: 8 2 2020
entrez: 15 6 2019
Statut: ppublish

Résumé

In skin diseases and experimental models of pruritus, pure itch is accompanied by additional sensations that are poorly characterized. This study compared the sensory qualities evoked by different models of experimentally induced pruritus including skin prick testing (SPT) with histamine or capsaicin and application of cowhage spicules. SPT as a method of capsaicin application was validated for this purpose. Two pilot experiments were performed in eight healthy volunteers. First, a concentration of 8% capsaicin was identified as evoking a reproducible itch using SPT. Further, a list of the seven most frequently reported sensations was chosen after SPT with 10 mg/mL histamine, 8% capsaicin and application of 40-45 cowhage spicules. Finally, 31 subjects were challenged with the same itch-inducers. Wheal and flare were measured at 10, 20, 40, 60 and 90 min, itch intensity every minute for 30 min, and the overall evaluation of sensory descriptors were recorded on a 100-mm visual analogue scale once itching had subsided. Skin prick testing with histamine and capsaicin resulted in flare reactions, which were 23% smaller for capsaicin (P < 0.001). Histamine, capsaicin and cowhage-induced pruritus, the duration of which was shorter for cowhage than for histamine (13.5 ± 1.4 vs. 8.8 ± 1.2 min, P = 0.005). Different mediators induced sensations of different intensities. Capsaicin produced less itch and physical urge to scratch than histamine (P = 0.001) and cowhage (P < 0.001). However, both capsaicin and cowhage induced more burning than histamine (P = 0.002 and P = 0.04, respectively). Provocation with cowhage caused more intense sensations of pricking than histamine (P = 0.033). This study shows that provocation with histamine, capsaicin and cowhage results in itch responses that are different in their duration, the profile of accompanying sensations, and the flare that comes with the itch.

Sections du résumé

BACKGROUND BACKGROUND
In skin diseases and experimental models of pruritus, pure itch is accompanied by additional sensations that are poorly characterized.
OBJECTIVES OBJECTIVE
This study compared the sensory qualities evoked by different models of experimentally induced pruritus including skin prick testing (SPT) with histamine or capsaicin and application of cowhage spicules. SPT as a method of capsaicin application was validated for this purpose.
METHODS METHODS
Two pilot experiments were performed in eight healthy volunteers. First, a concentration of 8% capsaicin was identified as evoking a reproducible itch using SPT. Further, a list of the seven most frequently reported sensations was chosen after SPT with 10 mg/mL histamine, 8% capsaicin and application of 40-45 cowhage spicules. Finally, 31 subjects were challenged with the same itch-inducers. Wheal and flare were measured at 10, 20, 40, 60 and 90 min, itch intensity every minute for 30 min, and the overall evaluation of sensory descriptors were recorded on a 100-mm visual analogue scale once itching had subsided.
RESULTS RESULTS
Skin prick testing with histamine and capsaicin resulted in flare reactions, which were 23% smaller for capsaicin (P < 0.001). Histamine, capsaicin and cowhage-induced pruritus, the duration of which was shorter for cowhage than for histamine (13.5 ± 1.4 vs. 8.8 ± 1.2 min, P = 0.005). Different mediators induced sensations of different intensities. Capsaicin produced less itch and physical urge to scratch than histamine (P = 0.001) and cowhage (P < 0.001). However, both capsaicin and cowhage induced more burning than histamine (P = 0.002 and P = 0.04, respectively). Provocation with cowhage caused more intense sensations of pricking than histamine (P = 0.033).
CONCLUSION CONCLUSIONS
This study shows that provocation with histamine, capsaicin and cowhage results in itch responses that are different in their duration, the profile of accompanying sensations, and the flare that comes with the itch.

Identifiants

pubmed: 31199524
doi: 10.1111/jdv.15743
doi:

Substances chimiques

Histamine 820484N8I3
Capsaicin S07O44R1ZM

Types de publication

Comparative Study Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1755-1761

Subventions

Organisme : International Institute of Dermatological Allergology
Organisme : Charité-Universitätsmedizin Berlin

Informations de copyright

© 2019 European Academy of Dermatology and Venereology.

