Mast cell dependent vascular changes associated with an acute response to cold immersion in primary contact urticaria
While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature,...
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Published in | PloS one Vol. 8; no. 2; p. e56773 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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22.02.2013
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Abstract | While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature, critical to understanding the evolution of mast cell dependent inflammation.
To characterize the microcirculatory events that follow mast cell degranulation.
Perturbations in dermal blood flow, temperature and skin color were analyzed using laser-speckle contrast imaging, infrared and polarized-light colorimetry following cold-hand immersion (CHI) challenge in patients with cold-induced urticaria compared to the response in healthy controls. Evidence for mast cell degranulation was established by documentation of serum histamine levels and the localized release of tryptase in post-challenge urticarial biopsies. Laser-speckle contrast imaging quantified the attenuated response to cold challenge in patients on cetirizine. We found that the histamine-associated vascular response accompanying mast cell degranulation is rapid and extensive. At the tissue level, it is characterized by a uniform pattern of increased blood flow, thermal warming, vasodilation, and recruitment of collateral circulation. These vascular responses are modified by the administration of an antihistamine.
Monitoring the hemodynamic responses within tissues that are associated with mast cell degranulation provides additional insight into the evolution of the acute inflammatory response and offers a unique approach to assess the effectiveness of treatment intervention. |
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AbstractList | While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature, critical to understanding the evolution of mast cell dependent inflammation.
To characterize the microcirculatory events that follow mast cell degranulation.
Perturbations in dermal blood flow, temperature and skin color were analyzed using laser-speckle contrast imaging, infrared and polarized-light colorimetry following cold-hand immersion (CHI) challenge in patients with cold-induced urticaria compared to the response in healthy controls. Evidence for mast cell degranulation was established by documentation of serum histamine levels and the localized release of tryptase in post-challenge urticarial biopsies. Laser-speckle contrast imaging quantified the attenuated response to cold challenge in patients on cetirizine. We found that the histamine-associated vascular response accompanying mast cell degranulation is rapid and extensive. At the tissue level, it is characterized by a uniform pattern of increased blood flow, thermal warming, vasodilation, and recruitment of collateral circulation. These vascular responses are modified by the administration of an antihistamine.
Monitoring the hemodynamic responses within tissues that are associated with mast cell degranulation provides additional insight into the evolution of the acute inflammatory response and offers a unique approach to assess the effectiveness of treatment intervention. Background While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature, critical to understanding the evolution of mast cell dependent inflammation. Objective To characterize the microcirculatory events that follow mast cell degranulation. Methodology/Principal Findings Perturbations in dermal blood flow, temperature and skin color were analyzed using laser-speckle contrast imaging, infrared and polarized-light colorimetry following cold-hand immersion (CHI) challenge in patients with cold-induced urticaria compared to the response in healthy controls. Evidence for mast cell degranulation was established by documentation of serum histamine levels and the localized release of tryptase in post-challenge urticarial biopsies. Laser-speckle contrast imaging quantified the attenuated response to cold challenge in patients on cetirizine. We found that the histamine-associated vascular response accompanying mast cell degranulation is rapid and extensive. At the tissue level, it is characterized by a uniform pattern of increased blood flow, thermal warming, vasodilation, and