Cargando…

An epidemiological model for proliferative kidney disease in salmonid populations

BACKGROUND: Proliferative kidney disease (PKD) affects salmonid populations in European and North-American rivers. It is caused by the endoparasitic myxozoan Tetracapsuloides bryosalmonae, which exploits freshwater bryozoans and salmonids as hosts. Incidence and severity of PKD in brown trout popula...

Descripción completa

Detalles Bibliográficos
Autores principales: Carraro, Luca, Mari, Lorenzo, Hartikainen, Hanna, Strepparava, Nicole, Wahli, Thomas, Jokela, Jukka, Gatto, Marino, Rinaldo, Andrea, Bertuzzo, Enrico
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5011885/
https://www.ncbi.nlm.nih.gov/pubmed/27596616
http://dx.doi.org/10.1186/s13071-016-1759-z
_version_ 1782451913762013184
author Carraro, Luca
Mari, Lorenzo
Hartikainen, Hanna
Strepparava, Nicole
Wahli, Thomas
Jokela, Jukka
Gatto, Marino
Rinaldo, Andrea
Bertuzzo, Enrico
author_facet Carraro, Luca
Mari, Lorenzo
Hartikainen, Hanna
Strepparava, Nicole
Wahli, Thomas
Jokela, Jukka
Gatto, Marino
Rinaldo, Andrea
Bertuzzo, Enrico
author_sort Carraro, Luca
collection PubMed
description BACKGROUND: Proliferative kidney disease (PKD) affects salmonid populations in European and North-American rivers. It is caused by the endoparasitic myxozoan Tetracapsuloides bryosalmonae, which exploits freshwater bryozoans and salmonids as hosts. Incidence and severity of PKD in brown trout populations have recently increased rapidly, causing a decline in fish catches and local extinctions in many river systems. PKD incidence and fish mortality are known to be enhanced by warmer water temperatures. Therefore, environmental change is feared to increase the severity of PKD outbreaks and extend the disease range to higher latitude and altitude regions. We present the first mathematical model regarding the epidemiology of PKD, including the complex life-cycle of its causative agent across multiple hosts. METHODS: A dynamical model of PKD epidemiology in riverine host populations is developed. The model accounts for local demographic and epidemiological dynamics of bryozoans and fish, explicitly incorporates the role of temperature, and couples intra-seasonal and inter-seasonal dynamics. The former are described in a continuous-time domain, the latter in a discrete-time domain. Stability and sensitivity analyses are performed to investigate the key processes controlling parasite invasion and persistence. RESULTS: Stability analysis shows that, for realistic parameter ranges, a disease-free system is highly invasible, which implies that the introduction of the parasite in a susceptible community is very likely to trigger a disease outbreak. Sensitivity analysis shows that, when the disease is endemic, the impact of PKD outbreaks is mostly controlled by the rates of disease development in the fish population. CONCLUSIONS: The developed mathematical model helps further our understanding of the modes of transmission of PKD in wild salmonid populations, and provides the basis for the design of interventions or mitigation strategies. It can also be used to project changes in disease severity and prevalence because of temperature regime shifts, and to guide field and laboratory experiments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1759-z) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-5011885
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-50118852016-09-07 An epidemiological model for proliferative kidney disease in salmonid populations Carraro, Luca Mari, Lorenzo Hartikainen, Hanna Strepparava, Nicole Wahli, Thomas Jokela, Jukka Gatto, Marino Rinaldo, Andrea Bertuzzo, Enrico Parasit Vectors Research BACKGROUND: Proliferative kidney disease (PKD) affects salmonid populations in European and North-American rivers. It is caused by the endoparasitic myxozoan Tetracapsuloides bryosalmonae, which exploits freshwater bryozoans and salmonids as hosts. Incidence and severity of PKD in brown trout populations have recently increased rapidly, causing a decline in fish catches and local extinctions in many river systems. PKD incidence and fish mortality are known to be enhanced by warmer water temperatures. Therefore, environmental change is feared to increase the severity of PKD outbreaks and extend the disease range to higher latitude and altitude regions. We present the first mathematical model regarding the epidemiology of PKD, including the complex life-cycle of its causative agent across multiple hosts. METHODS: A dynamical model of PKD epidemiology in riverine host populations is developed. The model accounts for local demographic and epidemiological dynamics of bryozoans and fish, explicitly incorporates the role of temperature, and couples intra-seasonal and inter-seasonal dynamics. The former are described in a continuous-time domain, the latter in a discrete-time domain. Stability and sensitivity analyses are performed to investigate the key processes controlling parasite invasion and persistence. RESULTS: Stability analysis shows that, for realistic parameter ranges, a disease-free system is highly invasible, which implies that the introduction of the parasite in a susceptible community is very likely to trigger a disease outbreak. Sensitivity analysis shows that, when the disease is endemic, the impact of PKD outbreaks is mostly controlled by the rates of disease development in the fish population. CONCLUSIONS: The developed mathematical model helps further our understanding of the modes of transmission of PKD in wild salmonid populations, and provides the basis for the design of interventions or mitigation strategies. It can also be used to project changes in disease severity and prevalence because of temperature regime shifts, and to guide field and laboratory experiments. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13071-016-1759-z) contains supplementary material, which is available to authorized users. BioMed Central 2016-09-05 /pmc/articles/PMC5011885/ /pubmed/27596616 http://dx.doi.org/10.1186/s13071-016-1759-z Text en © The Author(s). 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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.
spellingShingle Research
Carraro, Luca
Mari, Lorenzo
Hartikainen, Hanna
Strepparava, Nicole
Wahli, Thomas
Jokela, Jukka
Gatto, Marino
Rinaldo, Andrea
Bertuzzo, Enrico
An epidemiological model for proliferative kidney disease in salmonid populations
title An epidemiological model for proliferative kidney disease in salmonid populations
title_full An epidemiological model for proliferative kidney disease in salmonid populations
title_fullStr An epidemiological model for proliferative kidney disease in salmonid populations
title_full_unstemmed An epidemiological model for proliferative kidney disease in salmonid populations
title_short An epidemiological model for proliferative kidney disease in salmonid populations
title_sort epidemiological model for proliferative kidney disease in salmonid populations
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5011885/
https://www.ncbi.nlm.nih.gov/pubmed/27596616
http://dx.doi.org/10.1186/s13071-016-1759-z
work_keys_str_mv AT carraroluca anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT marilorenzo anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT hartikainenhanna anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT strepparavanicole anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT wahlithomas anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT jokelajukka anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT gattomarino anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT rinaldoandrea anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT bertuzzoenrico anepidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT carraroluca epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT marilorenzo epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT hartikainenhanna epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT strepparavanicole epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT wahlithomas epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT jokelajukka epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT gattomarino epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT rinaldoandrea epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations
AT bertuzzoenrico epidemiologicalmodelforproliferativekidneydiseaseinsalmonidpopulations