Références

Dawn A, Papoiu AD, Chan YH, Rapp SR, Rassette N, Yosipovitch G. Itch characteristics in atopic dermatitis: results of a web-based questionnaire. Br J Dermatol 2009; 160: 642-644.
Darsow U, Scharein E, Simon D, Walter G, Bromm B, Ring J. New aspects of itch pathophysiology: component analysis of atopic itch using the ‘Eppendorf Itch Questionnaire’. Int Arch Allergy Immunol 2001; 124: 326-331.
Hawro T, Lehmann S, Altrichter S et al. Skin provocation tests may help to diagnose atopic dermatitis. Allergy 2016; 71: 1745-1752.
Ringkamp M, Schepers RJ, Shimada SG et al. A role for nociceptive, myelinated nerve fibers in itch sensation. J Neurosci 2011; 31: 14841-14849.
Sikand P, Shimada SG, Green BG, LaMotte RH. Sensory responses to injection and punctate application of capsaicin and histamine to the skin. Pain 2011; 152: 2485-2494.
Sikand P, Shimada SG, Green BG, LaMotte RH. Similar itch and nociceptive sensations evoked by punctate cutaneous application of capsaicin, histamine and cowhage. Pain 2009; 144: 66-75.
Mackey S, Carroll I, Emir B, Murphy TK, Whalen E, Dumenci L. Sensory pain qualities in neuropathic pain. J Pain 2012; 13: 58-63.
Jensen MP, Dworkin RH, Gammaitoni AR, Olaleye DO, Oleka N, Galer BS. Do pain qualities and spatial characteristics make independent contributions to interference with physical and emotional functioning? J Pain 2006; 7: 644-653.
Jensen MP. Using pain quality assessment measures for selecting analgesic agents. Clin J Pain 2006; 22: S9-S13.
Melzack R. The short-form McGill pain questionnaire. Pain 1987; 30: 191-197.
Yosipovitch G, Zucker I, Boner G, Gafter U, Shapira Y, David M. A questionnaire for the assessment of pruritus: validation in uremic patients. Acta Derm Venereol 2001; 81: 108-111.
Weisshaar E, Gieler U, Kupfer J et al. Questionnaires to assess chronic itch: a consensus paper of the special interest group of the International Forum on the Study of Itch. Acta Derm Venereol 2012; 92: 493-496.
Andersen HH, Elberling J, Arendt-Nielsen L. Human surrogate models of histaminergic and non-histaminergic itch. Acta Derm Venereol 2015; 95: 771-777.
Hawro T, Fluhr JW, Mengeaud V et al. Polidocanol inhibits cowhage - but not histamine-induced itch in humans. Exp Dermatol 2014; 23: 922-923.
Hawro T, Saluja R, Weller K, Altrichter S, Metz M, Maurer M. Interleukin-31 does not induce immediate itch in atopic dermatitis patients and healthy controls after skin challenge. Allergy 2014; 69: 113-117.
Hoeck EA, Marker JB, Gazerani P, H Andersen H, Arendt-Nielsen L. Preclinical and human surrogate models of itch. Exp Dermatol 2016; 25: 750-757.
Papoiu AD, Valdes-Rodriguez R, Nattkemper LA, Chan YH, Hahn GS, Yosipovitch G. A novel topical formulation containing strontium chloride significantly reduces the intensity and duration of cowhage-induced itch. Acta Derm Venereol 2013; 93: 520-526.
Papoiu AD, Chaudhry H, Hayes EC, Chan YH, Herbst KD. TriCalm(®) hydrogel is significantly superior to 2% diphenhydramine and 1% hydrocortisone in reducing the peak intensity, duration, and overall magnitude of cowhage-induced itch. Clin Cosmet Investig Dermatol 2015; 8: 223-229.
Andersen HH, Sørensen AR, Nielsen GA et al. A test-retest reliability study of human experimental models of histaminergic and non-histaminergic itch. Acta Derm Venereol 2017; 97: 198-207.
Shelley W, Arthur R. Studies on cowhage (Mucuna pruriens) and its pruritogenic proteinase, mucunain. AMA Arch Derm 1955; 72: 399-406.
Papoiu AD, Tey HL, Coghill RC, Wang H, Yosipovitch G. Cowhage-induced itch as an experimental model for pruritus. A comparative study with histamine-induced itch. PLoS ONE 2011; 6: e17786.
Namer B, Carr R, Johanek LM, Schmelz M, Handwerker HO, Ringkamp M. Separate peripheral pathways for pruritus in man. J Neurophysiol 2008; 100: 2062-2069.
Schmelz M, Schmidt R, Bickel A, Handwerker HO, Torebjörk HE. Specific C-receptors for itch in human skin. J Neurosci 1997; 17: 8003-8008.
Steinhoff M, Neisius U, Ikoma A et al. Proteinase-activated receptor-2 mediates itch: a novel pathway for pruritus in human skin. J Neurosci 2003; 23: 6176-6180.
Reddy VB, Iuga AO, Shimada SG, LaMotte RH, Lerner EA. Cowhage-evoked itch is mediated by a novel cysteine protease: a ligand of protease-activated receptors. J Neurosci 2008; 28: 4331-4335.
Thurmond RL. The histamine H4 receptor: from orphan to the clinic. Front Pharmacol 2015; 6: 65.
Biro T, Toth BI, Marincsak R, Dobrosi N, Geczy T, Paus R. TRP channels as novel players in the pathogenesis and therapy of itch. Biochem Biophys Acta 2007; 1772: 1004-1021.
Shim WS, Tak MH, Lee MH et al. TRPV1 mediates histamine-induced itching via the activation of phospholipase A2 and 12-lipoxygenase. J Neurosci 2007; 27: 2331-2337.