recruitment of collateral circulation. These vascular responses are modified by the administration of an antihistamine. Conclusions/Significance Monitoring the hemodynamic responses within tissues that are associated with mast cell degranulation provides additional insight into the evolution of the acute inflammatory response and offers a unique approach to assess the effectiveness of treatment intervention. Background While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature, critical to understanding the evolution of mast cell dependent inflammation. Objective To characterize the microcirculatory events that follow mast cell degranulation. Methodology/Principal Findings Perturbations in dermal blood flow, temperature and skin color were analyzed using laser-speckle contrast imaging, infrared and polarized-light colorimetry following cold-hand immersion (CHI) challenge in patients with cold-induced urticaria compared to the response in healthy controls. Evidence for mast cell degranulation was established by documentation of serum histamine levels and the localized release of tryptase in post-challenge urticarial biopsies. Laser-speckle contrast imaging quantified the attenuated response to cold challenge in patients on cetirizine. We found that the histamine-associated vascular response accompanying mast cell degranulation is rapid and extensive. At the tissue level, it is characterized by a uniform pattern of increased blood flow, thermal warming, vasodilation, and recruitment of collateral circulation. These vascular responses are modified by the administration of an antihistamine. Conclusions/Significance Monitoring the hemodynamic responses within tissues that are associated with mast cell degranulation provides additional insight into the evolution of the acute inflammatory response and offers a unique approach to assess the effectiveness of treatment intervention. While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature, critical to understanding the evolution of mast cell dependent inflammation. To characterize the microcirculatory events that follow mast cell degranulation. Perturbations in dermal blood flow, temperature and skin color were analyzed using laser-speckle contrast imaging, infrared and polarized-light colorimetry following cold-hand immersion (CHI) challenge in patients with cold-induced urticaria compared to the response in healthy controls. Evidence for mast cell degranulation was established by documentation of serum histamine levels and the localized release of tryptase in post-challenge urticarial biopsies. Laser-speckle contrast imaging quantified the attenuated response to cold challenge in patients on cetirizine. We found that the histamine-associated vascular response accompanying mast cell degranulation is rapid and extensive. At the tissue level, it is characterized by a uniform pattern of increased blood flow, thermal warming, vasodilation, and recruitment of collateral circulation. These vascular responses are modified by the administration of an antihistamine. Monitoring the hemodynamic responses within tissues that are associated with mast cell degranulation provides additional insight into the evolution of the acute inflammatory response and offers a unique approach to assess the effectiveness of treatment intervention. While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature, critical to understanding the evolution of mast cell dependent inflammation.BACKGROUNDWhile a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and the subsequent cellular infiltrate, there is little known about the immediate effects of mast cell degranulation on the associated vasculature, critical to understanding the evolution of mast cell dependent inflammation.To characterize the microcirculatory events that follow mast cell degranulation.OBJECTIVETo characterize the microcirculatory events that follow mast cell degranulation.Perturbations in dermal blood flow, temperature and skin color were analyzed using laser-speckle contrast imaging, infrared and polarized-light colorimetry following cold-hand immersion (CHI) challenge in patients with cold-induced urticaria compared to the response in healthy controls. Evidence for mast cell degranulation was established by documentation of serum histamine levels and the localized release of tryptase in post-challenge urticarial biopsies. Laser-speckle contrast imaging quantified the