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      Interleukin-10 and soil-transmitted helminth infections in Honduran children

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          Abstract

          Background

          Soil-transmitted helminths (STH) establish chronic infections in the human intestine. The host reacts to these infections with a dominant T-helper type 2 cell (Th2) response that while attempting to control the worm population, can also provide an anti-inflammatory environment favourable for parasite survival. Regulatory cytokine interleukin 10 (IL-10) has been proposed as a key molecule involved in the attenuation of chronic inflammation and the ensuing tolerance for these helminth parasites. The objective of this study was to determine whether STH-infected children from an endemic community had increased circulating IL-10 levels when compared to non-infected children.

          Results

          A total of 39 children (25 boys and 14 girls, 7–15 years of age) were enrolled in study. Utilizing the Kato-Katz method to detect intestinal helminthiases, 10 children were non-infected and 29 were harbouring STH infections by Ascaris lumbricoides, Trichuris trichiura and/or hookworms. Of the 29 infected children, 11 had single-species infections and 18 were polyparasitized with two or three STH species. Serum samples from all 39 children were tested for IL-10 serum concentrations, out of which 12 had undetectable levels while 27 had levels ranging from 0.4-105 pg/mL. Excluding extreme outlying values, 25 samples had IL-10 concentration values ranging from 0.4 -7.2 pg/mL. Differences in IL-10 levels among non-parasitized, monoparasitized, and polyparasitized groups were not statistically significant. However, children infected with any of the three STH species investigated had higher IL-10 levels than non-parasitized children (geometric means: 0.89 pg/mL vs. 0.74 pg/mL, p = 0.428). Similarly, polyparasitized children had higher IL-10 levels than both monoparasitized and non-parasitized children (1.04 pg/mL, 0.69 pg/mL, and 0.74 pg/mL, respectively, p = 0.481). A significant moderate negative correlation between IL-10 levels and children’s age was found, but no correlations were observed between IL-10 levels and intensity of infection by any of the parasite species investigated.

          Conclusions

          We found no strong evidence for an association between STH infection and serum IL-10 concentration levels. However, the trends identified here warrant further investigation. Additional research is needed to expand the current understanding of the immune response elicited by STH infections in children living in endemic communities.

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          Most cited references47

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          The role of IL-10 in immune regulation during M. tuberculosis infection.

          During gaseous exchange the lungs are exposed to a vast variety of pathogens, allergens, and innocuous particles. A feature of the lung immune response to lung-tropic aerosol-transmitted bacteria such as Mycobacterium tuberculosis (Mtb) is a balanced immune response that serves to restrict pathogen growth while not leading to host-mediated collateral damage of the delicate lung tissues. One immune-limiting mechanism is the inhibitory and anti-inflammatory cytokine interleukin (IL)-10. IL-10 is made by many hematopoietic cells and a major role is to suppress macrophage and dendritic cell (DC) functions, which are required for the capture, control, and initiation of immune responses to pathogens such as Mtb. Here, we review the role of IL-10 on bacterial control during the course of Mtb infection, from early innate to adaptive immune responses. We propose that IL-10 is linked with the ability of Mtb to evade immune responses and mediate long-term infections in the lung.
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            Role of interleukin 10 transcriptional regulation in inflammation and autoimmune disease.

            Interleukin 10 (IL-10) is a cytokine with potent anti-inflammatory properties that plays a central role in limiting host immune response to pathogens, thereby preventing damage to the host and maintaining normal tissue homeostasis. Dysregulation of IL-10 is associated with enhanced immunopathology in response to infection as well as increased risk for development of many autoimmune diseases. Thus a fundamental understanding of IL-10 gene expression is critical for our comprehension of disease progression and resolution of host inflammatory response. In this review, we discuss modes of regulation of IL-10 gene expression in immune effector cell types, including signal transduction, epigenetics, promoter architecture, and post-transcriptional regulation, and how aberrant regulation contributes to immunopathology and disease progression.
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              Association between parasite infection and immune responses in multiple sclerosis.

              To assess whether parasite infection is correlated with a reduced number of exacerbations and altered immune reactivity in multiple sclerosis (MS). A prospective, double-cohort study was performed to assess the clinical course and radiological findings in 12 MS patients presenting associated eosinophilia. All patients presented parasitic infections with positive stool specimens. In all parasite-infected MS patients, the eosinophilia was not present during the 2 previous years. Eosinophil counts were monitored at 3- to 6-month intervals. When counts became elevated, patients were enrolled in the study. Interleukin (IL)-4, IL-10, IL-12, transforming growth factor (TGF)-beta, and interferon-gamma production by myelin basic protein-specific peripheral blood mononuclear cells were studied using enzyme-linked immunospot (ELISPOT). FoxP3 and Smad7 expression were studied by reverse-transcriptase polymerase chain reaction. During a 4.6-year follow-up period, parasite-infected MS patients showed a significantly lower number of exacerbations, minimal variation in disability scores, as well as fewer magnetic resonance imaging changes when compared with uninfected MS patients. Furthermore, myelin basic protein-specific responses in peripheral blood showed a significant increase in IL-10 and TGF-beta and a decrease in IL-12 and interferon-gamma-secreting cells in infected MS patients compared with noninfected patients. Myelin basic protein-specific T cells cloned from infected subjects were characterized by the absence of IL-2 and IL-4 production, but high IL-10 and/or TGF-beta secretion, showing a cytokine profile similar to the T-cell subsets Tr1 and Th3. Moreover, cloning frequency of CD4+CD25+ FoxP3+ T cells was substantially increased in infected patients compared with uninfected MS subjects. Finally, Smad7 messenger RNA was not detected in T cells from infected MS patients secreting TGF-beta. Increased production of IL-10 and TGF-beta, together with induction of CD25+CD4+ FoxP3+ T cells, suggests that regulatory T cells induced during parasite infections can alter the course of MS.
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                Author and article information

                Contributors
                ana.sanchez@brocku.ca
                dm09yk@brocku.ca
                jgabrie@brocku.ca
                Journal
                BMC Res Notes
                BMC Res Notes
                BMC Research Notes
                BioMed Central (London )
                1756-0500
                25 February 2015
                25 February 2015
                2015
                : 8
                : 55
                Affiliations
                [ ]Department of Health Sciences, Faculty of Applied Health Sciences, Brock University, 500 Glenridge Avenue, St. Catharines, ON Canada L2S 3A1
                [ ]Department of Biological Sciences, Faculty of Mathematics and Sciences, Brock University, 500 Glenridge Avenue, St. Catharines, ON Canada L2S 3A1
                [ ]Department of Health Sciences, Faculty of Applied Health Sciences, Brock University, 500 Glenridge Avenue, St. Catharines, ON Canada L2S 3A1
                Article
                1019
                10.1186/s13104-015-1019-x
                4347577
                25888883
                bdd860b6-2acb-477f-a079-5c8ea25374fd
                © Sanchez et al.; licensee BioMed Central. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 4 July 2014
                : 13 February 2015
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2015

                Medicine
                soil-transmitted helminths,geohelminths,interleukin-10,th2-type response,children,honduras
                Medicine
                soil-transmitted helminths, geohelminths, interleukin-10, th2-type response, children, honduras

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