Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivo

Abstract Background Effective strategies are urgently needed to control Campylobacteriosis, one of the most important foodborne gastrointestinal diseases worldwide. Administering bacteriophages (phages) is under evaluation as a possible intervention strategy in primary poultry production to reduce t...

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Main Authors: Elisa Peh, Vanessa Szott, Benjamin Reichelt, Anika Friese, Uwe Rösler, Madeleine Plötz, Sophie Kittler
Format: Article
Language:English
Published: BMC 2023-08-01
Series:BMC Microbiology
Subjects:
Online Access:https://doi.org/10.1186/s12866-023-02963-1
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author Elisa Peh
Vanessa Szott
Benjamin Reichelt
Anika Friese
Uwe Rösler
Madeleine Plötz
Sophie Kittler
author_facet Elisa Peh
Vanessa Szott
Benjamin Reichelt
Anika Friese
Uwe Rösler
Madeleine Plötz
Sophie Kittler
author_sort Elisa Peh
collection DOAJ
description Abstract Background Effective strategies are urgently needed to control Campylobacteriosis, one of the most important foodborne gastrointestinal diseases worldwide. Administering bacteriophages (phages) is under evaluation as a possible intervention strategy in primary poultry production to reduce the public health risk of human infection. A major challenge is the translation of results from small-scale animal studies to large broiler flocks. In this study, the in vitro lytic activity of 18 Campylobacter-specific group II phages and 19 group III phages were examined singly, and in different combinations from the same group and from both groups using a planktonic killing assay. Based on these results, a combination of phage NCTC 12,673 (group III) and vB_CcM-LmqsCPL1/1 (group II) was selected for in vivo application in a seeder bird model to study its effectiveness under conditions as close as possible to field conditions. One hundred eighty Ross 308 broiler chickens were divided into a control and a treatment group. Ten days post hatch, seeder birds were orally inoculated with the C. jejuni target strain. Phages were administered via drinking water at a total concentration of 107 PFU/mL four, three, and two days before necropsy. Results Combining group II and group III phages resulted in significantly higher in vitro growth inhibition against the C. jejuni target strain BfR-CA-14,430 than single application or combinations of phages from the same group. The results of the animal trial showed that the application of the two phages significantly reduced Campylobacter counts in cloacal swabs. At necropsy, Campylobacter counts in colonic content of the treatment group were significantly reduced by 2 log10 units compared to the control group. Conclusions We demonstrated that combining phages of groups II and III results in significantly increased lytic activities. The in vitro results were successfully translated into practical application in a study design close to field conditions, providing new data to apply phages in conventional broiler flocks in the future. Phage application reduced the fecal Campylobacter excretion and Campylobacter concentrations in the colon of broilers.
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spelling doaj.art-85e1bd5550b0441eb28315c3a05dfadb2023-11-19T12:33:08ZengBMCBMC Microbiology1471-21802023-08-0123111210.1186/s12866-023-02963-1Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivoElisa Peh0Vanessa Szott1Benjamin Reichelt2Anika Friese3Uwe Rösler4Madeleine Plötz5Sophie Kittler6Institute for Food Quality and Food Safety, University of Veterinary Medicine HannoverInstitute of Food Safety and Food Hygiene, Freie Universität BerlinInstitute for Animal Hygiene and Environmental Health, Freie Universität BerlinInstitute for Animal Hygiene and Environmental Health, Freie Universität BerlinInstitute for Animal Hygiene and Environmental Health, Freie Universität BerlinInstitute for Food Quality and Food Safety, University of Veterinary Medicine HannoverInstitute for Food Quality and Food Safety, University of Veterinary Medicine HannoverAbstract Background Effective strategies are urgently needed to control Campylobacteriosis, one of the most important foodborne gastrointestinal diseases worldwide. Administering bacteriophages (phages) is under evaluation as a possible intervention strategy in primary poultry production to reduce the public health risk of human infection. A major challenge is the translation of results from small-scale animal studies to large broiler flocks. In this study, the in vitro lytic activity of 18 Campylobacter-specific group II phages and 19 group III phages were examined singly, and in different combinations from the same group and from both groups using a planktonic killing assay. Based on these results, a combination of phage NCTC 12,673 (group III) and vB_CcM-LmqsCPL1/1 (group II) was selected for in vivo application in a seeder bird model to study its effectiveness under conditions as close as possible to field conditions. One hundred eighty Ross 308 broiler chickens were divided into a control and a treatment group. Ten days post hatch, seeder birds were orally inoculated with the C. jejuni target strain. Phages were administered via drinking water at a total concentration of 107 PFU/mL four, three, and two days before necropsy. Results Combining group II and group III phages resulted in significantly higher in vitro growth inhibition against the C. jejuni target strain BfR-CA-14,430 than single application or combinations of phages from the same group. The results of the animal trial showed that the application of the two phages significantly reduced Campylobacter counts in cloacal swabs. At necropsy, Campylobacter counts in colonic content of the treatment group were significantly reduced by 2 log10 units compared to the control group. Conclusions We demonstrated that combining phages of groups II and III results in significantly increased lytic activities. The in vitro results were successfully translated into practical application in a study design close to field conditions, providing new data to apply phages in conventional broiler flocks in the future. Phage application reduced the fecal Campylobacter excretion and Campylobacter concentrations in the colon of broilers.https://doi.org/10.1186/s12866-023-02963-1Phage therapyChickenCampylobacterSusceptibilityAntibacterialResistance
spellingShingle Elisa Peh
Vanessa Szott
Benjamin Reichelt
Anika Friese
Uwe Rösler
Madeleine Plötz
Sophie Kittler
Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivo
BMC Microbiology
Phage therapy
Chicken
Campylobacter
Susceptibility
Antibacterial
Resistance
title Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivo
title_full Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivo
title_fullStr Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivo
title_full_unstemmed Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivo
title_short Bacteriophage cocktail application for Campylobacter mitigation - from in vitro to in vivo
title_sort bacteriophage cocktail application for campylobacter mitigation from in vitro to in vivo
topic Phage therapy
Chicken
Campylobacter
Susceptibility
Antibacterial
Resistance
url https://doi.org/10.1186/s12866-023-02963-1
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