attenuated response to cold challenge in patients on cetirizine. We found that the histamine-associated vascular response accompanying mast cell degranulation is rapid and extensive. At the tissue level, it is characterized by a uniform pattern of increased blood flow, thermal warming, vasodilation, and recruitment of collateral circulation. These vascular responses are modified by the administration of an antihistamine.METHODOLOGY/PRINCIPAL FINDINGSPerturbations in dermal blood flow, temperature and skin color were analyzed using laser-speckle contrast imaging, infrared and polarized-light colorimetry following cold-hand immersion (CHI) challenge in patients with cold-induced urticaria compared to the response in healthy controls. Evidence for mast cell degranulation was established by documentation of serum histamine levels and the localized release of tryptase in post-challenge urticarial biopsies. Laser-speckle contrast imaging quantified the attenuated response to cold challenge in patients on cetirizine. We found that the histamine-associated vascular response accompanying mast cell degranulation is rapid and extensive. At the tissue level, it is characterized by a uniform pattern of increased blood flow, thermal warming, vasodilation, and recruitment of collateral circulation. These vascular responses are modified by the administration of an antihistamine.Monitoring the hemodynamic responses within tissues that are associated with mast cell degranulation provides additional insight into the evolution of the acute inflammatory response and offers a unique approach to assess the effectiveness of treatment intervention.CONCLUSIONS/SIGNIFICANCEMonitoring the hemodynamic responses within tissues that are associated with mast cell degranulation provides additional insight into the evolution of the acute inflammatory response and offers a unique approach to assess the effectiveness of treatment intervention. |
Audience | Academic |
Author | Medic, Nevenka Arceo, Sarah Nelson, Celeste Komarow, Hirsh D Liu, Wei-Min Metcalfe, Dean D Young, Michael Desai, Avanti Gorbach, Alexander M Meyer, Joseph |
AuthorAffiliation | 3 Clinical Research Directorate/CMRP, SAIC-Frederick, NCI Frederick, Frederick, Maryland, United States of America King’s College London School of Medicine, United Kingdom 2 Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America 1 Infrared Imaging and Thermometry Unit, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, Maryland, United States of America |
AuthorAffiliation_xml | – name: 2 Laboratory of Allergic Diseases, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, Maryland, United States of America – name: 3 Clinical Research Directorate/CMRP, SAIC-Frederick, NCI Frederick, Frederick, Maryland, United States of America – name: 1 Infrared Imaging and Thermometry Unit, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, Maryland, United States of America – name: King’s College London School of Medicine, United Kingdom |
Author_xml | – sequence: 1 givenname: Joseph surname: Meyer fullname: Meyer, Joseph organization: Infrared Imaging and Thermometry Unit, National Institute of Biomedical Imaging and Bioengineering, National Institutes of Health, Bethesda, Maryland, United States of America – sequence: 2 givenname: Alexander M surname: Gorbach fullname: Gorbach, Alexander M – sequence: 3 givenname: Wei-Min surname: Liu fullname: Liu, Wei-Min – sequence: 4 givenname: Nevenka surname: Medic fullname: Medic, Nevenka – sequence: 5 givenname: Michael surname: Young fullname: Young, Michael – sequence: 6 givenname: Celeste surname: Nelson fullname: Nelson, Celeste – sequence: 7 givenname: Sarah surname: Arceo fullname: Arceo, Sarah – sequence: 8 givenname: Avanti surname: Desai fullname: Desai, Avanti – sequence: 9 givenname: Dean D surname: Metcalfe fullname: Metcalfe, Dean D – sequence: 10 givenname: Hirsh D surname: Komarow fullname: Komarow, Hirsh D |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Competing Interests: The authors have declared that no competing interests exist. Obtained informed consent: MY SA. Conceived and designed the experiments: JM AMG WML MY CN SA DDM HDK. Performed the experiments: JM AMG WML NM MY CN AD DDM HDK. Analyzed the data: JM AMG WML NM AD DDM HDK. Contributed reagents/materials/analysis tools: JM AMG WML NM AD DDM HDK. Wrote the paper: JM AMG WML NM MY CN SA AD DDM HDK. |