Imamachi N, Park GH, Lee H et al. TRPV1-expressing primary afferents generate behavioral responses to pruritogens via multiple mechanisms. Proc Natl Acad Sci U S A 2009; 106: 11330-11335.
Jian T, Yang N, Yang Y et al. TRPV1 and PLC participate in histamine H4 receptor-induced itch. Neural Plast 2016; 2016: 1682972.
Dai Y, Moriyama T, Higashi T et al. Proteinase-activated receptor 2-mediated potentiation of transient receptor potential vanilloid subfamily 1 activity reveals a mechanism for proteinase-induced inflammatory pain. J Neurosci 2004; 24: 4293-4299.
Denda M, Fuziwara S, Inoue K et al. Immunoreactivity of VR1 on epidermal keratinocyte of human skin. Biochem Biophys Res Comm 2001; 285: 1250-1252.
Ständer S, Moormann C, Schumacher M et al. Expression of vanilloid receptor subtype 1 in cutaneous sensory nerve fibers, mast cells, and epithelial cells of appendage structures. Exp Dermatol 2004; 13: 129-139.
Costa R, Marotta DM, Manjavachi MN et al. Evidence for the role of neurogenic inflammation components in trypsin-elicited scratching behaviour in mice. Br J Pharmacol 2008; 154: 1094-1103.
LaMotte RH, Shain CN, Simone DA, Tsai EF. Neurogenic hyperalgesia: psychophysical studies of underlying mechanisms. J Neurophysiol 1991; 66: 190-211.
Schmelz M, Schmid R, Handwerker HO, Torebjörk HE. Encoding of burning pain from capsaicin-treated human skin in two categories of unmyelinated nerve fibres. Brain 2000; 123(Pt 3): 560-571.
Simone DA, Baumann TK, LaMotte RH. Dose-dependent pain and mechanical hyperalgesia in humans after intradermal injection of capsaicin. Pain 1989; 38: 99-107.
Hartmann EM, Handwerker HO, Forster C. Gender differences in itch and pain-related sensations provoked by histamine, cowhage and capsaicin. Acta Derm Venereol 2015; 95: 25-30.
Vierow V, Forster C, Vogelgsang R, Dörfler A, Handwerker HO. Cerebral networks linked to itch-related sensations induced by histamine and capsaicin. Acta Derm Venereol 2015; 95: 645-652.
Green BG, Shaffer GS. The sensory response to capsaicin during repeated topical exposures: differential effects on sensations of itching and pungency. Pain 1993; 53: 323-334.
Green BG. Spatial summation of chemical irritation and itch produced by topical application of capsaicin. Percept Psychophys 1990; 48: 12-18.
Bousquet J, Heinzerling L, Bachert C et al. Practical guide to skin prick tests in allergy to aeroallergens. Allergy 2012; 67: 18-24.
Schmelz M, Schmidt R, Weidner C, Hilliges M, Torebjork HE, Handwerker HO. Chemical response pattern of different classes of C-nociceptors to pruritogens and algogens. J Neurophysiol 2003; 89: 2441-2448.
Johanek LM, Meyer RA, Friedman RM et al. A role for polymodal C-fiber afferents in nonhistaminergic itch. J Neurosci 2008; 28: 7659-7669.
Schmidt R, Schmelz M, Weidner C, Handwerker HO, Torebjörk HE. Innervation territories of mechano-insensitive C nociceptors in human skin. J Neurophysiol 2002; 88: 1859-1866.
Ashina K, Tsubosaka Y, Nakamura T et al. Histamine induces vascular hyperpermeability by increasing blood flow and endothelial barrier disruption in vivo. PLoS ONE 2015; 10: e0132367.
Kwan HY, Huang Y, Yao X. TRP channels in endothelial function and dysfunction. Biochem Biophys Acta 2007; 1772: 907-914.
Hawro T, Ohanyan T, Schoepke N et al. Comparison and interpretability of the available urticaria activity scores. Allergy 2018; 73: 251-255.
Davidson S, Zhang X, Yoon CH, Khasabov SG, Simone DA, Giesler GJ. The itch-producing agents histamine and cowhage activate separate populations of primate spinothalamic tract neurons. J Neurosci 2007; 27: 10007-10014.
Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997; 389: 816-824.
Darsow U, Ring J, Scharein E, Bromm B. Correlations between histamine-induced wheal, flare and itch. Arch Dermatol Res 1996; 288: 436-441.
Darsow U, Scharein E, Bromm B, Ring J. Skin testing of the pruritogenic activity of histamine and cytokines (interleukin-2 and tumour necrosis factor-alpha) at the dermal-epidermal junction. Br J Dermatol 1997; 137: 415-417.

Auteurs

T Hawro (T)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

S Lehmann (S)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

E Deuring (E)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

K Weller (K)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

S Altrichter (S)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

M K Church (MK)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

M Maurer (M)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

M Metz (M)

Department of Dermatology and Allergy, Charité - Universitätsmedizin Berlin, Berlin, Germany.

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