Transmission ecology of canine parvovirus in a multi-host, multi-pathogen system

Behdenna, Abdelkader; Lembo, Tiziana; Calatayud, Olga; Cleaveland, Sarah; Halliday, Jo E. B.; Packer, Craig; Lankester, Felix; Hampson, Katie; Craft, Meggan E.; Czupryna, Anna; Dobson, Andrew; Dubovi, Edward J.; Eblate, Ernest; Fyumagwa, Robert D.; Hopcraft, J. Grant C.; Mentzel, Christine; Mzimbiri, Imam; Sutton, David; Willett, Brian J.; Haydon, Daniel T.; Viana, Mafalda

doi:10.1098/rspb.2018.2772

Cited by 34 publications

(38 citation statements)

References 60 publications

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“…The latter explanation seems possible given that most parvoviruses causing disease in large cats have been described not as FPV but as CPV (58). Indeed, a recent analysis of long-term serological data to investigate the transmission ecology of CPV in the Serengeti ecosystem indicates that infection cycles in lions are coupled with those in dogs, providing some evidence of cross-species transmission (59). However, as CPV and FPV are antigenically similar and difficult to distinguish serologically, it is likely that seropositive lions were infected with FPV, complicating the interpretation of the serological data.…”

Section: Discussionmentioning

confidence: 99%

Carnivore Parvovirus Ecology in the Serengeti Ecosystem: Vaccine Strains Circulating and New Host Species Identified

Calatayud¹,

Esperón

Cleaveland

et al. 2019

J Virol

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Carnivore parvoviruses infect wild and domestic carnivores, and crossspecies transmission is believed to occur. However, viral dynamics are not well understood, nor are the consequences for wild carnivore populations of the introduction of new strains into wild ecosystems. To clarify the ecology of these viruses in a multihost system such as the Serengeti ecosystem and identify potential threats for wildlife conservation, we analyzed, through real-time PCR, 152 samples belonging to 14 wild carnivore species and 62 samples from healthy domestic dogs. We detected parvovirus DNA in several wildlife tissues. Of the wild carnivore and domestic dog samples tested, 13% and 43%, respectively, were positive for carnivore parvovirus infection, but little evidence of transmission between the wild and domestic carnivores was detected. Instead, we describe two different epidemiological scenarios with separate routes of transmission: first, an endemic feline parvovirus (FPV) route of transmission maintained by wild carnivores inside the Serengeti National Park (SNP) and, second, a canine parvovirus (CPV) route of transmission among domestic dogs living around the periphery of the SNP. Twelve FPV sequences were characterized; new host-virus associations involving wild dogs, jackals, and hyenas were discovered; and our results suggest that mutations in the fragment of the vp2 gene were not required for infection of different carnivore species. In domestic dogs, 6 sequences belonged to the CPV-2a strain, while 11 belonged to the CPV-2 vaccinederived strain. This is the first description of a vaccine-derived parvovirus strain being transmitted naturally. IMPORTANCE Carnivore parvoviruses are widespread among wild and domestic carnivores, which are vulnerable to severe disease under certain circumstances. This study furthers the understanding of carnivore parvovirus epidemiology, suggesting that feline parvoviruses are endemic in wild carnivores in the Serengeti National Park (SNP), with new host species identified, and that canine parvoviruses are present in the dog population living around the SNP. Little evidence of transmission of canine parvoviruses into wild carnivore species was found; however, the detection of vaccine-derived virus (described here for the first time to be circulating naturally in domestic dogs) highlights the importance of performing epidemiological research in the region.

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Section: Discussionmentioning

confidence: 99%

Carnivore Parvovirus Ecology in the Serengeti Ecosystem: Vaccine Strains Circulating and New Host Species Identified

Calatayud¹,

Esperón

Cleaveland

et al. 2019

J Virol

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“…Although this virus could be a direct descendant of older FPVs that have been circulating in HG for decades, this virus showed no evidence of genetic drift, which is peculiar for a virus that supposedly evolved in seclusion for a long time. Another introduction mechanism, such as spillover from domestic animals or from fur farms, should therefore be considered for this virus [41]. Indeed, three mink farms were reported active on Graham Island in HG between 1922 and 1940 that were situated in active settlements [64] and the FPV-positive marten was found just north of one of these settlements, Port Clements, killed crossing the road from the local landfill.…”

Section: Ecology and Evolution Of Parvoviruses In Insular Bcmentioning

confidence: 99%

“…This is especially important for viruses of carnivores, particularly those of potential significance for vulnerable insular populations and for domestic and captive animal health, as most of these pathogens are not restricted to one single host, and over 90% of domestic carnivore pathogens infect multiple hosts [39]. For multi-host pathogens, combining these methods with the study of host ecology is fundamental in defining cross-species transmission dynamics, determining how hosts enable pathogen persistence and identifying which hosts, among epidemiologically connected and susceptible populations, are crucial for this persistence [40,41].…”

