Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms

Abstract German cockroaches (Blattella germanica) can be both mechanical and biological (amplifying) vectors of enteric pathogens, including Salmonella enterica serovar Typhimurium (S. Typhimurium), which they acquire by feeding upon contaminated substances. Blattella germanica is also a gregarious...

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Main Authors: Madison Mond, Jose E. Pietri
Format: Article
Language:English
Published: Wiley 2023-05-01
Series:Ecology and Evolution
Subjects:
Online Access:https://doi.org/10.1002/ece3.10070
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author Madison Mond
Jose E. Pietri
author_facet Madison Mond
Jose E. Pietri
author_sort Madison Mond
collection DOAJ
description Abstract German cockroaches (Blattella germanica) can be both mechanical and biological (amplifying) vectors of enteric pathogens, including Salmonella enterica serovar Typhimurium (S. Typhimurium), which they acquire by feeding upon contaminated substances. Blattella germanica is also a gregarious species that shelters in groups and partakes in unique feeding behaviors such as conspecific coprophagy, necrophagy, and emetophagy. These properties create an interphase for potential horizontal transmission of pathogens among cockroach populations through the fecal‐oral route, which could in turn enhance transmission to humans and other animals. Here, we performed a series of experiments to determine: (1) whether horizontal transmission of S. Typhimurium infection takes place in B. germanica, (2) the prevalence of the phenomenon, and (3) the route(s) through which it may occur. We reveal that true horizontal transmission of S. Typhimurium occurs among B. germanica. That is, uninfected cockroaches acquire infection of the gut when co‐housed with orally infected conspecifics, albeit at low frequency. Furthermore, we provide definitive evidence that coprophagy and necrophagy are routes of transmission but could not exclude sharing of food or water as contributing routes. On the contrary, transmission by emetophagy appears less likely as oral regurgitates from infected cockroaches contained S. Typhimurium for less than one day after ingesting the bacteria. Together, our data enhance current understanding of the ecology of vector‐borne S. Typhimurium transmission by cockroaches, implicating conspecific horizontal transmission as a phenomenon that contributes to maintaining infected cockroach populations independently of contact with primary sources of the pathogen. Although the relative importance of horizontal transmission of pathogens in cockroaches in the field remains to be determined, these results also highlight the important role that food and water sources in the local environment may play in cockroach‐borne pathogen transmission and emphasize the importance of sanitation for not only abating infestations but also mitigating pathogen transmission.
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spelling doaj.art-aa4dd28024e74d25b4dfb516e32a9fb22023-07-20T08:50:55ZengWileyEcology and Evolution2045-77582023-05-01135n/an/a10.1002/ece3.10070Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanismsMadison Mond0Jose E. Pietri1Division of Basic Biomedical Sciences, Sanford School of Medicine University of South Dakota Vermillion South Dakota USADivision of Basic Biomedical Sciences, Sanford School of Medicine University of South Dakota Vermillion South Dakota USAAbstract German cockroaches (Blattella germanica) can be both mechanical and biological (amplifying) vectors of enteric pathogens, including Salmonella enterica serovar Typhimurium (S. Typhimurium), which they acquire by feeding upon contaminated substances. Blattella germanica is also a gregarious species that shelters in groups and partakes in unique feeding behaviors such as conspecific coprophagy, necrophagy, and emetophagy. These properties create an interphase for potential horizontal transmission of pathogens among cockroach populations through the fecal‐oral route, which could in turn enhance transmission to humans and other animals. Here, we performed a series of experiments to determine: (1) whether horizontal transmission of S. Typhimurium infection takes place in B. germanica, (2) the prevalence of the phenomenon, and (3) the route(s) through which it may occur. We reveal that true horizontal transmission of S. Typhimurium occurs among B. germanica. That is, uninfected cockroaches acquire infection of the gut when co‐housed with orally infected conspecifics, albeit at low frequency. Furthermore, we provide definitive evidence that coprophagy and necrophagy are routes of transmission but could not exclude sharing of food or water as contributing routes. On the contrary, transmission by emetophagy appears less likely as oral regurgitates from infected cockroaches contained S. Typhimurium for less than one day after ingesting the bacteria. Together, our data enhance current understanding of the ecology of vector‐borne S. Typhimurium transmission by cockroaches, implicating conspecific horizontal transmission as a phenomenon that contributes to maintaining infected cockroach populations independently of contact with primary sources of the pathogen. Although the relative importance of horizontal transmission of pathogens in cockroaches in the field remains to be determined, these results also highlight the important role that food and water sources in the local environment may play in cockroach‐borne pathogen transmission and emphasize the importance of sanitation for not only abating infestations but also mitigating pathogen transmission.https://doi.org/10.1002/ece3.10070cockroachcoprophagyemetophagynecrophagySalmonellatransmission
spellingShingle Madison Mond
Jose E. Pietri
Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms
Ecology and Evolution
cockroach
coprophagy
emetophagy
necrophagy
Salmonella
transmission
title Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms
title_full Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms
title_fullStr Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms
title_full_unstemmed Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms
title_short Horizontal transmission of Salmonella Typhimurium among German cockroaches and its possible mechanisms
title_sort horizontal transmission of salmonella typhimurium among german cockroaches and its possible mechanisms
topic cockroach
coprophagy
emetophagy
necrophagy
Salmonella
transmission
url https://doi.org/10.1002/ece3.10070
work_keys_str_mv AT madisonmond horizontaltransmissionofsalmonellatyphimuriumamonggermancockroachesanditspossiblemechanisms
AT joseepietri horizontaltransmissionofsalmonellatyphimuriumamonggermancockroachesanditspossiblemechanisms