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Review Understanding Itch in Systemic Sclerosis in Order To Review Understanding itch in systemic sclerosis in order to improve patient quality of life T.M. Frech1, M. Baron2 1University of Utah, University of Utah ABSTRACT Mechanisms of pruritus and Veterans Affair Medical Center, Salt Pruritus is a common complaint in The pathophysiology of pruritus has Lake City, UT, USA; systemic sclerosis (SSc) and impairs been recently reviewed (3-8). These 2Jewish General Hospital, McGill patients’ quality of life. Little is known reviews broadly suggest that itch may University, Montreal, Quebec, Canada. about the pathogenesis of itch in SSc, originate from interplay between skin Tracy M. Frech, MD, MS but complex and multi-factorial mech- inflammation and the nervous system. Murray Baron, MD anisms of itch are appreciated in many Pruritogens, which may be mechanical, Please address correspondence to: chronic diseases. This review discusses Tracy M. Frech, MD, MS, electrical, thermal, or low pH stimuli 4B200 SOM 30 N 1900 E, the putative mechanisms of the patho- in origin, can directly stimulate nerve Salt Lake City, UT 84132, USA. genesis of itch to better understand the fibre endings, or may do so via media- E-mail: [email protected] mechanisms that may be relevant to tors released from resident cells in the Received on November 20, 2012; accepted pruritus in SSc. It discusses possible skin, particularly mast cells (9, 10). in revised form on May 28, 2013. therapeutics in the context of this com- The perception of itch depends on the Clin Exp Rheumatol 2013; 31 (Suppl. 76): plex pathogenesis. neurotransmission/neuromodulation of S81-S88. signal from the skin to brain and thus © Copyright CLINICAL AND Introduction can be modulated at multiple levels EXPERIMENTAL RHEUMATOLOGY 2013. Systemic sclerosis (SSc, scleroderma) throughout the nervous system, includ- is a chronic, multisystem disease char- ing the level of the skin, spinal cord, Key words: pruritus, systemic acterised by vasculopathy, fibrosis, and or brain (Fig. 1). As such, the goal of sclerosis autoimmunity. Pruritus has not been pruritus treatment is to remove the extensively studied in SSc. We have source of pruritogen, prevent or block demonstrated that 45% of patients the effect of local mediator release, complain of pruritus on most days and and/or interrupt the perception of itch that patients complaining of itch have at various points along nervous system more significant skin involvement, conduction. worse respiratory symptoms, and a greater number of gastrointestinal tract Pruritogens complaints (1). SSc patients with pru- Pruritogens are chemical mediators ritus have significantly worse mental that activate or sensitise nociceptor ter- and physical function and greater dis- minals to elicit or exacerbate pruritus. ability than patients without pruritus They can be generated within the skin (2). The origin of itch in SSc, whether or outside the skin (11). Although we systemic- or dermis-derived, and its re- commonly think of pruritogens as act- lationship to vasculopathy and fibrosis ing peripherally, in fact they may also is unclear. Nonetheless, an understand- act centrally. Their receptors have been ing the mechanism of itch in SSc is found in various intracutaneous cell important to improving patient quality types, peripheral and central nerves, Funding: the project described was of life. as well as sensory neurons (12). As supported by the National Center for Complex and multifactorial mecha- such, pruritus is associated with many Research Resources and the National nisms of itch are appreciated in many inflammatory, dermatologic, and sys- Center for Advancing Translational chronic diseases. Little is known about temic conditions. Sciences, National Institutes of Health, the pathogenesis of itch in SSc, we through Grant 8UL1TR000105 (formerly UL1RR025764). The content is solely the undertook this review of the putative Histamine responsibility of the authors and does not mechanisms of the pathogenesis of itch Although a multitude of mediators ca- necessarily represent the official views of and its treatment in other diseases to pable of stimulating afferent nerves the NIH. better understand the mechanisms that leading to itch exist, the classic inflam- Competing interests: none declared. may be relevant to itch in SSc. matory pruritogen is histamine, a prod- S-81 REVIEW Understanding itch in SSc to improve QoL / T.M. Frech & M. Baron uct of mast cells. In atopic dermatitis (AD) an increase in plasma histamine has been demonstrated, presumably generated by antigen/IgE-stimulated degranulation of mast cells in the gut and/or skin (10). Importantly, simi- lar abnormalities have been noted in SSc. Elevated levels of histamine were found in 18/32 (56%) patients with SSc and was more common in patients with diffuse disease (74%), in contrast to limited disease (31%) (13). In AD anti-histamine therapy is often not ef- fective in relieving itch, suggesting that although there may be an excess hista- mine release, there are also likely to be other mediators in skin equally impor- tant in itch generation (11). The com- plexity