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characteristics of facial skin temperatures publication-title: Physiol Meas doi: 10.1088/0967-3334/30/4/N01 contributor: fullname: BR Nhan – volume: 313 start-page: 405 year: 1985 ident: ref17 article-title: Association of platelet-activating factor with primary acquired cold urticaria publication-title: N Engl J Med doi: 10.1056/NEJM198508153130702 contributor: fullname: KE Grandel – volume: 294 start-page: 687 year: 1976 ident: ref16 article-title: Cold urticaria: release into the circulation of histamine and eosinophil chemotactic factor of anaphylaxis during cold challenge publication-title: N Engl J Med doi: 10.1056/NEJM197603252941302 contributor: fullname: NA Soter – volume: 14 start-page: 416 year: 1989 ident: ref10 article-title: A timed study of the histopathology, direct immunofluorescence and ultrastructural findings in idiopathic cold-contact urticaria over a 24-h period publication-title: Clin Exp Dermatol doi: 10.1111/j.1365-2230.1989.tb02601.x contributor: fullname: F Lawlor – volume: 134 start-page: 41 year: 1998 ident: ref15 article-title: Microscopic morphology of different types of urticaria publication-title: Archives of dermatology doi: 10.1001/archderm.134.1.41 contributor: fullname: N Haas – volume: 106 start-page: 65 year: 2000 ident: ref18 article-title: Histamine and tryptase levels in patients with acute allergic reactions: An emergency department-based study publication-title: J Allergy Clin Immunol doi: 10.1067/mai.2000.107600 contributor: fullname: RY Lin – volume: 242 start-page: 31 year: 2011 ident: ref3 article-title: Pathophysiology of allergic inflammation publication-title: Immunological reviews doi: 10.1111/j.1600-065X.2011.01020.x contributor: fullname: PJ Barnes – volume: 29 start-page: 54 year: 1999 ident: ref11 article-title: Beyond the histamine receptor: effect of antihistamines on mast cells publication-title: Clinical and experimental allergy : journal of the British Society for Allergy and Clinical Immunology doi: 10.1046/j.1365-2222.1999.00013.x contributor: fullname: FM Cuss – volume: 83 start-page: 1551 year: 1989 ident: ref13 article-title: Time course of appearance and disappearance of human mast cell tryptase in the circulation after anaphylaxis publication-title: J Clin Invest doi: 10.1172/JCI114051 contributor: fullname: LB Schwartz – volume: 55 start-page: 394 year: 1975 ident: ref12 article-title: In vivo studies of mediator release in cold urticaria and cholinergic urticaria publication-title: J Allergy Clin Immunol doi: 10.1016/0091-6749(75)90078-0 contributor: fullname: AP Kaplan – volume: 305 start-page: 1074 year: 1981 ident: ref22 article-title: Idiopathic cold urticaria: in vitro demonstration of histamine release upon challenge of skin biopsies publication-title: N Engl J Med doi: 10.1056/NEJM198110293051808 contributor: fullname: AP Kaplan – volume: 67 start-page: S54 year: 2009 ident: ref30 article-title: Dynamic infrared imaging of cutaneous melanoma and normal skin in patients treated with BNCT publication-title: Appl Radiat Isot doi: 10.1016/j.apradiso.2009.03.093 contributor: fullname: GA Santa Cruz – volume: 80 start-page: 603 year: 1987 ident: ref9 article-title: Morphologically distinctive forms of cutaneous mast cell degranulation induced by cold and mechanical stimuli: an ultrastructural study publication-title: The Journal of allergy and clinical immunology doi: 10.1016/0091-6749(87)90015-7 contributor: fullname: GF Murphy – volume: 109 start-page: 287 year: 2002 ident: ref21 article-title: Characterization of mast-cell tryptase-expressing peripheral blood cells as basophils publication-title: The Journal of allergy and clinical immunology doi: 10.1067/mai.2002.121454 contributor: fullname: B Foster – volume: 13 start-page: 472 year: 2007 ident: ref33 article-title: Sub-epidermal imaging using polarized light spectroscopy for assessment of skin microcirculation publication-title: Skin research and technology : official journal of International Society for Bioengineering and the Skin doi: 10.1111/j.1600-0846.2007.00253.x contributor: fullname: J O’Doherty – volume: 104 start-page: S132 year: 1999 ident: ref2 article-title: Pathophysiology of the inflammatory response publication-title: The Journal of allergy and clinical immunology doi: 10.1016/S0091-6749(99)70308-8 contributor: fullname: DS Pearlman – ident: ref7 doi: 10.1111/1523-1747.ep12469015 – volume: 454 start-page: 445 year: 2008 ident: