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      Effect of Antihelminthic Treatment on Vaccine Immunogenicity to a Seasonal Influenza Vaccine in Primary School Children in Gabon: A Randomized Placebo-Controlled Trial

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          Abstract

          Background

          Helminth infections are a major public health problem, especially in the tropics. Infected individuals have an altered immune response with evidence that antibody response to vaccination is impaired. Hence, treatment of helminth infections before vaccination may be a simple intervention to improve vaccine immunogenicity. In the present study we investigated whether a single-dose antihelminthic treatment influences antibody responses to a seasonal influenza vaccine in primary school children living in Gabon, Central Africa.

          Methods

          In this placebo-controlled double-blind trial conducted in Gabon the effect of a single-dose antihelminthic treatment with 400 mg albendazole versus a placebo one month prior to immunization with a seasonal influenza vaccine was investigated. Antiviral antibody titers against all three vaccine strains were assessed by haemagglutination inhibition (HI) test at baseline (Day 0; vaccination) and four weeks (Day 28) as well as 12 weeks (Day 84) following vaccination. Vaccine-specific memory B-cell response was measured at Day 0 and Day 84 by vaccine-specific Enzyme-linked Immunospot (ELISpot) assay. The trial is registered with the Pan African Clinical Trials Registry (PACTR) (PACTR201303000434188).

          Results

          98 school children aged 6–10 years were randomly allocated to receive either antihelminthic treatment or placebo and were vaccinated one month after the treatment. The prevalence of helminths at baseline was 21%. Vaccine-specific HI titers against at least one of the three vaccine strains increased at Day 28 and Day 84 in all participants. HI titers against both influenza A strains as well as memory B-cell response were modestly higher in the antihelminthic treated group compared to the placebo group but the difference was not statistically significant. Total but not specific IgA was elevated in the antihelminthic treated group compared to the control group at Day 28.

          Conclusion

          In our setting antihelminthic treatment had no significant effect on influenza vaccine immunogenicity. A trend towards better antiviral and vaccine immunogenicity in the antihelminthic treated group encourages studies to be conducted with alternative treatment schedules or in populations with a higher helminth burden.

          Author Summary

          Helminth infections are a major health problem in the tropics and most affected are children. The parasites are able to influence the immune system from a T-helper 1 type response to a T-helper 2 type response. There is evidence that in infected individuals the immune response following vaccination is impaired. Thus pre-treatment with a single-dose of an antihelminthic treatment before vaccination could be a simple and cost-effective intervention to improve vaccine efficacy. In the present study we investigated whether a single-dose antihelminthic treatment with albendazole influences the vaccine outcome to a seasonal influenza vaccine in primary school children living in Gabon, Central Africa. We observed a trend towards a higher anti-viral antibody titer after vaccination in the pre-treated group compared to the placebo control group, albeit not statistical significant. Furthermore we detected a higher concentration of total IgA but not of vaccine-specific IgA. In conclusion, our findings show subtle effects of antihelminthic pre-treatment but are not conclusive enough to recommend a single-dose of albendazole before vaccination to improve vaccine immunogenicity but encourage to conduct further studies in endemic areas with other treatment regiments.

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          Most cited references36

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          Immune regulation by helminth parasites: cellular and molecular mechanisms.

          Immunology was founded by studying the body's response to infectious microorganisms, and yet microbial prokaryotes only tell half the story of the immune system. Eukaryotic pathogens--protozoa, helminths, fungi and ectoparasites--have all been powerful selective forces for immune evolution. Often, as with lethal protozoal parasites, the focus has been on acute infections and the inflammatory responses they evoke. Long-lived parasites such as the helminths, however, are more remarkable for their ability to downregulate host immunity, protecting themselves from elimination and minimizing severe pathology in the host.
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            Maintenance of serological memory by polyclonal activation of human memory B cells.

            Production of antibodies can last for a lifetime, through mechanisms that remain poorly understood. Here, we show that human memory B lymphocytes proliferate and differentiate into plasma cells in response to polyclonal stimuli, such as bystander T cell help and CpG DNA. Furthermore, plasma cells secreting antibodies to recall antigens are produced in vivo at levels proportional to the frequency of specific memory B cells, even several years after antigenic stimulation. Although antigen boosting leads to a transient increase in specific antibody levels, ongoing polyclonal activation of memory B cells offers a means to maintain serological memory for a human lifetime.
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              Detection of antibody to avian influenza A (H5N1) virus in human serum by using a combination of serologic assays.

              From May to December 1997, 18 cases of mild to severe respiratory illness caused by avian influenza A (H5N1) viruses were identified in Hong Kong. The emergence of an avian virus in the human population prompted an epidemiological investigation to determine the extent of human-to-human transmission of the virus and risk factors associated with infection. The hemagglutination inhibition (HI) assay, the standard method for serologic detection of influenza virus infection in humans, has been shown to be less sensitive for the detection of antibodies induced by avian influenza viruses. Therefore, we developed a more sensitive microneutralization assay to detect antibodies to avian influenza in humans. Direct comparison of an HI assay and the microneutralization assay demonstrated that the latter was substantially more sensitive in detecting human antibodies to H5N1 virus in infected individuals. An H5-specific indirect enzyme-linked immunosorbent assay (ELISA) was also established to test children's sera. The sensitivity and specificity of the microneutralization assay were compared with those of an H5-specific indirect ELISA. When combined with a confirmatory H5-specific Western blot test, the specificities of both assays were improved. Maximum sensitivity (80%) and specificity (96%) for the detection of anti-H5 antibody in adults aged 18 to 59 years were achieved by using the microneutralization assay combined with Western blotting. Maximum sensitivity (100%) and specificity (100%) in detecting anti-H5 antibody in sera obtained from children less than 15 years of age were achieved by using ELISA combined with Western blotting. This new test algorithm is being used for the seroepidemiologic investigations of the avian H5N1 influenza outbreak.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                8 June 2015
                June 2015
                : 9
                : 6
                : e0003768
                Affiliations
                [1 ]Institute of Tropical Medicine, University of Tübingen, Tübingen, Germany
                [2 ]Centre de Recherches Médicales de Lambaréné, Albert Schweitzer Hospital, Lambaréné, Gabon
                [3 ]Nationales Referenzzentrum für Influenza, Robert-Koch-Institut, Berlin, Germany
                [4 ]Leiden Medical University Center, Department of Parasitology, Leiden, The Netherlands
                George Washington University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: ME STA PGK MY. Performed the experiments: SBr ME STA SBe EB JFF BS TE BM MML. Analyzed the data: SBr ME TE BM. Contributed reagents/materials/analysis tools: ME STA BL BM AAA BS. Wrote the paper: SBr ME BM STA BS TE BL AAA MY PGK.

                [¤]

                Current address: Department of Medicine II, Klinikum Rechts der Isar, Technische Universität München, München, Germany

                Article
                PNTD-D-14-02124
                10.1371/journal.pntd.0003768
                4459874
                26053679
                c9a789cc-d3f2-453d-a4d5-a406faa8bcaa
                Copyright @ 2015

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                History
                : 8 December 2014
                : 17 April 2015
                Page count
                Figures: 7, Tables: 4, Pages: 17
                Funding
                The study was funded by the Bundesministerium für Bildung und Forschung (BMBF). The grant number is 01 KA 1009. The ministery can be found under the following url http://www.bmbf.de/. The author who received funding was ME. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Custom metadata
                All relevant data are within the paper and its Supporting Information file.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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