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      Interactions between the intestinal microbiome and helminth parasites

      review-article
      1 , 1 ,
      Parasite Immunology
      John Wiley and Sons Inc.
      helminths, intestinal bacteria, microbiota, nematodes

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          Summary

          Throughout evolution, both helminths and bacteria have inhabited our intestines. As intestinal helminths and bacteria inhabit the same environmental niche, it is likely that these organisms interact with, and impact on, each other. In addition, intestinal helminths are well known to alter intestinal physiology, permeability, mucous secretion and the production of antimicrobial peptides – all of which may impact on bacterial survival and spatial organization. Yet despite rapid advances in our understanding of host–intestinal bacteria interactions, the impact of helminths on this relationship has remained largely unexplored. Moreover, although intestinal helminths are generally accepted to possess potent immuno‐modulatory activity, it is unknown whether this capacity requires interactions with intestinal bacteria. We propose that this ‘ménage à trois’ situation is likely to have exerted a strong selective pressure on the development of our metabolic and immune systems. Whilst such pressures remain in developing countries, the eradication of helminths in industrialized countries has shifted this evolutionary balance, possibly underlying the increased development of chronic inflammatory diseases. Thus, helminth–bacteria interactions may represent a key determinant of healthy homoeostasis.

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          Most cited references29

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          Interactions between commensal intestinal bacteria and the immune system.

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            Lymphatic filariasis and onchocerciasis.

            Lymphatic filariasis and onchocerciasis are parasitic helminth diseases that constitute a serious public health issue in tropical regions. The filarial nematodes that cause these diseases are transmitted by blood-feeding insects and produce chronic and long-term infection through suppression of host immunity. Disease pathogenesis is linked to host inflammation invoked by the death of the parasite, causing hydrocoele, lymphoedema, and elephantiasis in lymphatic filariasis, and skin disease and blindness in onchocerciasis. Most filarial species that infect people co-exist in mutualistic symbiosis with Wolbachia bacteria, which are essential for growth, development, and survival of their nematode hosts. These endosymbionts contribute to inflammatory disease pathogenesis and are a target for doxycycline therapy, which delivers macrofilaricidal activity, improves pathological outcomes, and is effective as monotherapy. Drugs to treat filariasis include diethylcarbamazine, ivermectin, and albendazole, which are used mostly in combination to reduce microfilariae in blood (lymphatic filariasis) and skin (onchocerciasis). Global programmes for control and elimination have been developed to provide sustained delivery of drugs to affected communities to interrupt transmission of disease and ultimately eliminate this burden on public health. Copyright © 2010 Elsevier Ltd. All rights reserved.
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              Use of axenic animals in studying the adaptation of mammals to their commensal intestinal microbiota.

              Vertebrates are essentially born germ-free but normally acquire a complex intestinal microbiota soon after birth. Most of these organisms are non-pathogenic to immunocompetent hosts; in fact, many are beneficial, supplying vitamins for host nutrition and filling the available microbiological niche to limit access and consequent pathology when pathogens are encountered. Thus, mammalian health depends on mutualism between host and flora. This is evident in inflammatory conditions such as inflammatory bowel disease, where aberrant responses to microbiota can result in host pathology. Studies with axenic (germ-free) or deliberately colonised animals have revealed that commensal organisms are required for the development of a fully functional immune system and affect many physiological processes within the host. Here, we describe the technical requirements for raising and maintaining axenic and gnotobiotic animals, and highlight the extreme diversity of changes within and beyond the immune system that occur when a germ-free animal is colonized with commensal bacteria.
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                Author and article information

                Journal
                Parasite Immunol
                Parasite Immunol
                10.1111/(ISSN)1365-3024
                PIM
                Parasite Immunology
                John Wiley and Sons Inc. (Hoboken )
                0141-9838
                1365-3024
                23 December 2015
                January 2016
                : 38
                : 1 , Highlight on Microbiome, Parasites and Immunity ( doiID: 10.1111/pim.2016.38.issue-1 )
                : 5-11
                Affiliations
                [ 1 ] Global Health InstituteÉcole Polytechnique Fédérale de Lausanne (EPFL) LausanneSwitzerland
                Author notes
                [*] [* ] Correspondence: Nicola L. Harris, Laboratory of Intestinal Immunology, Global Health Institute, Department of Life Sciences, École Polytechnique Fédérale de Lausanne, EPFL, Station 19, 1015 Lausanne, Switzerland (e‐mail: nicola.harris@ 123456epfl.ch )
                Article
                PIM12274
                10.1111/pim.12274
                5019230
                26345715
                be154247-cd1a-465c-91f0-331266fbfe63
                © 2015 The Authors. Parasite Immunology Published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution‐NonCommercial‐NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 15 May 2015
                : 01 September 2015
                Page count
                Pages: 7
                Funding
                Funded by: European Union's Seventh Framework Programme
                Award ID: FP/2007‐2013
                Funded by: ERC Grant Agreement
                Award ID: 310948
                Categories
                Review Article
                Review Articles
                Custom metadata
                2.0
                pim12274
                January 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.4 mode:remove_FC converted:12.09.2016

                Immunology
                helminths,intestinal bacteria,microbiota,nematodes
                Immunology
                helminths, intestinal bacteria, microbiota, nematodes

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