Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice.
The world health organization estimates that more than a quarter of the human population is infected with parasitic worms that are called helminths. Many helminths suppress the immune system of their hosts to prolong their survival. This helminth-induced immunosuppression "spills over" to...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-01-01
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| Series: | PLoS ONE |
| Online Access: | https://doi.org/10.1371/journal.pone.0266456 |
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| author | Wiebke Hartmann Marie-Luise Brunn Nadine Stetter Gülsah Gabriel Minka Breloer |
| author_facet | Wiebke Hartmann Marie-Luise Brunn Nadine Stetter Gülsah Gabriel Minka Breloer |
| author_sort | Wiebke Hartmann |
| collection | DOAJ |
| description | The world health organization estimates that more than a quarter of the human population is infected with parasitic worms that are called helminths. Many helminths suppress the immune system of their hosts to prolong their survival. This helminth-induced immunosuppression "spills over" to unrelated antigens and can suppress the immune response to vaccination against other pathogens. Indeed, several human studies have reported a negative correlation between helminth infections and responses to vaccinations. Using mice that are infected with the parasitic nematode Litomosoides sigmodontis as a model for chronic human filarial infections, we reported previously that concurrent helminth infection impaired the vaccination-induced protection against the human pathogenic 2009 pandemic H1N1 influenza A virus (2009 pH1N1). Vaccinated, helminth-infected mice produced less neutralizing, influenza-specific antibodies than vaccinated naïve control mice. Consequently helminth-infected and vaccinated mice were not protected against a challenge infection with influenza virus but displayed high virus burden in the lung and a transient weight loss. In the current study we tried to improve the vaccination efficacy using vaccines that are licensed for humans. We either introduced a prime-boost vaccination regimen using the non-adjuvanted anti-influenza vaccine Begripal or employed the adjuvanted influenza vaccine Fluad. Although both strategies elevated the production of influenza-specific antibodies and protected mice from the transient weight loss that is caused by an influenza challenge infection, sterile immunity was not achieved. Helminth-infected vaccinated mice still had high virus burden in the lung while non-helminth-infected vaccinated mice rapidly cleared the virus. In summary we demonstrate that basic improvements of influenza vaccination regimen are not sufficient to confer sterile immunity on the background of helminth-induced immunosuppression, despite amelioration of pathology i.e. weight loss. Our findings highlight the risk of failed vaccinations in helminth-endemic areas, especially in light of the ongoing vaccination campaign to control the COVID-19 pandemic. |
| first_indexed | 2024-04-14T00:00:29Z |
| format | Article |
| id | doaj.art-a6796fae088240d29363374a54ecf60a |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-04-14T00:00:29Z |
| publishDate | 2022-01-01 |
| publisher | Public Library of Science (PLoS) |
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| series | PLoS ONE |
| spelling | doaj.art-a6796fae088240d29363374a54ecf60a2022-12-22T02:23:43ZengPublic Library of Science (PLoS)PLoS ONE1932-62032022-01-01173e026645610.1371/journal.pone.0266456Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice.Wiebke HartmannMarie-Luise BrunnNadine StetterGülsah GabrielMinka BreloerThe world health organization estimates that more than a quarter of the human population is infected with parasitic worms that are called helminths. Many helminths suppress the immune system of their hosts to prolong their survival. This helminth-induced immunosuppression "spills over" to unrelated antigens and can suppress the immune response to vaccination against other pathogens. Indeed, several human studies have reported a negative correlation between helminth infections and responses to vaccinations. Using mice that are infected with the parasitic nematode Litomosoides sigmodontis as a model for chronic human filarial infections, we reported previously that concurrent helminth infection impaired the vaccination-induced protection against the human pathogenic 2009 pandemic H1N1 influenza A virus (2009 pH1N1). Vaccinated, helminth-infected mice produced less neutralizing, influenza-specific antibodies than vaccinated naïve control mice. Consequently helminth-infected and vaccinated mice were not protected against a challenge infection with influenza virus but displayed high virus burden in the lung and a transient weight loss. In the current study we tried to improve the vaccination efficacy using vaccines that are licensed for humans. We either introduced a prime-boost vaccination regimen using the non-adjuvanted anti-influenza vaccine Begripal or employed the adjuvanted influenza vaccine Fluad. Although both strategies elevated the production of influenza-specific antibodies and protected mice from the transient weight loss that is caused by an influenza challenge infection, sterile immunity was not achieved. Helminth-infected vaccinated mice still had high virus burden in the lung while non-helminth-infected vaccinated mice rapidly cleared the virus. In summary we demonstrate that basic improvements of influenza vaccination regimen are not sufficient to confer sterile immunity on the background of helminth-induced immunosuppression, despite amelioration of pathology i.e. weight loss. Our findings highlight the risk of failed vaccinations in helminth-endemic areas, especially in light of the ongoing vaccination campaign to control the COVID-19 pandemic.https://doi.org/10.1371/journal.pone.0266456 |
| spellingShingle | Wiebke Hartmann Marie-Luise Brunn Nadine Stetter Gülsah Gabriel Minka Breloer Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice. PLoS ONE |
| title | Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice. |
| title_full | Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice. |
| title_fullStr | Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice. |
| title_full_unstemmed | Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice. |
| title_short | Pre-existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice. |
| title_sort | pre existing helminth infection impairs the efficacy of adjuvanted influenza vaccination in mice |
| url | https://doi.org/10.1371/journal.pone.0266456 |
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