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Distinctive cytokine, chemokine, and antibody responses in Echinococcus multilocularis-infected patients with cured, stable, or progressive disease

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Abstract

Metacestode larvae of the tapeworm Echinococcus multilocularis can cause alveolar echinococcosis (AE), a severe parasitic disease in man, which, if it remains untreated, may cause organ failure and death. Spontaneous and parasite antigen-induced cellular responses were studied in patients with cured, stable, and progressive AE to differentiate the response profiles between the distinct states of infection. Antibody reactivity was evaluated in AE patients with cured, stable, and progressive disease. The spontaneous cellular release of pro-inflammatory IL-31 and IL-33 was clearly depressed in all AE patients, while regulatory IL-27, anti-inflammatory SDF-1/CXCL12, and eosinophil granulocyte attracting Eotaxin-1, Eotaxin-2, and Eotaxin-3 (CCL11, CCL24, CCL26) were enhanced with disease progression. Such distinctive response profiles could be applied for monitoring of AE disease progression or regression. E. multilocularis metacestode (Em) antigens (entire metacestode EmAg as well as EmVesicles) stimulated in vitro IL-31, IL-33, Eotaxin-1, Eotaxin-3, and CXCL12 cytokine and chemokine responses, which were similarly present in all AE patient groups, while regulatory IL-27 was suppressed and pro-inflammatory Eotaxin-2 was enhanced. E. multilocularis metacestode-specific IgG1, IgG3, and IgE responses progressively diminished with regression from active to stable and cured AE. IgG2 and IgG4 reactivity remained similarly high in stable and progressive cases, and lessened only with cured AE. Antibody reactivity against E. multilocularis vesicle antigen distinctively separated between cured, stable, or progressive AE, with the exception of IgG4. In sum, the combined and longitudinal study of several cytokines and chemokines, together with the evaluation of E. multilocularis vesicle-specific antibody responses, should provide a better understanding of the immune response during progression and regression of AE, and may help to improve the staging of AE patients.

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Acknowledgments

This work was supported by the Baden-Württemberg Stiftung (Grant P-LS-AL2/06). Xiangsheng Huang was supported by the Chinese Scholarship Council.

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Institute for Tropical Medicine, University of Tübingen, Wilhelmstraße 27, 72074, Tübingen, Germany

    Xiangsheng Huang, Christian J. Lechner & Peter T. Soboslay

  2. Section of Infectious Diseases and Clinical Immunology, University of Ulm, Robert-Koch-Straße 8, 89081, Ulm, Germany

    Beate Grüner & Peter Kern

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  1. Xiangsheng Huang
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  2. Beate Grüner
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Correspondence to Peter T. Soboslay.

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Huang, X., Grüner, B., Lechner, C.J. et al. Distinctive cytokine, chemokine, and antibody responses in Echinococcus multilocularis-infected patients with cured, stable, or progressive disease. Med Microbiol Immunol 203, 185–193 (2014). https://doi.org/10.1007/s00430-014-0331-8

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