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The Emergence of Parvoviruses of Carnivores Karin Hoelzer, Colin R

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The Emergence of Parvoviruses of Carnivores Karin Hoelzer, Colin R The emergence of parvoviruses of carnivores Karin Hoelzer, Colin R. Parrish To cite this version: Karin Hoelzer, Colin R. Parrish. The emergence of parvoviruses of carnivores. Veterinary Research, BioMed Central, 2010, 41 (6), 10.1051/vetres/2010011. hal-00903177 HAL Id: hal-00903177 https://hal.archives-ouvertes.fr/hal-00903177 Submitted on 1 Jan 2010 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Vet. Res. (2010) 41:39 www.vetres.org DOI: 10.1051/vetres/2010011 Ó INRA, EDP Sciences, 2010 Review article The emergence of parvoviruses of carnivores Karin HOELZER, Colin R. PARRISH* Baker Institute for Animal Health, Department of Microbiology and Immunology, Cornell University, College of Veterinary Medicine, Hungerford Hill Road, Ithaca, NY 14853, USA (Received 11 November 2009; accepted 10 February 2010) Abstract – The emergence of canine parvovirus (CPV) represents a well-documented example highlighting the emergence of a new virus through cross-species transmission. CPV emerged in the mid-1970s as a new pathogen of dogs and has since become endemic in the global dog population. Despite widespread vaccination, CPV has remained a widespread disease of dogs, and new genetic and antigenic variants have arisen and sometimes reached high frequency in certain geographic regions or throughout the world. Here we review our understanding of this emergence event and contrast it to what is known about the emergence of a disease in mink caused by mink enteritis virus (MEV). In addition, we summarize the evolution of CPV over the past 30 years in the global dog population, and describe the epidemiology of contemporary parvovirus infections of dogs and cats. CPV represents a valuable model for understanding disease emergence through cross-species transmission, while MEV provides an interesting comparison. canine parvovirus / mink enteritis virus / disease emergence / viral evolution Table of contents 1. Introduction........................................................................................................................................... 1 2. The parvoviruses of carnivores ............................................................................................................ 2 3. The emergence of MEV ....................................................................................................................... 3 4. The emergence of CPV ........................................................................................................................ 4 5. Continuing evolution and spread of CPV in the global dog population – the roles of capsid variants ........ 7 6. CPV infections of cats.......................................................................................................................... 9 7. Conclusions........................................................................................................................................... 10 1. INTRODUCTION related autonomous parvoviruses which we will refer to as ‘‘carnivore parvoviruses’’, canine par- Members of the parvovirus genus (i.e. auton- vovirus (CPV), feline panleukopenia virus omous parvoviruses, subfamily Parvovirinae) (FPV) and mink enteritis virus (MEV). Dogs infect a wide variety of mammalian hosts and mink are also hosts for other distantly including pigs, several members of the order related viruses in the same subfamily, including Carnivora (henceforth referred to as ‘‘carni- the minute virus of canines (also known as CPV vores’’) and various rodents, and are character- type-1 or canine minute virus) and Aleutian ized by more or less strict host specificity mink disease virus (AMDV) which belong to [13, 42]. Carnivores are infected by three closely the Bocavirus and Amdovirus genera, respec- tively. There appear to be no immunological, * Corresponding author: [email protected] epidemiological or pathological interactions This is an Open Access article distributed under the terms of the Creative Commons Attribution-Noncommercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits unrestricted use, distribution, and reproduction in any noncommercial medium, provided the original work is properly cited. Article published by EDP Sciences Vet. Res. (2010) 41:39 K. Hoelzer, C.R. Parrish between CPV-1 or AMDV and CPV, FPV or 2. THE PARVOVIRUSES OF CARNIVORES MEV respectively in their various hosts. Parvoviruses are non-enveloped viruses with Carnivore parvoviruses