Section: Introductionmentioning

confidence: 99%

Ecology and Infection Dynamics of Multi-Host Amdoparvoviral and Protoparvoviral Carnivore Pathogens

et al. 2020

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Amdoparvovirus and Protoparvovirus are monophyletic viral genera that infect carnivores. We performed surveillance for and sequence analyses of parvoviruses in mustelids in insular British Columbia to investigate parvoviral maintenance and cross-species transmission among wildlife. Overall, 19.1% (49/256) of the tested animals were parvovirus-positive. Aleutian mink disease virus (AMDV) was more prevalent in mink (41.6%, 32/77) than martens (3.1%, 4/130), feline panleukopenia virus (FPV) was more prevalent in otters (27.3%, 6/22) than mink (5.2%, 4/77) or martens (2.3%, 3/130), and canine parvovirus 2 (CPV-2) was found in one mink, one otter, and zero ermines (N = 27). Viruses were endemic and bottleneck events, founder effects, and genetic drift generated regional lineages. We identified two local closely related AMDV lineages, one CPV-2 lineage, and five FPV lineages. Highly similar viruses were identified in different hosts, demonstrating cross-species transmission. The likelihood for cross-species transmission differed among viruses and some species likely represented dead-end spillover hosts. We suggest that there are principal maintenance hosts (otters for FPV, raccoons for CPV-2/FPV, mink for AMDV) that enable viral persistence and serve as sources for other susceptible species. In this multi-host system, viral and host factors affect viral persistence and distribution, shaping parvoviral ecology and evolution, with implications for insular carnivore conservation.

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“…Chi‐squared tests of year–prevalence relationships supported three epidemic years for both viruses: ~1977, 1981 and 1994 for CDV and 1977, 1985 and 1992 for parvovirus (Packer et al, ). Subsequent Bayesian state‐space analysis of this data further confirmed these years as epidemic for CDV and parvovirus (Behdenna et al, ; Viana et al, ).…”

Section: Worked Examples: Modelling Lion Exposure Riskmentioning

confidence: 59%

How to make more from exposure data? An integrated machine learning pipeline to predict pathogen exposure

Fountain-Jones

Machado

Carver

et al. 2019

Journal of Animal Ecology

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Predicting infectious disease dynamics is a central challenge in disease ecology.Models that can assess which individuals are most at risk of being exposed to a pathogen not only provide valuable insights into disease transmission and dynamics but can also guide management interventions. Constructing such models for wild animal populations, however, is particularly challenging; often only serological data are available on a subset of individuals and nonlinear relationships between variables are common.2. Here we provide a guide to the latest advances in statistical machine learning to construct pathogen-risk models that automatically incorporate complex nonlinear relationships with minimal statistical assumptions from ecological data with missing data. Our approach compares multiple machine learning algorithms in a unified environment to find the model with the best predictive performance and uses game theory to better interpret results. We apply this framework on two major pathogens that infect African lions: canine distemper virus (CDV) and feline parvovirus.3. Our modelling approach provided enhanced predictive performance compared to more traditional approaches, as well as new insights into disease risks in a wild population. We were able to efficiently capture and visualize strong nonlinear patterns, as well as model complex interactions between variables in shaping exposure risk from CDV and feline parvovirus. For example, we found that lions were more likely to be exposed to CDV at a young age but only in low rainfall years.4. When combined with our data calibration approach, our framework helped us to answer questions about risk of pathogen exposure that are difficult to address with previous methods. Our framework not only has the potential to aid in predicting disease risk in animal populations, but also can be used to build robust predictive models suitable for other ecological applications such as modelling species distribution or diversity patterns. K E Y W O R D Sboosted regression trees, disease ecology, gradient boosting models, machine learning, model-agnostic methods, random forests, serology, support vector machines Plotting prevalence relationships across host age and time is an essential first step to start calibrating exposure models. When evaluating year-prevalence curves, spikes in prevalence in certain years may estimate the timing of likely epidemics, particularly when the yearprevalence curves of juveniles are considered (Figure 1; Packer et al., 1999). Knowledge of pathogen natural history (e.g. chronic vs. acute infection) and analyses such as chi-squared test that quantify temporal fluctuations can be used to support these estimates (Figure 1, | 1449Journal of Animal Ecology FOUNTAIN-JONES ET Al.

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Transmission ecology of canine parvovirus in a multi-host, multi-pathogen system

Cited by 34 publications

References 60 publications

Carnivore Parvovirus Ecology in the Serengeti Ecosystem: Vaccine Strains Circulating and New Host Species Identified

Carnivore Parvovirus Ecology in the Serengeti Ecosystem: Vaccine Strains Circulating and New Host Species Identified

Ecology and Infection Dynamics of Multi-Host Amdoparvoviral and Protoparvoviral Carnivore Pathogens

How to make more from exposure data? An integrated machine learning pipeline to predict pathogen exposure

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