of management required for AD suggests that there may be many altered neurophysiological mediators of itch in this condition, which are important to consider in management of SSc-pruri- tus (14). Preformed histamine is present in large amounts in mast cell granules. Thus, af- ter cell activation, can be immediately released into the surrounding area in which it induces itch via H1R (histamine Fig 1. The neurology of itch. 1 receptors) on nerve fibres (8). Experi- ments in mice demonstrated that the erate itching; capsaicin always induces and the adaptive immune response in decreased threshold in response to H3R pain but never pruritus; and serotonin, an attempt to restore connective tissue antagonism activates H1R and H4R on acetylcholine, and bradykinin induced homeostasis (21, 22). Local production sensory neurons, which in turn results pain more often than pruritus (19). of cytokine in damaged skin can induce in the excitation of histamine-sensitive Thus, a better understanding of cuta- itch and immune dysregulation (23). afferents and elicits the sensation of neous mechano-insensitive C-fibres in Modulation of lipid mediators, pro- itch (15). Thus, H3R and H4R may be SSc may help clarify the painful and duced by mast cells have been studied of particular interest in SSc since H3R pruritic aspects of this disease. in the treatment of pruritus and may be can suppress itch, whereas H4R not of interest in SSc (5). only induces the sensation of itch, but Non-histamine mast cell-derived One lipid mediator, lysophosphatidic also modulates dendritic cell migration pruritogens: acid (LPA) may be of particular inter- through skin and can influence T cell re- Due to the central role of histamine in est in SSc. LPA is a potent signalling actions (15, 16); possibly linking itch to certain forms of pruritus, attention has phospholipid that can activate mast immune mediated fibrosis. been paid to the role of mast cells in cell LPA receptors, which when in the Histamine acts on a specific subgroup various conditions associated with pru- perivascular location results in vascu- of mechano-insensitive C-fibres, which ritus. The mast cell may be relevant to lar inflammation (24). Of interest, se- are also sensitive to other mediators itch but not necessarily via histamine rum samples from cholestatic patients (17). An ‘intensity theory’ suggests that release. complaining of pruritus contain higher both itching and pain result from the ac- Mast cell-derived mediators are of amounts of LPA (25). This study hy- tivation of nociceptors, but to a different three basic types and include: (1) pre- pothesised that the LPA accumulation extent, with a weak one leading to itch- formed mediators, such as histamine in the circulation of cholestatic patients ing and a stronger one to pain (18). As and heparin, stored in secretory gran- activated sensory neurons. LPA has such, the sensitivity profile of human ules, (2) newly-synthesised lipid me- also been reported to be elevated in cutaneous C-nociceptors determine diators, and (3) chemokines and cy- SSc , but secreted from activated plate- perception; histamine tends to provoke tokines (20). Mast cells produce and lets (26). Studies suggest that increased pruritus and rarely pain; prostaglandin secrete these substances in order to local formation of LPA near unmyeli- E(2) (PGE2) causes preferentially mod- influence the innate immune system nated nerve endings can cause itch S-82 Understanding itch in SSc to improve QoL / T.M. Frech & M. Baron REVIEW (25). The role of LPA/LPA1 pathway antagonist, are both used for treatment decrease in nerve fibre density stains, inhibition as a potential effective new of pulmonary arterial hypertension in including VIP immunostaining and mi- therapeutic strategy for SSc dermal fi- SSc, the study of the effect of these crovascular abnormalities in SSc skin brosis was suggested in a mouse model medications on itch in SSc is indicated. (41). Since itch is most significant in (27). Thus, in addition to fibrosis the early SSc with significant skin involve- LPA/LPA1 axis may be important in the Neuropeptides ment (42), neuropeptides may have a pruritus of SSc. Neuropeptides from unmyelinated role as a biomarker in SSc or for studies nerve ending may be responsible for of pruritus therapeutic responsiveness. Prostaglandin E (2) itch. The mast cell-nerve functional In sum, neuropeptides can induce the PGE2 is a proinflammatory cytokine, units at sites near unmyelinated nerve release histamine from skin mast cells which is reported to be a potent vasodi- fibres have been associated with dif- and can also directly act as pruritogens. lator and a weak pruritic agent in nor- ferential secretion and degranulation Neuropeptides, such as CGRP, VIP, sP, mal skin and in patients with AD (28). which may explain varying responsive- and ET-1, play an important role in the PGE2 production and the expression of ness to therapeutics used for itch and maintenance of tissue integrity in the cytosolic phospholipase A2 (cPLA2), account for some of the challenge in skin and may serve as potential bio- cyclooxygenase (COX)-1, and COX-2 studying itch (34).
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