are endemic in most a capsid of about 25 nm in diameter, that pack- domestic and feral carnivore populations and age a single-stranded DNA genome of approx- they infect a variety of host species (see for imately 5 000 bases. The genomes are simple example [19, 21, 28, 62, 64, 67, 73, 77]). The and contain two large open reading frames related group of ‘‘FPV-like’’ viruses, which (ORF) as well some smaller or overlapping includes FPV, viruses from raccoons (termed genes, mostly generated by alternative splicing. RPV) and arctic foxes (termed blue fox parvo- In the conventional orientation, the right-hand virus (BFPV)), has been widespread for many ORF encodes the capsid proteins and the left- decades. ‘‘FPV-like’’ viruses infect various hand ORF encode the non-structural proteins hosts including domestic and wild cats, lions, (reviewed for example in [14]). Parvovirus tigers, leopards, cougars, lynx, civets, leopard capsids are highly antigenic and play major roles cats, arctic foxes and raccoons [7, 8, 19, 32, in determining viral host ranges and tissue tro- 64, 65, 74]. These viruses are all very similar, pisms (reviewed for example in [31]). The appear to be transmitted readily among these non-structural proteins are multi-functional and hosts, and form a monophyletic clade in phylo- required for viral gene expression and genome genetic analyses of the viral sequences [56, 66]. replication. Parvoviruses replicate using various However, FPV-like viruses do not spread components of the host cell DNA replication among dogs, which are infected only in thymus complex and, since they cannot induce mitosis, and bone marrow and therefore do not appear to only replicate in actively dividing cells [47]. allow onward transmission [68]. Several aspects of this replication scheme – As parvoviruses only infect actively dividing including the likely lack of involvement or host cells, the clinical manifestations of disease absence of some subunits of the host cell are strongly dependent on the age of the host, DNA polymerase complex, the rapid replication and symptoms are similar in wild and domestic of the genome, and the single-stranded nature animals [54]. In animals older than about of the parvovirus genome – lead to a lower 4 weeks, the virus mainly replicates in the tis- fidelity of parvovirus replication compared to sues containing proliferating cells, including that observed during cellular DNA replication the bone marrow, lymph nodes, the spleen in (reviewed in [25]). While parvoviruses of some cases, and the progenitor cells in the rodents and AMDV can establish long-lasting crypts of Lieberku¨hn in the intestine. Cytolysis or persistent infections, carnivore parvoviruses of bone marrow and other lymphoid cells leads are usually cleared within 10 days of infection, to lymphopenia or leukopenia, while loss of after which little residual viral DNA remains intestinal epithelial cells can lead to hemor- [1, 54, 59]. The immune response that protects rhagic enteritis, the most pronounced clinical animals against parvovirus infection is predom- symptoms associated with parvovirus infections inantly humoral, and antibodies efficiently neu- of carnivores. Lymphoid depletion can involve tralize most parvoviruses. The important role of loss of all myeloid progenitor cells, decreasing antibodies in protecting animals from infection the number of circulating thrombocytes, eryth- is emphasized by the effectiveness of maternal rocytes, granulocytes and mast cells. However, immunity, which is antibody mediated, and viral strain, individual host and host-species dif- which confers efficient protection against these ferences result in preferential tissue tropisms parvoviruses. Infections occur predominantly in and differential clinical symptoms, so that the young animals after maternal antibodies have manifestation of clinical disease can vary from declined to low levels, generally between 2 severe to subclinical. If animals survive the and 4 months of age depending on the maternal acute infection, complete recovery normally antibody titer and level of transfer. Cell medi- occurs. ated immunity clearly plays an important role Where maternal immunity is not present, in recovery from disease. infection of neonatal animals and fetuses may Page 2 of 13 (page number not for citation purpose) Emerging parvoviruses of carnivores Vet. Res. (2010) 41:39 occur. In those animals additional tissues can be regarding dosage, the most appropriate type of infected, and virus replication is seen in the vaccines to use in which wildlife species, the myocardium and/or cerebellum, leading to
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