ref4 article-title: The development of allergic inflammation publication-title: Nature doi: 10.1038/nature07204 contributor: fullname: SJ Galli – volume: 83 start-page: 738 year: 1989 ident: ref19 article-title: Refractory cholinergic urticaria successfully treated with ketotifen publication-title: The Journal of allergy and clinical immunology doi: 10.1016/0091-6749(89)90008-0 contributor: fullname: SP McClean – volume: 130 start-page: 849 year: 2010 ident: ref25 article-title: Aging-Associated Sensory Neuropathy Alters Pressure-Induced Vasodilation in Humans publication-title: Journal of Investigative Dermatology doi: 10.1038/jid.2009.279 contributor: fullname: B Fromy – ident: ref23 doi: 10.1016/j.jaci.2011.07.021 – volume: 54 start-page: S282 year: 2006 ident: ref32 article-title: Noninvasive techniques for the evaluation of skin color publication-title: J Am Acad Dermatol doi: 10.1016/j.jaad.2005.12.041 contributor: fullname: S Taylor – volume: 21 start-page: 73 year: 2002 ident: ref24 article-title: Infrared functional imaging applied to Raynaud’s phenomenon publication-title: IEEE Eng Med Biol Mag doi: 10.1109/MEMB.2002.1175141 contributor: fullname: A Merla – ident: ref26 doi: 10.1016/j.iac.2004.01.001 – volume: 100 start-page: 635 year: 1979 ident: ref20 article-title: Distribution of mast cells in human dermis: development of a mapping technique publication-title: Br J Dermatol doi: 10.1111/j.1365-2133.1979.tb08066.x contributor: fullname: T Cowen – volume: 2 start-page: 1470 year: 2011 ident: ref27 article-title: Real-time full field laser Doppler imaging publication-title: Biomed Opt Express doi: 10.1364/BOE.2.001470 contributor: fullname: M Leutenegger – volume: 125 start-page: S73 year: 2010 ident: ref1 article-title: IgE, mast cells, basophils, and eosinophils publication-title: The Journal of allergy and clinical immunology doi: 10.1016/j.jaci.2009.11.017 contributor: fullname: KD Stone – volume: 106 start-page: 677 year: 2000 ident: ref5 article-title: Basophil and eosinophil accumulation and mast cell degranulation in the nasal mucosa of patients with hay fever after local allergen provocation publication-title: The Journal of allergy and clinical immunology doi: 10.1067/mai.2000.109621 contributor: fullname: A KleinJan – volume: 75 start-page: 479 year: 1985 ident: ref6 article-title: Exercise-induced anaphylaxis: a serious form of physical allergy associated with mast cell degranulation publication-title: The Journal of allergy and clinical immunology doi: 10.1016/S0091-6749(85)80021-X contributor: fullname: AL Sheffer – volume: 128 start-page: 1153 year: 2011 ident: ref14 article-title: Regulation of the immune response and inflammation by histamine and histamine receptors publication-title: The Journal of allergy and clinical immunology doi: 10.1016/j.jaci.2011.06.051 contributor: fullname: L O’Mahony |
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Snippet | While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as bronchospasm and... Background While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as... Background While a number of the consequences of mast cell degranulation within tissues have been documented including tissue-specific changes such as... |
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SubjectTerms | Adolescent Adult Aged Allergies Antihistamines Bioengineering Biology Biopsy Blood Blood circulation Blood flow Bronchospasm Cell Degranulation - drug effects Cell Degranulation - physiology Cetirizine Child Child, Preschool Cold Cold Temperature Color temperature Colorimetry Comparative analysis Degranulation Dermatitis Edema Evolution Evolution (Biology) Female Hemodynamic responses Histamine Histamine - metabolism Histamine Antagonists - pharmacology Hives (Disease) Humans Immersion Immunology Infant Infectious diseases Inflammation Inflammatory response Infrared analysis Infrared imaging Infrared lasers Laboratories Lasers Male Mast Cells - metabolism Mast Cells - pathology Medicine Middle Aged Patients Recruitment Regional Blood Flow - drug effects Skin Skin - drug effects Skin - pathology Tissues Tryptase Tryptases - blood Urticaria Urticaria - physiopathology Vasodilation Young Adult |
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Title | Mast cell dependent vascular changes associated with an acute response to cold immersion in primary contact urticaria |
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